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1 Department of Veterinary Microbiology, Western College of Veterinary Medicine, 52 Campus Dr., University of Saskatchewan, Saskatoon, Saskatchewan, S7N 5B4, Canada
2 United States Department of Agriculture, Agricultural Research Service, US National Parasite Collection, Animal Parasitic Disease Laboratory, BARC East No. 1180, 10300 Baltimore Avenue, Beltsville, Maryland 20705, USA
3 Corresponding author (email: emily.jenkins{at}usask.ca)
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Parelaphostrongylus odocoilei is a member of the Elaphostrongylinae (Family Protostrongylidae), which is comprised of two genera, Parelaphostrongylus (of North American origin) and Elaphostrongylus (of Eurasian origin) (Lankester, 2001). All protostrongylids undergo a similar life cycle, where first-stage larvae (L1) are shed in the feces of the mammalian definitive host, invade a gastropod intermediate host, and develop to third-stage larvae (L3) infective for another definitive host. The route of migration and target organ within the definitive host, usually a cervid, varies among the elaphostrongylines. Adults of P. odocoilei and Parelaphostrongylus andersoni are considered to be strictly muscle-dwelling, with a pattern of migration through the central nervous system (CNS) having either been secondarily lost or never acquired (Platt, 1984; Anderson, 2000). Adults of Parelaphostrongylus tenuis, the meningeal worm, establish in the CNS and cranial venous sinuses and do not invade the muscles. Adults of Elaphostrongylus spp. (E. rangiferi, E. cervi, and E. alces) travel through some aspect of the CNS before establishing in the skeletal musculature (Anderson, 2000; Lankester, 2001).
Elaphostrongylines with a neural migration can cause neurologic disease in "typical" or "atypical" definitive hosts, and eggs and larvae of all elaphostrongyline species travel via the venous circulation to the lungs, causing granulomatous interstitial pneumonia (Lankester, 2001). All elaphostrongylines have the potential to cause disease in individual hosts and can have effects at the population level (Anderson, 1972; Ball et al., 2001; Lankester, 2001). Based on clinical respiratory disease and lung pathology in both naturally and experimentally infected hosts (Brunetti, 1969; Platt and Samuel, 1978b; Pybus and Samuel, 1984a; Pybus et al., 1984; Kutz et al., 2001), P. odocoilei could be a significant pathogen in thinhorn sheep.
Using various gastropod intermediate hosts, the life cycle of P. odocoilei of cervid origin has been completed in mule deer (Odocoileus hemionus hemionus) (Platt and Samuel, 1978b; Pybus and Samuel, 1984b), black-tailed deer (O. hemionus columbianus) (Hobmaier and Hobmaier, 1934; Brunetti, 1969; Platt and Samuel, 1978b), and moose (Alces alces) (Platt and Samuel, 1978b). Attempts to infect white-tailed deer (Odocoileus virginianus) were only marginally successful, whereas domestic goats (Capra hircus) and domestic sheep (Ovis aries) seem to be refractory to infection (Platt and Samuel, 1978b; Pybus, 1983; Pybus and Samuel, 1984b; Kutz, unpubl. data). For the first time, we complete the life cycle and describe the pathogenesis of P. odocoilei in experimentally infected thinhorn sheep. This work has implications for understanding life history patterns among the Elaphostrongylinae and the significance of a newly discovered host-parasite relationship, P. odocoilei in thinhorn sheep.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Three captive Stone’s sheep (SS1, SS2, and SS3; Table 1
) were acquired from a zoo in June 2000 and housed individually (SS1) or together (SS2 and SS3) in concrete pens measuring 2.3 x 4 m at the Western College of Veterinary Medicine (WCVM), Saskatoon, Saskatchewan, Canada (52°07'N; 106°38'W). Four hand-raised thinhorn hybrids (O. dalli stonei x O. dalli dalli, TS4–TS7; Table 1), originally from a game ranch in Saskatchewan, were brought in from pasture in October 2003 and housed in pairs (TS4 with TS5, and TS6 with TS7) in concrete rooms measuring 3.4 x 4.5 m at WCVM. Animals had unlimited access to water, mineral blocks, and grass or alfalfa hay and were offered ruminant pellets daily (Landmark Feeds, Winnipeg, Manitoba) and browse as available. SS1, SS2, and SS3 were housed in natural lighting conditions, whereas TS4–TS7 had regulated photoperiods (12 hr light:12 hr dark). Housing and procedures were approved by the University of Saskatchewan Committee on Animal Care (protocol 2000–0040).
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For infection of SS1, first-stage larvae (L1) were obtained from four fecal samples collected in May 2000 from a Dall’s sheep population known to be infected with P. odocoilei and no other elaphostrongylines, in the Mackenzie Mountains, Northwest Territories (65°01'N; 127°35'W) (Kutz et al., 2001). For the other sheep, L1 were obtained from feces of SS1. Slugs (Deroceras laeve) were infected with L1 and, after 18–35 days at room temperature, infective third-stage larvae (L3) were harvested (Hoberg et al., 1995). Motile or tightly coiled L3 were hand-picked under a dissecting microscope and held in tap water at 4 C overnight. Sheep were fasted for 24 hr, anesthetized (protocol modified from Kutz et al., 2004), and infected with 200 L3 in 60 ml of tap water administered by dose syringe and gastric tube (9.5 mm outer diameter), which were immediately flushed with a minimum of 60 ml of water, then twice with 60 ml of air. Control animals (TS6 and TS7) received the same treatment, except no L3 were administered.
Parasitologic monitoring
For SS1 in the prepatent period (PPP), we used a funnel Baermann technique to examine twelve 20-g samples from feces collected over 24 hr every 4 days until 38 days postinfection (dpi), then every 2 days (Kutz et al., 1999). Otherwise, protostrongylid larvae were recovered from feces using modified beaker Baermann sedimentation and counted using an aliquot or total count method (Forrester and Lankester, 1997; Jenkins et al., 2005). Larvae per gram (LPG) of wet feces was calculated, and one to three 5-g samples from each fecal collection were air dried for at least 2 wk, and LPG of the dry feces was calculated. From each pair of infected sheep housed together in the PPP, we examined six to twelve 5-g samples from pooled feces collected over 24 hr every 2 days starting at 30–40 dpi. Once patency was established, SS2 and SS3 were separated for 24 hr, and TS4 and TS5 for 4–6 hr, every Monday and Thursday. Three 5-g samples were examined from feces collected from each sheep over the period of separation or over 24 hr every Monday and Thursday for SS1. From TS6 and TS7, we examined six 5-g samples from pooled feces collected over 24 hr once a week from 43 to 380 dpi.
TS4 and TS5 were treated with 200 µg/kg subcutaneous ivermectin (10 mg/ml, Ivomec®, Merial, Baie d’Urfe, Quebec, Canada) at 180, 278, and 292 dpi. One uninfected control sheep (TS6) was treated with ivermectin at the same dose and time as infected sheep. Following treatment, we examined six 5-g samples from feces pooled from TS4 and TS5 collected over 24 hr every Monday and Thursday until 361 dpi. If larvae were detected, samples were collected from individual animals to identify the source.
The ITS-2 regions of rDNA of L1 shed in feces from SS1, TS4, and TS5 were sequenced (Jenkins et al., 2005). Total worm counts were obtained for SS1, SS2, and SS3 (Kutz et al., 2001). Five or six adult male nematodes from each Stone’s sheep were fixed in 70% ethanol and 5% glycerol, cleared with lactophenol, and identified using standard morphometric techniques, including measurements of spicules and gubernacula.
Clinical monitoring
Sheep were observed daily by staff of the Animal Care Unit and at least twice a week by researchers. Animals with clinical signs were examined by researchers several times a day and at least once per episode by large animal clinicians from the WCVM. Clinical pathology, including complete blood counts (CBC) and serum chemistry, was performed by Prairie Diagnostic Services, WCVM, Saskatoon, Saskatchewan, Canada. The three Stone’s sheep (SS1–SS3) were anesthetized every 1–4 wk for monitoring changes in the lungs associated with P. odocoilei (reported elsewhere); body weight and blood were also obtained at these times. Starting at 2 wk before infection, TS4–TS7 were weighed every week. Starting at 6 wk before infection, blood for CBC was obtained every 1–2 mo from TS4–TS7 under manual restraint, with increased frequency during times of clinical illness (weekly) or following treatment (every 2 wk for 6 wk). Blood from TS4–TS7 for serum chemistry was obtained every 2–3 mo. TS4–TS7 were anesthetized for cerebrospinal fluid (CSF) taps at 61–64 dpi, for medical imaging at 140 dpi, and, for TS4 only, for magnetic resonance imaging of the spinal column at 223 dpi (anesthetic protocols modified from Kutz et al., 2004). After each procedure, TS4–TS7 were treated prophylactically with subcutaneous injections of 10 mg/kg tilmycosin (300 mg/ml, Micotil®, Provel, division of Eli-Lilly, Guelph, Ontario, Canada). Examination of CSF included differential white blood cell counts, total numbers of nucleated and red blood cells, and total protein. Serum and CSF from TS4–TS7 were analyzed using protein electrophoresis and an assay for specific antibody to excretory-secretory products of Parelaphostrongylus spp. (Ogunremi et al., 1999).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Before infection with P. odocoilei, dorsalspined larvae were not recovered from the feces of any sheep or from the feces of uninfected control sheep at any time in the study. Dorsalspined larvae were first detected in feces from infected sheep from 68 to 74 dpi (Table 1
). For SS1, larval shedding increased gradually in the first few weeks, reached a peak at 106 dpi, and then stabilized at a mean value of 6,117 LPG (wet weight) for a 2-mo plateau period (Table 1, Fig. 1). During this period, based on average daily production of 320 g of feces (wet weight), SS1 shed approximately two million larvae per day (120 million larvae in total). For TS4 and TS5, larval shedding increased exponentially in the first few weeks, reaching a peak between 95 and 110 dpi, then gradually decreased (Fig. 1).
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Sequences from L1 from SS1, TS4, and TS5 were identical to each other and to that of P. odocoilei (GenBank accession numbers AY648380, 648392, and 648393). Seventy-five adult nematodes were recovered from skeletal muscles of SS1 (38% recovery of infective dose of 200 L3), 27 from SS2 (13.5%), and 14 from SS3 (7%). Measurements of 17 adult male nematodes from SS1, SS2, and SS3 were within the range reported for P. odocoilei (Platt and Samuel, 1978a; Kutz et al., 2001). At least three voucher specimens from each Stone’s sheep were deposited at the United States National Parasite Collection, Beltsville, Maryland, USA (accession numbers 94891–94894, 95314, and 95315).
Clinical observations
Weight loss in SS1, SS2, and SS3 began at approximately 28 dpi and continued until death, at which point sheep had lost, respectively, 16%, 7%, and 13% of body weight at time of infection. Weight loss was observed initially in all thinhorn hybrids on confinement, but weights of control sheep (TS6 and TS7) stabilized at about 30 dpi, whereas infected sheep (TS4 and TS5) continued to lose weight until 85–99 dpi (Fig. 2), losing a maximum of 23% and 16% of body weight at the time of infection. The infected thinhorn hybrids reached their lowest weights shortly after patency and subsequently gained weight, corresponding with decreasing larval counts (Fig. 3). All thinhorn hybrids began to gain weight after 260 dpi (Fig. 2).
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). Increasing eosinophil counts correlated with spontaneous declines in larval shedding in TS4 and TS5 before treatment with ivermectin (Fig. 5). Fifteen days after the first treatment, counts peaked at 7.5 and 6.2 x 109 eosinophils/l (54% and 48% of total white blood cells), respectively, and then fell but rose again in TS5, which continued to shed larvae after the first treatment. After the second and third treatments, eosinophil counts in both TS4 and TS5 returned to baseline values (Fig. 4). Mildly elevated eosinophil counts in a control sheep (TS7) after 280 dpi probably reflect experimental infection with a gastrointestinal parasite. No abnormalities were observed in serum chemistry panels from any sheep.
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TS5 (infected) and TS6 (control) developed signs consistent with a mild bacterial pneumonia shortly after anesthesia at 0 dpi, but these resolved within 2–3 wk following antibiotic treatment. Otherwise, no clinical abnormalities were observed in TS4–TS7 until 54 dpi, when the two infected sheep (TS4 and TS5) developed depression and incoordination, had difficulty getting up and lying down, lay with hind, and sometimes fore, limbs in full extension, and assumed a "stacked up" posture (Fig. 6). If made to move, the animals frequently slipped and fell, and spontaneously crossed hind limbs when turning or trying to lie down. Both animals ground their teeth, and TS4 rubbed her head frequently. Treatment with an anti-inflammatory analgesic (1 mg/kg intramuscular [IM] flunixin meglumine, 50 mg/ml, CronyxinTM, Bioniche Animal Health Inc., Belleville, Ontario, Canada) at 55 and 67 dpi did not alleviate clinical signs. Examination by large animal clinicians, including specific tests of neurologic function (sensation, reflexes, placing reactions, gait) at 60 and 67 dpi established that signs were consistent with posterior ataxia, loss of conscious proprioception, increased extensor tone, exaggerated reflexes, and hyperesthesia. At 61 dpi, eosinophilic pleocytosis, hemorrhage, and increased total protein were present in CSF from infected (TS4 and TS5), but not control (TS6 and TS7), sheep (Table 2). There was an equivocal increase in the ß-globulin protein fraction in the CSF of TS4 and TS5, but not TS7 (not available for TS6), and no abnormalities were observed in serum protein profiles of any of the four sheep. Antibodies for Parelaphostrongylus spp. were detected in the cerebrospinal fluid and serum of infected, but not control, sheep. Neurologic signs stabilized at patency and subsequently disappeared until a mild recurrence in TS4, 20 days following the first treatment with ivermectin. At this time, this sheep also developed signs consistent with neurologic bladder dysfunction, with frequent (
1–2 min) posturing to urinate, spastically producing only a small amount of urine each time. The urinary abnormalities resolved within a few days, but this sheep dragged the dorsal surface of the right hind foot slightly until the end of the monitoring period. Onset of shedding of the winter coat, which began in April 2004 for the two control sheep (TS6 and TS7), was delayed until June–July 2004 for the two infected sheep (TS4 and TS5). Uninfected control sheep showed no clinical abnormalities at any time.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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The prepatent period in five thinhorn sheep (68–74 days) was longer than that reported for mule deer infected with up to 334 L3 of P. odocoilei (45–62 days), but similar to that reported in black-tailed deer and moose infected with 50–750 L3 of P. odocoilei (58–72 days) (Platt and Samuel, 1978b; Pybus and Samuel, 1984b). The pattern of larval shedding in thinhorn sheep was similar to that observed in mule deer infected with P. odocoilei, with larval counts increasing for the first 3–4 wk, peaking at 20–40 days after patency, then reaching a plateau or gradually declining over a period of weeks to months (Platt and Samuel, 1978b; Pybus and Samuel, 1984b). Differences in patterns and magnitude of larval shedding among sheep in the current study likely reflect individual variation in susceptibility or immunity. Stressors, such as fasting or anesthesia, were associated with transient peaks in larval shedding (Fig. 1); stress-related immunosuppression has been linked to increased shedding of larvae of E. rangiferi (Gaudernack et al., 1984).
Stone’s sheep infected with 200 L3 of P. odocoilei developed relative eosinophilia and weight loss, similar to the mild eosinophilia and overall loss of condition observed in mule deer fawns experimentally infected with 300 L3 of P. odocoilei (Pybus and Samuel, 1984a). Absolute eosinophilia in the two thinhorn hybrids was associated with a spontaneous decrease in larval counts as well as treatment-induced inflammatory destruction of parasites. Marked weight loss in the two thinhorn hybrids that developed neurologic signs could, in part, reflect muscle atrophy due to inactivity, whereas delayed shedding of the winter coat was likely a nonspecific indicator of poor health (Woolf and Kradel, 1973). Emaciation has been reported in other definitive hosts with naturally acquired infections of P. odocoilei (Brunetti, 1969; Pybus et al., 1984). Following treatment, infected sheep reached and even exceeded weights at time of infection, possibly, in part, because of seasonal effects; control sheep also gained weight at this time (Fig. 2).
Timing of the deaths of two experimentally infected Stone’s sheep (SS1 and SS3) and pathology associated with eggs and larvae of P. odocoilei in the lungs suggest that infection was at least a contributing factor. Fatal respiratory failure following exertion has been observed in a naturally infected Dall’s yearling with similar pulmonary lesions associated with P. odocoilei (Kutz, Bollinger, Jenkins, unpubl. data). Two mule deer experimentally infected with P. odocoilei developed clinical signs suggestive of gastroenteritis shortly after patency and had severe interstitial pneumonia on postmortem (Platt and Samuel, 1978b). Pybus and Samuel (1984a) found that all experimentally infected mule deer developed signs of respiratory distress at 20–25 days postpatency, with one animal dying at 49 days post-patency "with much hemorrhagic foam. . . discharged from the mouth and nares," similar to that observed in SS1.
Aspiration and stress associated with multiple anesthesias likely caused the bacterial pneumonia that led to euthanasia of one older Stone’s ewe (SS2). Mild bacterial pneumonia in two of four thinhorn hybrids following routine anesthesia, and transmission of bovine corona virus from nearby calves to the three Stone’s sheep (the first report of this pathogen in thinhorn sheep), reinforce the need for strict biosecurity for wildlife species kept in captivity.
This is the first report of a neurologic syndrome associated with P. odocoilei in any host species. Loss of conscious proprioception and increased extensor tone in the hind limbs are associated with lesions in the superficial dorsolateral funiculi of the spinal cord between T3 and L3, whereas hyperesthesia is associated with lesions of the dorsal roots (DeLahunta, 1983). Neurogenic bladder dysfunction (possibly reflex dyssynergia or detrussor hyperreflexia) of one thinhorn sheep following treatment can be linked to partial disruption of the long spinocerebellar tracts (superficial lateral funiculi) (Oliver et al., 1997), possibly due to inflammation associated with dying nematodes. The Stone’s ewe that was euthanized because of bacterial pneumonia first presented with unilateral lameness and staggering, which may have been ataxia or weakness; without a neurologic examination, the two cannot easily be differentiated. The clinical signs that we observed were similar to those described in both typical and atypical hosts infected with E. rangiferi (which localizes in the leptomeninges and sub-arachnoid space), or with Parelaphostrongylus tenuis (which invades the gray matter of the dorsal horns before migrating to the subdural space and venous sinuses) (Handeland, 1994; Pybus et al., 1996; Anderson, 2000; Lankester, 2001). Clinical signs of cerebrospinal parelaphostrongylosis and elaphostrongylosis are nonspecific, often multifocal, and difficult to localize (Anderson, 1968).
Clinical signs, as well as eosinophilic inflammation and hemorrhage in cerebrospinal fluid, would be considered diagnostic for cerebrospinal nematodiasis in domestic animals (Mayhew et al., 1976; DeLahunta, 1983). These findings in the thinhorn hybrids, combined with detection of parasite-specific antibody in the CSF (Dew et al., 1992), strongly suggest that P. odocoilei was present in the CNS and was the cause of inflammation in the subarachnoid space, leptomeninges, and superficial dorsal regions of the spinal cord and nerve roots. Onset of clinical signs at 20 days before patency and cessation at patency are consistent with transient migration of immature P. odocoilei through the CNS, similar to the route demonstrated for E. rangiferi (Hemmingsen et al., 1993) (Fig. 7). The recurrence of clinical signs and mild residual gait abnormalities in one animal following treatment suggests that, like E. rangiferi, some nematodes have prolonged residence in the CNS (Hemmingsen et al., 1993). Magnetic resonance imaging (MRI) of the spinal cord at this time did not reveal nematodes or lesions. MRI at the onset of clinical signs before patency might have been revealing (Wood et al., 1991) but was delayed until after treatment because animals would likely not have survived the necessary extended anesthesia.
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A neural migration for P. odocoilei and P. andersoni has, however, been suggested previously, based on the migration pattern of related parasites (Anderson, 1968) and because adults, eggs, and L1 of both "muscle-worm" species have been found in the epidural tissues and vertebral canals in experimentally infected deer (Pybus, 1983; Pybus and Samuel, 1984b). In early patency, two white-tailed deer experimentally infected with 5,000 L3 of P. andersoni, and in the PPP one mule deer infected with 300 L3 of P. andersoni, developed unilateral or bilateral posterior lameness and weakness as well as postural and gait abnormalities that, in retrospect, could be neurologic (Nettles and Prestwood, 1976; Pybus, 1983). Serial postmortem examinations of the CNS of experimentally infected hosts are needed to confirm the migration route of these "muscle-worms"; to our knowledge, such examinations have not been accomplished for P. odocoilei or P. andersoni in the PPP in any definitive host. No adult P. odocoilei were found on gross examination of the vertebral canal or neural parenchyma of the three experimentally infected Stone’s sheep examined after patency or from naturally infected Dall’s sheep (Jenkins, Kutz, and Veitch, unpubl. data); however, detection may depend on the stage of infection as well as techniques used for examination (Pybus and Samuel, 1984b). Further experimental work is needed to determine if neurologic signs occur in thinhorn sheep infected with P. odocoilei at doses and methods of exposure comparable to naturally acquired infections.
If detailed and timely examinations of the CNS of both experimentally and naturally infected hosts confirm the hypothesis that the "muscleworms" (P. andersoni and P. odocoilei) are neurotropic, the life history patterns and phylogeny of the elaphostrongylines may need to be revisited (Platt, 1984; Carreno and Lankester, 1994). Migration through the CNS followed by establishment in skeletal muscles may be the ancestral pattern, occurring in all species of Elaphostrongylus and, possibly, in P. odocoilei and P. andersoni. The CNS-only migration of P. tenuis may represent attenuation or loss of the ancestral pattern. If the "muscleworms" (P. andersoni and P. odocoilei) are neurotropic, this supports the alternative phylogeny outlined by Platt (1984), in which P. odocoilei is the sister of P. tenuis and P. andersoni. Further experimental work and molecular characterization are needed to resolve fully the phylogeny of the elaphostrongylines.
Treatment for protostrongylid parasites in bighorn sheep has been a common, if controversial, management intervention (Schmidt et al., 1979; Jones and Worley, 1997; Miller et al., 2000), and there has been significant interest in the feasibility of such treatment in thinhorn sheep. Following parenteral ivermectin, neurologic signs recurred and larval shedding ceased in one thinhorn hybrid infected with P. odocoilei. In the other thinhorn hybrid, which remained clinically normal following treatment, larval shedding was transiently suppressed but not eliminated, as reported in cervids infected with P. andersoni, P. tenuis, and E. cervi (Kocan, 1985; Watson, 1985; Samuel and Gray, 1988). An extended monitoring period (at least 69 days in the current study) was necessary to detect resumption of larval shedding. Multiple treatments with oral fenbendazole did not eliminate shedding of Protostrongylus spp. larvae in at least one naturally infected Stone’s sheep or in a thinhorn hybrid experimentally infected with Protostrongylus stilesi (Jenkins and Skific, unpubl. data). For these reasons, anthelmintic treatment may not be effective or realistic for translocations or health management of thinhorn sheep infected with protostrongylid parasites.
Mixed infections with both P. odocoilei and P. stilesi are common in Dall’s and Stone’s sheep in the Subarctic (Jenkins et al., 2005), and additive, or even synergistic, pulmonary pathology is likely (Petney and Andrews, 1998; Kutz et al., 2001). Bighorn sheep (Ovis canadensis) undergo allage die-offs due to respiratory disease (which may involve preexisting lung damage by protostrongylid lungworms), and thinhorn sheep are susceptible to fatal pneumonia (Foreyt et al., 1996; Jenkins et al., 2000). Thinhorn sheep inhabit a high-latitude, high-altitude environment and are subject to predation by wolves. Parasites that cause respiratory compromise at high-infection intensities (such as P. stilesi in bighorn sheep, and Echinococcus granulosus in moose) may increase the susceptibility of ungulates to such chase-predators (Uhazy et al., 1973; Messier et al., 1989). Also, if P. odocoilei causes even minor, transient neurologic signs in naturally infected thinhorn sheep, it could increase susceptibility to predation and falls in hazardous terrain. It would be interesting to compare health, fecundity, and causes of mortality in Dall’s sheep populations infected with both P. odocoilei and P. stilesi (e.g., in the Mackenzie Mountains, Northwest Territories) with nearby populations where only P. stilesi is present (e.g., in the Nahanni or Richardson Mountains, Northwest Territories) (Hoberg et al., 2002; Jenkins et al., 2005).
Dall’s sheep in the Mackenzie Mountains will soon share range with muskoxen (Ovibos moschatus moschatus) infected with U. pallikuukensis (Kutz et al., 2004). Although U. pallikuukensis does not establish in Dall’s sheep, it may "prime" a stronger immune response against migrating P. odocoilei, resulting in clinical disease. Although it is not known if muskoxen can be infected with P. odocoilei, muskoxen in the Richardson Mountains are naturally infected with P. stilesi from Dall’s sheep and, elsewhere, are susceptible to cerebrospinal elaphostrongylosis (Holt et al., 1990; Hoberg et al., 2002). Historical precedent for colonization of new host species by protostrongylid parasites (i.e., P. stilesi in muskoxen and P. odocoilei in thinhorn sheep) and the potential health consequences for naïve hosts warrant continued surveillance by wildlife managers.
The widespread geographic distribution, high prevalence, resistance to treatment, and the possibility of respiratory and neurologic disease indicate that P. odocoilei may constitute a significant emerging disease risk for thinhorn sheep. Because of its wide host range and the possibility of a neural migration, P. odocoilei should be considered a differential diagnosis for dorsalspined larvae in feces and cerebrospinal nematodiasis (often identified only on histopathology) in a number of ungulate hosts, including mule and black-tailed deer, caribou, moose, mountain goat, and bighorn and thinhorn sheep. Definitive diagnosis and differentiation from closely related elaphostrongylines require comparative morphology of adult nematodes or identification of larvae using validated molecular techniques.
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ACKNOWLEDGMENTS |
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LITERATURE CITED |
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Received for publication 15 December 2004.
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