DIiHllHHIHllWWWlHlWWW!”WWW ll|||UllilllllllllllllllIlillllllllllllllllllllllflll rHEs'als . 3 1293 00079 3996 LIBRARY Michigan Stau‘: University This is to certify that the thesis entitled Clinical Treatment of Meningeal Worm (Parelaphostrongylus Tennis) in White-Tailed Deer (Odocoileus Virginianus) with Albendazole presented by James Gerard Sikarskie has been accepted towards fulfillment of the requirements for M. S. Jag-win Department of Fisheries and Wildlife professor Date a/xa/r/ 0-7639 OVERDUE FINES: 25¢ per day per item RETURNING LIBRARY MATERIALS: -_ :. , Place in book return to remove 3 “My ‘ 4 charge from circulation records :frm fl-‘\\\\‘ s CLINICAL TREATMENT OF MENINGEAL WORM (PARELAPHOSTRONGYLUS TENUIS) IN WHITE-TAILED DEER (ODOCOILEUS VIRGINIANUS) WITH ALBENDAZOLE BY James Gerard Sikarskie A THESIS Submitted to Michigan State University in partial fulfillment of the requirements for the degree of MASTER OF SCIENCE Department of Fisheries and Wildlife 1981 ABSTRACT . CLINICAL TREATMENT OF MENINGBAL WORM (PARELAPHOSTRONGYLUS TENUIS) IN WHITE-TAILBD DEER (ODOCOILEUS VIRGINIANUS) WITH ALBENDAZOLB BY James Gerard Sikarskie This study was initiated to evaluate the efficacy of albendazole as an anthelmintic for clinical treatment of meningeal worm ,(‘Pare‘lczphostrongylus tennis) in white- tailed deer (Odocoileus virginianus). Although infection with this parasite is seldom manifested clinically in the normal host, the white-tailed deer, typically it causes a neurological disease which is often fatal in abnormal hosts such as moose (AZces alces), elk (Cervus canadeneis), and woodland caribou (Rangifer tarandus terraenovae), as well as domestic sheep and goats. It was felt that if an oral anthelmintic was found that could be used to treat hosts which serve as a reservoir of this parasite, it might have value as a management tool to assist reintroduction or establishment of moose and elk or other susceptible wild ruminants in areas inhabited by deer with meningeal worm. It would also be useful to help control the problem in areas where domestic and exotic animals are affected. James Gerard Sikarskie Two trials were conducted using captive reared white- tailed deer infected experimentally with meningeal worm. Parasite burden was established by performing daily Baermann fecal analyses on 2 gm samples from each deer. A 2-week treatment of albendazole at approximately 25 mg/kg of body weight in each of 2 daily feedings drapped fecal larval counts to zero, while counts in controls remained unaffected. Necropsy revealed live worms in the meninges of all deer 1 week after the end of treatment in trial I. Necropsy of trial II deer 1 month after treatment revealed only dead encapsulated worms in treated animals, while controls were infected with many live parasites. These results permit the conclusion that albendazole is effective against meningeal worm in white-tailed deer. ACKNOWLEDGEMENTS I wish to thank my major professor, Dr. Leslie Gysel, for the support and flexibility given me throughout my Master's program. I would like to express my gratitude to Dr. John Stuht of the Michigan Department of Natural Resources for his guidance and encouragement in helping design and carry out this research project. I also wish to thank the other members of my graduate committee, Dr. Jeffrey Williams and Dr. Rollin Baker, for their interest and assistance. Special thanks are due to the personnel of the Wildlife Laboratory at the Rose Lake Wildlife Research Center for their help and for the use of their research facilities. I also wish to.acknowledge Smith Kline Animal Health Products and thank them for their financial support and use of the drug Albendazole. Special thanks to Dr. Cecil Miller for suggestions on treatment and dosage. Finally, a Special heartfelt thanks goes to my wife, Mary Jo, for her support and encouragement in all aspects of my degree program. ii TABLE OF CONTENTS Page INTRODUCTION . . . . . . . . . . . . . . . . . . . . . 1 History . . . . P. tenuis in White- Tailed Deer. . . . P. tenuia in Abnormal Hosts . . . . . Ecology and Management of the Disease . . Albendazole as a Potential Management Tool. £001<>NH MATERIALS AND METHODS. . . . . . . . . . . . . . . . . 12 RESULTS. . . . . . . . . . . . . . . . . . . . . . . . 15 Trial I . . . . . . . . . . . . . . . . . . . . 15 Trial II. . . . . . . . . . . . . . . . . . . . 17 DISCUSSION . . . . . . . . . . . . . . . . . . . . . . 20 LIST OF REFERENCES . . . . . . . . . . . . . . . . . . 25 APPENDICES . . . . . . . . . . . . . . . . . . . . . . so iii Table A1 B1 C1 LIST OF TABLES Page Larval output in feces of white-tailed deer infected with meningeal worm. . . . . . . . . . 16 Appendices Consecutive daily counts of larvae per gram of feces in deer on albendazole study. . . . . . . 30 Uneaten feed in kg when fed 90% of free choice consumption in 2 daily feedings . . . . . . . . 32 Vital statistics of deer in albendazole study . 34 iv INTRODUCTION History The meningeal worm was first identified in white-tailed deer and named Pneumostrongylns tennis by Daugherty (1945). The parasite had a rather confusing taxonomic history because its larvae resembled those of several other meta- strongyle parasites and it was given new names as it was discovered in different hoSts. Whitlock (1952) found the parasite in Sheep and later (Whitlock, 1959) helped explain some of the confusion. Anderson (1972) brought the history up to date with an explanation of the transfer of the para- site to the genus PurelaphostrongyZns ‘by Pryadko and Boev in 1971. Some other synonyms occurring in the literature before this point are OdocoileostrongyZns tennis, EZapho- strongylns tennis, and Neurofilaria cornellensis. The problems caused by Parelaphostrongylns tennis were just as confusing. There was a neurological disease seen in moose for years, but the etiology was unknown and it was simply referred to as "moose sickness" or "moose disease." Smith (1964) tentatively determined it was caused by P. tennis, and in 1967 Smith and Archibald published that naturally occurring moose sickness was definitely caused 2 by the common deer meningeal worm. Much research was done in the 1960's on the development of the meningeal worm in its normal host, the white-tailed deer (Anderson, 1963, 1965a), and its development and effects in experimentally infected abnormal hosts (Anderson, 1964; Anderson et al., 1966). There was also increased interest in the effects white-tailed deer infected with P. tennis could have on other wild populations of artiodactylids (Anderson, 1965c, 1972). ' P. tennis in White-Tailed Deer Parelaphostrongylns tennis is a metastrongyle nematode. Metastrongyles are referred to as lungworms because they either reside in the lungs or have a stage of their life cycle passing through the lungs of their host. The parasite is acquired by a foraging deer ingesting slugs or snails containing third stage (L3) infective larvae. Lankester and Anderson (1968) showed that many species of land gastropods functioned as natural intermediate hosts. No aquatic snails were found to be infected, even though earlier studies (Anderson, 1963) showed that some could be infected experi- mentally. They also determined that infected snails could survive the winter and thus were a potential source of infec- tion early in the spring when the moisture favors the snails and deer are eagerly eating the new growth of vegetation. After ingestion the P. tennis larvae penetrate the bowel and make their way to the spinal cord, presumably by way of the nerves (Anderson, 1965a). They undergo development to adults 3 while migrating through the dorsal horns of the gray matter within the Spinal cord. They cause very little tissue reaction within the parenchyma of the spinal cord and normally by 40 days time move into the spinal subdural spaces, where they mature. Adult P. tennis migrate to the cranial region, where they reside in the venous sinuses and the subdural space. Females deposit eggs in venous blood vessels or surrounding tissues. These eggs can either embryonate within the cranium with larvae penetrating the venus sinuses and being carried to the lungs or be deposited directly within blood vessels and are carried to the lungs, where they form emboli and later embryonate. Larvae penetrate the alveolus,' are coughed up or ascend the respiratory tract and are swallowed, passing out in the feces. The length of time from ingestion of the infected snail until patency or passage of larvae in the feces is usually 82-91 days (Anderson, 1965a). First stage (L1) larvae passing out in the feces are usually within the mucous coat around the fecal pellet. Snails are attracted to the feces and the P. tennis larvae penetrate the foot of the snail or are ingested. They mature to L3 within 3-4 weeks at summer temperatures. Lankester and Anderson (1967) showed that first stage larvae can remain infective when frozen over winter but tend to wash out of the fecal pellet and are readily dispersed by high Spring water or heavy rainfall. P. tennis in Abnormal Hosts Although infection with this parasite is seldom mani- fested clinically in the normal host, the white-tailed deer (Anderson, 1963), it can cause a neurological disease which is often fatal in many abnormal hosts. Woolf et a1. (1977) gave a complete listing of the clinical signs associated with neurological disease in elk in Pennsylvania. Along with listlessness and decreased flight distance, there is general and lumbar weakness with ataxia and Staggering often accompanied by circling. These signs are caused by damage to the spinal cord and brain tissue and the resulting inflammation. They often progress to paralysis and death. Naturally infected white-tailed deer occupying the same range as susceptible abnormal host species have been Shown to be the source of these clinical problems under at least 3 types of management conditions. Probably the most common and important area is in management of wild populations of susceptible native cervids. Smith et al. (1964) and Anderson (1965b) were the first to expose the problem in moose. Anderson et a1. (1966) showed that mule deer (0. hemionns) were experimentally susceptible. In 1973 Pay and Stuht linked Pu tennis to neurological disease in elk in Michigan, and later Carpenter et a1. (1973) found P. tennis in elk in Oklahoma. 'Reindeer (Rangifer tarandns tarandns) (Anderson, 1971) and caribou (Trainer, 1973) are also affected by this disease under natural conditions. The second situation in which P. tennis has caused clinical disease is in exotic ruminants introduced in areas to which 5 infected wild white-tailed deer had access. Kistner et a1. (1977) and Nettles et a1. (1977) found fallow deer (Dama dama) with neurological disease caused by meningeal worm and Brown et a1. (1978) found the problem in llamas (Lama gnanicoe). The third important area of concern is cerebro- spinal parelaphostrongylosis in domestic animals. It was found as early as 1952 (Whitlock) in Sheep and written up by Nielsen and Aftosmis (1964) and found again in sheep by Alden et al. (1975). Parelaphostrongylus tennis has also caused neurological disease in goats on pastures used by infected white-tailed deer (Mayhew et al., 1976; Guthery et al., 1979). Ecology and Management of the Disease If an effective oral anthelmintic could be found, it might be used to treat the reservoir hosts in areas where managers are attempting introduction or reestablishment of susceptible species like moose and elk. It would.also be useful to treat white-tailed deer prior to translocation to “areas like the western 0.5. and Canada, which apparently do not have P. tennis, although some areas have white-tailed deer and there are many Species of land gastrOpods which could function as intermediate hosts. There are many poten- tially susceptible Species in western North America, and introduction of meningeal worm could have very grave conse- quences. This is especially true with the pressures that dwindling habitat have put on wild populations. Competition for limited range and forage would tend to bring susceptible 6 species into contact with infected white-tailed deer and could increase the potential for exposure. Anderson (1972) discussed the ecological relationship of meningeal worm in the adaptable white-tailed deer and the competitive advan- tages the parasite gives this Species over susceptible cervids. Management of moose. It is well documented with moose that habitat changes, such as logging, have increased deer populations and P. tennis has caused neurological disease decreasing moose numbers (Karns, 1967; Smith and Archibald, 1967). The implications of this deer-moose relationship have been studied extensively in Maine. Behrend and Witler (1968) found the Prevalence of P. tennis highest (100%) in white-tailed deer where populations were densest and expanding. This would indicate that greater density can facilitate spread of the parasite but that it does not seem to exert any major limitations on deer pOpulations. However, there have been a few naturally occurring cases of neurological disease in white-tailed deer (Alibasoglu et al., 1961; Bckroade et al., 1970; Prestwood, 1970). Gilbert's study (1973) of white-tailed deer and P. tennis in Maine did not always correlate rate of infection with deer density. This indicates other variables, such as habitat types and prevalence of snail intermediate hosts, must help influence rate of infection and transmission. Further Studies did, however, directly relate prevalence in moose to density of the deer population (Gilbert, 1974). 7 Kearney and Gilbert (1976) studied the ecological factors affecting transmission of P. tennis to moose and found that there are areas where white-tailed deer and moose can coexist on the same range. They showed that areas supplying optimum habitat for both moose and deer allowed some isolation by habitat preferences during the summer when Spread of the parasite is more likely to occur. Areas supplying these habitat configurations served as "refugia" or "refuges" for moose and helped maintain local papulations in areas where white-tailed deer with P. tennis existed., Anderson (1979, personal communication) feels this occurrence is exceptional and that the reason for the decline in moose pOpulations with the influx of deer in many areas is the fact that they have very similar habitat requirements and preferences and P. tennis helps the deer eliminate the moose. Management of elk. Much attention has been given to elk and the Similar problem they have surviving in areas inhabited by white-tailed deer with P. tennis. Moran (1973), in his thorough study of Rocky Mountain elk in Michigan, attributed much of the decline in elk numbers and reproduc- tive success to deterioration of habitat quality. He also felt that P. tennis and neurologic disease played a role in hindering the success of introduction, dispersion, and establishment of both moose and elk over the north-central range of the white-tailed deer. George et a1. (1974) did an in-depth study of the ecology of the remaining Rocky Mountain elk in Pennsylvania. They felt habitat quality was 8 not a major problem but that P. tennis was the most serious reason for the declining papulation. Further research on a captive herd of elk at the Rachelwood Wildlife Research Preserve in Pennsylvania by Woolf et al.‘(l977) showed a high prevalence of infection (26.6-64.3t of samples taken). Many individuals did not show obvious signs and they felt that even though there were no sudden or massive die-offs the parasite might be limiting the growth of the herd, especially by its detrimental effect on population recruitment with the apparently greater suscep- tibility of younger age classes. Further studies by Olsen and Woolf (1978) showed that neurologic disease may have other subtle detrimental effects on pOpulation dynamics besides causing death. It increases susceptibility to preda- tion.by natural means or harvest by man. It also may have a detrimental or disrupting effect on social organization within the herd and affect individual behavior such as breed- ‘ing, rut, calving, and maternal care. An update on prevalence in the herd in 1979 (Olsen and Woolf) showed the disease to be increasing. They explained some of the variability of prevalence from year to year possibly being due to changes in weather leading to variation in gastropod abundance and distribution and altered feeding behavior produced by annual variations in natural forage availability. Anderson (1972) Speculated that the eastern subspecies of elk which is now extinct may have been immune to P. tennis or even tolerated the parasite as well as the white-tailed deer. Other possibilities are that deer and elk coexisted 9 on the same range because habitat preferences and seasonal migration patterns reduced the potential for exposure. All these studies indicate that habitat manipulations and control of papulation density might be useful measures for manage- ment of this problem with moose and elk. Treatments utilizing a palatable oral anthelmintic with a wide margin of safety effective against P. tennis in the source of the problem, white-tailed deer, could also have an important role in modern wildlife management as well as management for exotic and domestic animals. Albendazole as a Potential Management Tool Albendazole is a newly developed benzimidazol anthel- mintic. It was chosen as a suitable drug to test against meningeal worm because of its known safety and efficacy against a broad spectrum of other parasites, such as lung- worms and liver flukes as well as intestinal parasites, in white-tailed deer (Foreyt and Drawe, 1978). In abnormal hosts, P. tennis larvae penetrate the gray matter in the dorsal horn of the Spinal cord and can cause much more tissue damage and inflammation than in their normal host. This phenomenon is generally true of migrating nematodes in abnormal hosts. Parelaphostrongylns tennis may also invade the brain as subadults or adults, causing the classical neurological disease already described. Brain tissue itself is selectively protected from circulating substances by the blood-brain barrier, so it was felt that systemic treatment in abnormal hosts where the parasite is often in the 10 parenchyma of the Spinal cord or brain might be less successful than in white-tailed deer, where the adult is associated with the venous sinuses in the subdural space. Diethylcarbamazine citrate, levamisole phosphate, and thiabendazole have been used to treat cerebrospinal par- elaphostrongylosis in goats (Mayhew et al., 1976); However, no conclusions concerning efficacy of these drugs could be drawn from these uncontrolled treatments because they were isolated clinical cases which may have recovered after running their natural course. It was also felt that an attempt at management by treating the source of the problem in the white-tailed deer would have more merit than treating the clinically affected abnormal host. Successful treatment would be hard to evaluate clinically, as nerve and brain damage heal Slowly, if at all. Also, the parasite does not usually complete its life“ cycle in the abnormal host, so larval output in the feces could not be monitored as an experimental parameter. There are some references in the literature on the presence of P. tennis larvae in the feces of abnormal hosts. Loken et al. (1965) demonstrated what they thought were meningeal worm larvae in feces from an infected Sick moose. Karns (1966) demonstrated larvae in what he thought was elk feces. Karns and Jordan (1969) found a low incidence of larvae identical to P. tennis in moose on Isle Royal and there had been no deer present for 30 years, so they felt the parasite was completing its life cycle in moose. Tompkins et al. (1977) found larvae that looked like P. tennis in 11 what they thought were elk feces in Michigan but felt that they could not say for sure they were P. tennis.' Larvae from P. andersoni, P. odoeoilei, and EZaphostrongyZns oervi all look like P. tennis and they could not rule out the existence of these other parasites in deer or elk in Michigan. There is some question as to whether P. tennis does complete its life cycle in abnormal hosts in the wild and no doubt that abnormal hosts are not an important reservoir of the parasite. Anderson (1966) experimentally infected an elk which shed P. tennis larvae in its feces 92 days after inoculation, which is the approximateprepatency period in the normal host. The elk showed some transient neurological symptoms but grew and developed normally. After reviewing the literature and evidence, it appears that under ideal conditions a low number of parasites (at least one male and one female) could complete their life cycle in the abnormal host. Typically, the parasite does not reach patency in any host but white-tailed deer because the inflam- matory changes caused by the migrating parasite kill either the host or the parasite before the life cycle can be com- pleted. It seems that a great potential exists for manage- ment of this problem if P. tennis could be controlled in white-tailed deer, thus eliminating or decreasing the risk of exposure to abnormal susceptible hosts. MATERIALS AND METHODS A noninfected white-tailed deer buck weighing approxi- mately 80 kg was given 8 gm of albendazole by eSOphageal intubation. This high dose of 100 mg/kg caused transient hemorrhagic diarrhea from 24-48 hours after treatment, but no other obvious problems. Histologic sections of many organs and several sites along the digestive tract appeared normal when the deer was sacrificed one week after treatment. An experimentally infected pregnant doe near term was dosed with 6,370 mg albendazole (100 mg/kg). Again, there was some transient hemorrhagic diarrhea the day following treat- ment, but no obvious decrease in larval output. The deer died during the second week after treatment from a clostridial infection at the tranquilizer dart injection site. Its fetus apparently died at the same time as the doe. ' Since a single high dose apparently failed, it was felt that a lower dose over a longer period of time would deter- mine if the drug was effective. A dose of 25 mg/kg tWice a day for 5 days was suggested by Smith Kline representatives, but to be sure the drug was given a chance, a 2-week treat- ment was decided on for the main research project. Snails (Triodopsis ngtiZineata) artificially infected with first Stage meningeal worm larvae which had been obtained from 12 13 deer at the Rachelwood Wildlife Refuge in Pennsylvania were used to infect the deer. Snails were crushed and digested for 4 hours in aBaermann apparatus at 37°C in a solution of l gmpepsin, 1.4 ml HCl, and 166 ml of distilled H20. The planned protocol was to inoculate each of four 6-month-old white~tailed deer fawns in 2 trials with 100 larvae. How- ever, only the healthiest and most active half of the snails were digested for trial I, yielding only enough larvae to give 62 third stage infective larvae to each deer. One month later, the rest of the snails, which had been main- tained in a terrarium with water, moisteneddog‘food,’lettuCe and chalk, were digested. At least 3,000 larvae were recovered and 5 available fawns were each inoCulated orally with 100 infective larvae. Apparently, decreased activity and unthriftiness of the snail might be an indication of greater parasite burden, although it is possible some larvae in the first group of snails had not yet reached the L3 stage and were killed by the digesting solution. Onset of larval production in the deer was monitored by weekly fecal examinations for the second half of the approxi- mately 90-day prepatency period for P. tennis. A standardized technique was used with 2 gm of fresh feces suspended on a singLe layer of tissue paper in 90 m1 of water in a Baermann funnel for 18 hours at room temperature. Fifteen milliliters were drawn off, resuspended and placed in a gridded petri dish 88 mm in diameter for counting under a dissecting micro- scope. Variations of volumes and times were tried and this method allowed nearly all larvae to settle out for easy 14 counting. Lankester and Anderson (1968) found that 83% of larvae left a submerged fecal pellet within the first 5 minutes of soaking. An inside and outside set of 4 grids (one from each quadrant) was counted for each examination -after vibration to randomize larvae. Treatment of the deer was carried out by including the dose of albendazole with double its volume of ViNaturaR (a natural honey apple flavored equine vitamin syrup made by Jensen-Salsbery Laboratories in Kansas City, Missouri) mixed with their normal diet of exotic ruminant pellets made by The Andersons of Maumee, Ohio. Free choice feed consump- tion was determined for each deer prior to treatment by averaging consumption over an 8- to 10-day period. Each deer was fed twice a day with 45% of its daily ad Zibitnm consumption of pellets with the ViNatura for 1 week prior to treatment. This was to get them accustomed to the ViNatura. It was also an attempt to equilibrate fecal out- put and thus larval counts to a Standard because decreased feed intake would lower fecal output and appear to increase larvalLoutput per gram of feces. Daily larval counts were determined before, during, and after the 2-week treatment (Appendix A). Uneaten feed was removed and weighed before the morning feeding each day (Appendix B). At the end of each trial deer were euthanatized with 20 mg of succinyl- choline chloride. The brain and cranial cavity were examined and worms counted. A 10 gm sample of the right apical lobe of the lung was macerated and examined for larvae by the same Baermannmethod used on the feces. RESULTS Trial I One of the deer in trial I died from overexertion due to harrassment by dogs near the pens. Of the remaining 3, 2 were treated and l was used as a control. The control, receiving food with ViNatura only, ate everything regularly, but 1 treated deer rejected feed completely after eating most of the first dose. This deer (No. 2) was offered the treated food for 1 week without consuming any, so it was returned to feed without albendazole for the rest of the study and immediately resumed eating, as seen in Appendix B. Larval output was followed during this period, even though the data could not be included with those from other treatedi deer. Counts went from less than 10,000 larvae/gm of feces before treatment to over 56,000 larvae/gm, then down to zero by the end of the second week. The deer had begun shedding a few larvae by the end of the week after treatment when all the animals were sacrificed. The other treated deer ate regularly, but almost never ate all of the drugged feed. Larval counts went to zero and remained there until the end of trial I. Average weekly larval counts for treatment and control animals were calculated and are shown for both trials in Table 1. On postmortem examination (data shown in 15 16 Table 1. Larval output in feces of white-tailed deer infected with meningeal worm Trial I. Larvae_per gm of feces Control 0 0 0 0 0 1921 1129 2575l2330 l67l|1199 1584 Treated 0 2 2 1 169 927 1214 4155|254Z 191| 8 0 Wk post- I l infection 12 13 14 15 I16 17 18 l9I 20 le 22 23 treat- ] ment I ,period Trial II. Larvae_per ga of feces Control ? 1298 742] 1088 £916|114S 12907 742 34 169 Treated ? 658 767! 2847 i103| 0 0 0 0 0 ‘Wk Post- I . I infection 20 21 22l 23 [ 24l 25 26 27 28 29 treatment 'period Figures were ca1Cu1ated by taking the daily counts and averaging for each week, then averaging counts for all control and treated animals for each trial. 17 Appendix C), live adult P. tennis were recovered from all 3 deer, although there were some dead encapsulated worms in the brain of the deer which accepted treatment. Baermann examinations of lung tissue revealed high numbers of larvae in the control, a few in the treated animal which rejected the drug, and 1 dead decomposing larva from the other treated deer. Trial II It was decided to keep the deer in trial II alive for at least a month after the end of treatment to be sure the drug was killing the adults in the brain and not just the peripheral larvae. There were 2 deer treated and 2 used as controls in trial II because 1 deer had to be euthanatized with an apparent clinical case of meningeal worm. One of the controls had a very low larval count, while the one that was euthanatized was not shedding any larvae, even though there were many adult worms found in the meninges on post- mortem examination. Again, the albendazole seemed to lower feed consumption, as shown in Appendix B, but both treated deer ate regularly. It was hard to attribute the anorexia to the drug exclusively because other variables, such as hot muggy weather, human activities near the pens, inclusion of the ViNatura and even the effect of the parasite seemed to affect feed consumption of both treatment and control animals. Table 1 shows that although deer in trial II received a greater number of parasites, the average larval output was lower. Larval output dropped to zero during the 18 2-week treatment for both treated deer and larval output did not resume before euthanasia 1 month later. At the time of necrOpsy, larval counts were low in both control deer, but counts fluctuated daily from over 12,000 to less than 100 larvae/gm of feces in the animal with the higher output. At necropsy (Appendix C), the brains of both control deer con- tained many live adult P. tennis and the meninges were very hemorrhagic and necrotic (Figure 1). A mass of live worms about 1 cm in diameter and 3 cm in length was found in the dorsal median sulcus between the cerebral hemispheres of the deer which Showed fluctuating larval counts. This clumping was also found by Prestwood (1970) in a white-tailed deer with neurological disease. She suggested that the neuro- logical symptoms shown by this deer were caused by the large masses of parasites and resulting circulatory disturbances. Similar lesions in the deer in this study might help explain the varying feed consumption as well as the erratic larval counts becauSe larvae get to the lungs via the venous blood supply, which was obviously compromised. No live worms were found in either of the treated deer.. Extensive dissection and examination Showed only some dead, well encapsulated worms on the meninges. There was no gross evidence of the severe inflammation and hemorrhage seen in the controls. The meninges appeared glistening white_and healthy (Figure 2). The damage caused to the meninges by the parasites as well as the inflammation associated with the dead, decomposing adult worms had apparently healed by 1 month post-treatment. Figure 1. Cranium of control white-tailed deer. Note the inflammation and hemorrhagic meningitis. Figure 2. Cranium of white-tailed deer 1 month after treatment with albendazole. Note the glistening healthy white meninges and the dead encapsulated parasite at the tip of the forceps. DISCUSSION Although this research was done on a rather small number of animals and was hampered by the nervous, unpre- dictable nature of the wild deer, albendazole was shown to be effective against P. tennis in white-tailed deer. -Addi- tional research determining optimum effective dosage might show efficacy at a lower dosage or shorter treatment period. A lower dosage would make drugged feed more palatable, limit potential side effects and make widespread group treatment a feasible management tool for a herd or yard of deer. Initial research on optimum drug dosage and feasibility of group treatment with consideration of some of the drug's known potential side effects, such as teratogenicity or abortions, should be done on a captive group of deer. Fur- ther field Studies might be conducted on a group of wild deer confined to their winter yard by snow. In this study. deer averaging 35 kg body weight con- sumed approximately 1.25 kg of untreated pellets daily. For group treatment, these data would suggest a pelleted .feed with 1.4 gm of albendazole per kg of feed to give an approximate daily dose of 50 mg/kg of albendazole to each deer. Incorporating the drug in a palatable pelleted feed offered free choice would be a practical method of treatment 20 21 with larger deer receiving a larger dose by eating a greater volume. Another method of treatment might be to include the drug in ensiled apple pomace as was done by Colorado researchers (Schmidt et al., 1978) with bighorn sheep. Their research showed feasibility and success of using anthelmintic drug treatment in management of wild popula- tions. In their study, a Single dose of 8.4 gm of Cambenda- zole was incorporated in as little as 1.30 kg of apple pomace to give the drug at approximately 125 mg/kg body weight to treat Protestrongylns spp. of lungworms in bighorn sheep. This Single dose treatment could allow a dominant animal or an aggressive eater to overdose while depriving subordinate animals of adequate dosage. The suggested 2-week treatment with albendazole in a pellet designed to be fed free choice would allow most deer to get adequate dosages while aggresSive eaters might experience minimal side effects. Data from this research suggest that a lower dose for a shorter period of time might be as effective. The dramatic drop in larval output in deer No. 2 of trial I after only 1 treatment indicates that a shorter treatment period might be effective. The rejection of drugged feed by other successfully treated deer definitely shows that daily doses lower than 50 mg/kg would be effi- cacious. Also incorporating a certain percentage of the anthelmintic directly into the pelleted ration as it was manufactured would offer several advantages. It would allow known dosages by measuring consumption by individuals, and 22 premixed feed would be more palatable because the taste would be diluted out and the drug would be less detectable than on the outside of the pellets as in this study. An added benefit of treatment of white-tailed deer with obvious management implications is the already proven (Foreyt and Drawe, 1978) effectiveness of albendazole against lungworms, liver flukes, and intestinal nematodes as well as meningeal worms. Another asset of albendazole is its acceptance for use against liver flukes in food producing animals by USDA and FDA. Although its approval for use in sheep and cattle does not make its use in wildlife "legal", it makes special approval of its use by wildlife managers much more likely. The withdrawal time for albendazole in sheep in Australia is 10 days (Prichard, 1978). Because of the experimental nature of the drug in the U.S., the cautious required withholding period for cattle and sheep is 180 days (FDA Memo, 1980). Even this would permit treatment of wild populations in the winter and allow a longer withdrawal time before legal hunt- ing, thus minimizing the chance of this drug getting into the human food chain. Modern pressures of habitat encroachment and overpopu- lation of remaining habitat with competition, both within and between species, facilitate disease spread. This concept is conSidered for moose by Franzmann (1978) in a recent manage- ment text, while the same concept with consideration of anthelmintic treatment as an important management tool is discussed by Wishart (1978) in the chapter on bighorn sheep. Moran (1973) felt that if the P. tennis reservoir could be 23 reduced, this might help elk increase their numbers despite deteriorating habitat quality. George et a1. (1974) felt that P. tennis was the most important factor in the decline of Pennsylvania elk and much more research should be aimed at solving the disease problem if elk were to be saved in the east. Successful drug treatment of P. tennis in white-tailed deer with albendazole raises hopes for management of this parasite in cervids such as moose and elk in the north- central range of the white-tailed deer. It also has poten- tial for management of cerebral parelaphostrongylosis in other abnormal exotic and domestic hosts as well as diseases caused by other metastrongyle nematodes. A parasite which might have similar potential for management with albendazole is the arterial worm (EZaeophora schneideri). This parasite is carried by both mule deer and white-tailed deer and was Shown by Hibler and Adcock (1971) to cause a very serious neurological disease in native elk. Recently this parasite was shown to cause disease in exotic Sika deer in Texas (Robinson et al., 1978). Another parasite which might be managed is the Eurasian caribou parasite (EZaphostrongyZus eervi), which was recently identified in North America (Lankester and Northcott, 1979), causing a disease similar to P. tennis in caribou. The danger of this disease and the importance of preventing its spread were shown earlier by Lankester (1977) when an experimental infection was able to complete its life cycle in moose while causing serious neuro- logical disease. 24 It is evident that much more research is needed to define precise treatment of P. tennis in white-tailed deer with albendazole and to evaluate this and other drugs for their potentail in managing other parasites in other species. It is encouraging to note that a broad-spectrum anthelmintic with a wide margin of safety like albendazole could have a very important role in modern wildlife management. LIST OF REFERENCES 10. LIST OF REFERENCES ALDEN, C., F. WOODSON, R. MOHAN AND S. MILLER. 1975. Cerebrospinal nematodiasis in sheep. J. Am. Vet. Med. Ass. 166:784-786. ALIBASOGLU, M., D. C. KRADEL, AND H. W. DUNNE. 1961. Cerebral nematodiasis in Pennsylvania deer (Odocoileus virginianus). Cornell Vet. 51:431-444. ANDERSON, R. C. $1963. The incidence, development, and experimental transmission of Pneumostrongylns tennis Dougherty (Metastrongyloidea: Protostrongylidae) of the meninges of the white-tailed deer (Odocoileus virginianns borealis) in Ontario. Can. J. 2001. 41:775-792. 1964. Neurologic disease in moose infected experimentally with Pnenmostrongylns tennis from white- tailed deer. Path. Vet. 1:289-322. . 1965a. The development of Pneumoatrongylns tennis in the central nervous system of white-tailed deer. Path. Vet. 2:360-379. 1965b. An examination of wild moose exhibit- ing neurologic signs, in Ontario. Can. J. Zool. 43: 635-639. 1965c. Cerebrospinal nematodiasis (Pneumo-I strongylns tennis) in North American cervids. Trans. 13N. Amer. Wildl. Nat. Res. Conf. 30:156-167. , M. W. LANKESTER AND U. R. STRELIVE. 1966. Further experimental studies of Pneumostrongylns tennis in cervids. Can. J. 2001. 44:851-861. . 1971. Neurologic disease in reindeer (Rangifer taranZns tarandns) introduced into Ontario. Can. J. 2001. 49:159-166. 1972. The ecological relationship of meningeal worm and native cervids in North America. J. Wildl. Dis. 8:304-310. 25 11. 12. 13. 14. 15. 16. 17. 18. 19. 20. 21. 22. 23. 26 BEHREND, D. F. AND J. F. WITTER. 1968. Pneumostrongylns tennis in white-tailed deer in Maine. J. Wildl. Mgmt. 32:963-966. BROWN, T. T., H. E. JORDAN AND C. N. DEMOREST. 1978. Cerebrospinal ~ parelaphostrongylosis in llamas. J. CARPENTER, J. W., H. E. JORDAN AND B. C. WARD. 1973. Neurologic disease in wapiti naturally infected with meningeal worms. J. Wildl. Dis. 9:148-153. DOUGHERTY, E. C. 1945. The nematode lungworms (sub- order Strongylina) of North American deer of the genus Odocoileus. Parasitology 36:199-208. ECKROADE, R. J., G. M. ZU RHEIN AND W. J. FOREYT. 1970. Meningeal worm invasion of the brain of a naturally infected white-tailed deer. J. Wildl. Dis. 6:430-436. FAY, L. D. AND J. N. STUHT. 1973. MEningeal worm in association with neurologic disease in Michigan wapiti. 1973 Wildl. Dis. Conf. Papers and Abstracts, No. 24. FDA MEMO NO. 80-6038. 1980. Special liver fluke pro- gram. Issued by: Information Services Staff, Bureau of Veterinary Medicine, Rockville, Maryland, 7 pp. FOREYT, W. J. AND L. DRAWE. 1978. Anthelmintic activity of albendazole in white-tailed deer. Am. J. Vet. Res. 39:1901-1903. FRANZMANN, A. W. 1978. Moose. pp 67-81. In: Big Game of North America Ecology and Management. Schmidt, J. L. and D. L. Gilbert, eds. Stackpole Books, Harrisburg, Pennsylvania, and Wildlife Management Institute, Washington, DC. 494 pp. 'GEORGE, J. L., J. EVELAND, AND N. HUNTER. 1974. The Pennsylvania elk herd. Mimeographed Progress Report for Pennsylvania State University, September, 1974. GILBERT, F. F. 1973. PareZaphostrongyZns tennis (Daugherty) in Maine: I - The parasite in white-tailed deer (Odocoileus virginianns, Zimmerman). J. Wildl. Dis. 9:136-143. 1974. Parelaphostrongylns tennis in Maine: - revalence in moose. J. Wildl. Mgmt. 38:42-46. GUTHERY, F. 8., S. L. BEASOM AND L. JONES. 1979. Cerebrospinal nematodiasis caused by PareZaphostrongyZns tennis in Angora goats in Texas. J. Wildl. Dis. 15: 37-42. 24. 25. 26. 27. 28. 29. 30. 31. 32. 33. 34. 35. 27 HIBLER, C. P., AND J. L. ADCOCK. 1971. Elaeophorosis. pp 263-278. In: Parasitic Diseases of Wild Mammals. Davis, J. W. and R. C. Anderson, eds. Iowa State Univ. Press, Ames, Iowa. 364 pp. KARNS, P. D. 1966. Pnenmostrongylus tennis from elk (Cervns eanadensis) in Minnesota. Bull. Wildl. Dis. Assoc. 2:79-80. 4 . 1967. Pneumostrongylns tennis in deer in Minnesota and implications for moose. J. Wildl. Mgmt. 31:299-303. , AND P. A. JORDAN. 1969. Pneumostrongylns tennis on a deer-free island. J. Wildl. Mgmt. 33:341- 433. KISTNER, T. P., G. R. JOHNSON AND G. A. RILLING. 1977. Naturally occurring neurologic disease in a fallow deer . infected with meningeal warms. .J. Wildl. Dis. 13:55-58. LANKESTER, M. W., AND R. C. ANDERSON. 1968. Gastro- pods as intermediate hosts of Pneumostrongylns tennis Daugherty of white-tailed deer. Can. J. 2001. 46:373- 383. . 1977. Neurologic disease in moose caused by EZapHostrongyZns eervi Cameron 1931 from caribou. Proceedings of the 13th Annual North American Moose Conference and Workshop, Jasper, Alberta. 177-190 pp. AND T. H. NORTHCOTT. 1979. EdeHostrongyZns eervi Cameron 1931 (Nematoda: Metastrongylaidea) in caribou (Rangifer tarandns caribou) of Newfoundland. Can. J. 2001. 57:1384-1392. LOKEN, K. I., J. C. SCHLOTTHAUER, H. J. KURTZ, AND P. D. KARNS. 1965. Pneumostrongylns tennis in Minnesota moose (AZses alces). Bull. Wildl. Dis. Assoc. 1:7. MAYHEW, I. G., A. de LAHUNTA, J. R. GEORGI AND D. G. ASPROS. 1976. Naturally occurring cerebrospinal parelaphostrongylosis. Cornell Vet. 66:56-71. MORAN, R. J. 1973. The Rocky Mountain elk in Michigan. Michigan Dept. of Nat. Res. Research and Development Report No. 267. NETTLES, V. P., A. K. PRESTWOOD, R. G. NICHOLS AND C. J. WHITEHEAD. 1977. Meningeal worm-induced neura- logic disease in black-tailed deer. J. Wildl. Dis. 13:137-143. 36. 37. 38. 39. 40. 41. 42. 43. 44. 45. 46. 47. 28 , A. K. PRESTWOOD AND R. D. SMITH. 1977. CereBraspinal parelaphostrongylosis in fallow deer. J. Wildl. Dis. 13:440-444. NIELSEN, S. W. AND J. AFTOSMIS. 1964. Spinal‘nema- todiasis in tWO sheep. J. Am. Vet. Med. Assoc. 166: 784-786. OLSEN, A., AND A. WOOLF. 1978. The development of clinical signs and the population significance of neurologic diseases in a captive wapiti herd. J. Wildl. Dis. 14:263-268. 1979. A summary of the prevalence of Par- eZapHostrongyZns tennis in a captive wapiti population. J. Wildl. Dis. 15:33-35. PRESTWOOD, A. K. 1970. Neurologic disease in a white- tailed deer massively infected with meningeal worm. J. Wildl. Dis. 6:84-86. PRICHARD, R. K. 1978. Sheep anthelmintics. pp 80-81. In: The Epidemiology and Control of Gastrointestinal Parasites of Sheep in Australia. Donald, A. D., W. H. Southcott, and J. K. Dineen, eds. Division of Animal Health, Commonwealth Scientific and Industrial Research Organization, Australia. 153 pp. ROBINSON, R. M., L. P. JONES, T. J. GALVIN, AND G. M. HARWELL. 1978. Elaeapharosis in Sika deer in Texas. J. Wildl. Dis. 14:137-141. SCHMIDT, R. L., C. P. HIBLER, T. R. SPRAKER AND W. H. RUTHERFORD. 1979. An evaluation of drug treatment for lungworm in Bighorn sheep- J. Wildl. Mgmt. 43: 461-467. SMITH, H.‘J., R. M. ARCHIBALD, AND A. H. CORNER. 1964. Elaphostrongylns in Maritime moose and deer. Can. Vet. "J. 5:287-296. SMITH, H. J. AND R. M. ARCHIBALD. 1967. Moose sickness, a neurological disease of moose infected with the common cervine parasite, EZaphostrongyZfis tennis. Can. Vet. J. 8:173-177. TRAINER, D. O. 1973. Caribou mortality due to the meningeal worm (PareZaphostrongyZns tennis). J. Wildl. Dis. 9:376-378. WHITLOCK, J. H. 1952. NeurofilarOsis, a paralytic disease of sheep: II - NenrofiZaria corneZZenSis, N.G., N.Sp. (Nematoda, Filaroidea), a new nematode parasite from the spinal cord of sheep. Cornell Vet. 42:125-132. 48. 49. so. 29 . 1959. EZaphostrongyZns, the praper designa- tion of NenrofiZaria. Cornell Vet. 49:3-14. WISHART, W. 1978. Bighorn sheep. pp 161-171. In: Big Game of North America Ecology and Management. Schmidt, J. L. and D. L. Gilbert, eds. Stackpole Books, Harrisburg, Pennsylvania, and Wildlife Manage- ment Institute, Washington,-DC. 494 pp. WOOLF, A., C. A. MASON AND D. KRADEL. 1977. Prevalence and effects of PareZaphostrongyZns tennis in a captive wapiti population. J. Wildl. Dis. 13:149-154. APPENDI CES 30 APPENDIX A Table A1. Consecutive daily counts of larvae per gram of feces in deer on albendazole study Trial I Trial II C6ntr61 Treated’ Control Treated No I N6”2 N043 No l N012 No 3 No 4 Pre- 2006 8323 4869 792 51 1432 152 treatment 3033 9233 3976 741 17 1399 152 1887 8644 4263 994 " 910 286 2 week 2713 17439 2561 1685 " 4987 202 treatment period 2460 28492 4111 2612 " 1095 1297 3100 55737 2123 4078 51 9065 388 2932 56225 2140 4482 0 4617 169 1921 37944 1938 691 0 8913 1668 1297 25813 657 640 0 5543 708 1735 10935 320 741 0 910 67 2190 1449 202 944 0 0 17 1078 202 506 725 0 17 84 2831 51 169 1786 17 219 0 1095 0 84 707 0 67 0 1702 0 34 1348 0 34 0 1062 0 17 6554 0 l7 0 1382 0 34 2999 0 0 0 Post- 1264 0 0 1786 0 0 0 treatment 960 0 17 3100 0 0 0 31 Table A1 (continued) Trial I Trial II Cbntrol TTreatéd Control TTeated No I No 2 N023 No 1 No 2 No 3 No 4 1025 0 O 775 0' 0 0 2477 17 0 927 17 0 0 776 0 0 674 0 0 0 Past- mortem 1584 0 0 Returned to free choice feed for 3 weeks 32 APPENDIX B Table Bl. Uneaten feed in kg when fed 90% of free choice consumption in 2 daily feedings _‘ Trial I Trial II Feed 1.0 120' ‘1)4 110 7 1.1 0.9T1 1.3 Offered Na 1 Na 2 No 3 . No 1 No 2 No 3 Na 4 Pre- treatment 0 0 0 .33 ' .28 .09 .45 0 0 0 09 .13 00 00 0 0 0 25 .05 06 00 2 week 0 7 0 59 .25 17 .77 treatment period 0 5 0 .55 .25 80 77 0 1.07 .8 .23 .39 .93 .72 0 1.05 .24 .ll .29 .95 .08 0 1.06 .14 .07 .07 .75 .92 0 1.065 ".27 .06 . .19 .26 .41 o 1.888’ .28 .oo .12 .17 .24 stopped drug . . 0 .245 .15 .ll .14 .42 .40 0 .14 .27 .ll .19 .78 .79 0 0 .22 .49 ' .08 .51 .21 0 0 .03 .26 .04 36 38 l 0 30 .26 13 19 55 0 0 .13 .26 .07 24 34 0 0 .165 .26 .17 15 45 Post- 0 0 .165 .24 .05 .25 .40 treatment 0 0 0 08 .02 07 07 _Appendix B1 (continued) 33 Trial I ITO 1.0 11.47 No 1 No 2 No 3 Trial II I.0 I.I 0.9 1.3— Na 1 Na 2 No 3 No 4 0 0 0 0 0 0 0 0 0 Euthanasia .03 .02 .00 .00 .01 .01 .00 .00 .00 .08 .00 .00 Returned to free choice feed for 3 weeks 34 APPENDIX C Table C1. Vital statistics of deer in albendazole study Trial I Trial II No I ‘No 2* ’Nof3 No 1 ‘TNOTZ' No 3 No 4 Estimated pre- treatment body _40 30 30 30 30 30 30 weight, kg Daily free choice feed 111 1.2 1.6 1.1 1.2 1.0 1.4 consumption, k8 Daily Treatment 90% feed, kg 1.0 1.0 1.4 1.0 1.1 0.9 i 1.3 ViNatura, cc 40 30 30 30 30 30 40 Albendazole, mg 0 1500 1500 0 0 1500 2000 Postmortem Body weight, kg 35 26 32' 31 32 31 45 Larvae/gm feces 1584 0 0 169 0 0 0 'Larvae from lungs 100's ' 3 1 dead 2 0 0 0 Meningitis yes yes yes yes yes no no No. of P. -10 12 8 -70 -25 5 6 tennis in alive alive 44live alive alive dead dead meninges Condition of dis- dis- dis- en- P. tennis persed persed.44dead clumped persed capsulated