Effect of forage legumes containing condensed tannins on lungworm (Dictyocaulus sp.) and gastrointestinal parasitism in young red deer (Cervus elaphus)

To investigate the effect of feeding forage legumes containing condensed tannins ( ) on internal parasitism, red deer calves were fed either lucerne (Medicago sativa; 0.1 per cent ), birdsfoot trefoil (Lotus corniculatus; 1.9 per cent ) or sulla (Hedysarum coronarium; 3.5 per cent ) and trickle-infected with deer-origin gastrointestinal nematode and lungworm (Dictyocaulus sp.) larvae for 5 weeks, then slaughtered at 7 weeks. There was a significant negative linear relationship between dietary concentration and abomasal nematode burdens. No significant differences in faecal egg counts, lungworm burdens or voluntary feed intake were found. Deer fed sulla had higher liveweight gain, carcass weight and carcass dressing-out percentage, higher serum total protein and albumin concentration and lower serum gastrin concentration and faecal lungworm larval count, compared with lucerne-fed deer. Inclusion of sulla in diets for young red deer may reduce the impact of internal parasites and/or reduce the dependence on anthelmintic treatment.     

A model for study of lungworm (Dictyocaulus sp.) and gastrointestinal nematode infection in young red deer (Cervus elaphus)

A model of sub-clinical parasitism in young red deer, using concurrent trickle infections of lungworm (Dictyocaulus sp.) and mixed gastro-intestinal (GI) nematodes of deer-origin was evaluated. 20 parasite-free deer calves were artificially reared indoors from 4 days of age. A further five calves were naturally reared on pasture with their dams, treated with anthelmintic and brought indoors at 3-4 months. At 4-4.5 months of age they were individually housed and allocated to five groups (n=5). Groups were dosed 3 x per week, for 9 weeks with 0, 100 and 500, 200 and 1000 (2 groups), 400 and 2000 infective larvae of lungworm and mixed GI nematodes, respectively, cultured from deer faeces. Liveweight and voluntary feed intake measurements and faecal and blood samples were taken weekly. In the fourth week following cessation of trickle infection, deer were euthanased and lung and GI nematodes recovered. Both lungworm and GI nematode infections became patent at Week 4 of infection. Maximum group arithmetic mean faecal egg counts were 100-190 epg. Maximum group arithmetic mean faecal lungworm larval counts were 58-123 lpg. Group arithmetic mean nematode counts at slaughter ranged from 439-806 for GI nematodes and 31-73 for lungworm, respectively. Despite low nematode counts, reduced liveweight gain, voluntary feed intake and serum albumin concentration, elevated serum pepsinogen, gastrin and globulin concentrations and elevated peripheral eosinophil counts and slight haemoconcentration, but no clinical signs, were observed. The reduction in liveweight gain was related to the reduction in voluntary feed intake (r2=0.83; p<0.088). Naturally-reared deer had similar liveweight gains, voluntary feed intake and nematode counts to artificially-reared deer. Thus, methods of infection to produce concurrent sub-clinical lungworm and GI nematode burdens for study of sub-clinical parasitism in young deer have been defined.     

Novel forages for growth and health in farmed deer

AIMS: This paper reviews recent research on the use of new forages in deer farming that may be useful for increasing growth in weaner deer for venison production, increasing the trace element status of deer, and for developing systems less reliant on chemical inputs, notably of anthelmintics used to control internal parasites. GROWTH: Grazing on pure swards of red clover (Trifolium pratense) or chicory (Chicorium intybus) increased weaner growth during autumn by 26-47% and during spring by 10-14%, relative to red deer (Cervus elaphus) grazed on perennial ryegrass (Lolium perenne) /white clover (Trifolium repens) pasture (0.8/0.2). Pre-weaning growth during lactation was increased by approximately 20%. These increases were due to increased rate of degradation of feed particles in the rumen, leading to higher digestibility and higher voluntary feed intakes (VFI). Red clover and chicory produce a greater proportion of their total dry matter (DM) during late summer and autumn than perennial ryegrass/white clover pastures, and are therefore better aligned with the seasonal feed requirements of deer. Grazing on the legume, sulla (Hedysarum coronarium), in autumn and spring increased the growth of weaner deer by 33% and 10%, respectively, relative to pasture-fed animals. PARASITES: Plants containing substantial concentrations of secondary compounds such as condensed tannins (CT) show promise for reducing problems caused by internal parasites. CT present in some legumes and the presence of low concentrations of both CT and sesquiterpene lactones in chicory are reviewed. Feeding sulla containing 35g CT /kg DM reduced abomasal nematode establishment and tended to reduce lungworm (Dictyocaulis eckerti) larval counts in faeces. Relative to weaner deer grazing pasture, weaner deer grazing chicory during autumn required fewer anthelmintic treatments without depressing growth rates. CT extracted from a range of legumes, and CT and sesquiterpene lactones extracted from chicory reduced the in vitro motility of both lungworm and gastrointestinal nematode larvae. The beneficial effects of CT-containing forages on the ability of young deer to manage internal parasite infections could be due to: indirect effects of CT resulting in increased amino-acid absorption, better meeting demands of the immune system; direct inhibitory effects of CT on parasite larvae and; taller plant morphology, reducing the ingestion of infective larvae. The effects of CT depend upon both their structure and CT Condensed tannins DM Dry matter L1 First-stage larvae L3 Infective third-stage larvae LWG Liveweight gain ME Metabolisable energy OM Organic matter OMD Organic matter digestibility VFIVoluntary food intake concentration in the plant, which vary between growing conditions, plant varieties and species. TRACE ELEMENTS: Chicory contained higher concentrations of copper and cobalt than perennial ryegrass/white clover pasture grown on the same farm, and deer grazing chicory had higher liver concentrations of both copper and vitamin B12. These forages may contribute to maintaining adequate trace element status in deer. CONCLUSIONS: Grazing systems that include legumes and herbs such as sulla, red clover and chicory can be used to substantially increase the growth of weaner deer for venison production whilst maintaining deer health and reducing requirements for chemical inputs. For maximum plant persistence and animal responses, these plants should be grown and managed as special-purpose forages and not used in seed mixtures with perennial grasses.     

Effect of condensed tannins extracted from four forages on the viability of the larvae of deer lungworms and gastrointestinal nematodes

The inhibitory activity of condensed tannins extracted from four forage legume plants were evaluated by using a larval migration inhibition assay. The first (L1) and third (L3) stages of deer lungworm (Dictyocaulus viviparus), and the third stage (L3) of deer gastrointestinal nematodes were incubated with tannins extracted from Lotus pedunculatus, Lotus corniculatus, sulla (Hedysarum coronarium) and sainfoin (Onobrychus viciifolia). The tannins extracted from all the forages had inhibitory activity as measured by their ability to paralyse the larvae and inhibit them from passing through sieves. At the highest concentration used (1200 microg/ml) the tannins extracted from sainfoin had the highest activity against ensheathed L1 lungworm larvae (58 per cent), followed by L. pedunculatus (45 per cent), sulla (42 per cent) and L. comiculatus (35 per cent) when the larvae were incubated at 37 degrees C. The same trend, but with lower activities, was observed when the larvae were incubated at 22 degrees C. Anthelmintic activity against L3 lungworm larvae was evaluated by measuring the death rate of ensheathed L3 larvae after incubation with condensed tannins for two, 24 and 48 hours at room temperature (22 degrees C). The death rate was significantly higher (P<0.001) after 48 hours incubation than after two hours or 24 hours, and significantly higher (P<0.001) after 24 hours than after two hours incubation. Condensed tannins from sainfoin had the highest inhibitory activity followed by L. pedunculatus, sulla and L. comiculatus. The tannins from sainfoin also had the highest activity against L3 larvae of gastrointestinal nematodes, followed by L. pedunculatus, sulla and L. comiculatus. Exsheathed larvae of gastrointestinal nematodes were significantly more susceptible to the action of the tannins than ensheathed larvae.     

A comparison of lungworm faecal larval counts and trichostrongyloid faecal egg counts between red deer (Cervus elaphus) and red deer x wapiti F1 hybrids

To determine if breed differences in susceptibility to trichostrongyloid and lungworm infection exist, two groups of weaner deer containing seven red deer and red deer x wapiti F1 hybrids were compared using faecal egg counts and faecal larval counts. All animals were run on the same pasture at the same time and treated with the same anthelmintics at the same time. Results indicated that there were significant differences between red deer and red deer x wapiti hybrids, with red deer having higher faecal lungworm counts and red deer x wapiti hybrids having significantly higher faecal egg counts. It is likely that these differences were due to breed. Differences in the efficacy of anthelmintic treatments were also noted between the two groups, with oral oxfendazole being less effective at reducing faecal lungworm counts in red deer X wapiti hybrids than red deer.     

The effect of feeding sulla (Hedysarum coronarium) or lucerne (Medicago sativa) on lamb parasite burdens and development of immunity to gastrointestinal nematodes

Two experiments investigated the efficacy of the legume Hedysarum coronarium (sulla), which contains condensed tannins (CTs), for reducing gastrointestinal nematode infections relative to lucerne. Experiment 1 was aimed to show whether the lower faecal egg count (FEC) and larval establishment previously reported in lambs grazing sulla were due to direct effects of the forage on Ostertagia circumcincta and Trichostrongylus colubriformis or were mediated through an enhanced immune response. Experiment 2 evaluated the impact of feeding sulla relative to feeding lucerne (Medicago sativa), before, at, or after larval challenge on subsequent FECs and nematode burdens. In experiment 1, 64 Romney lambs were fed either freshly cut lucerne or sulla (32 lambs per herbage) for the duration of the trial. Within each herbage there were four treatment groups (n=8 per group). Initial levels of immunity were assessed in uninfected (UN) lambs which were maintained parasite-free until challenged with 15,000 O. circumcincta and 15,000 T. colubriformis larvae on day 63, and slaughtered on day 81. The other three treatment groups were trickle-infected with each of 5000 O. circumcincta and 5000 T. colubriformis larvae three times per week from day 1 to 35. Non-steroid infected (CONTROL) and steroid-treated (STER) groups were treated with anthelmintic on day 49 and challenged with 15,000 O. circumcincta and 15,000 T. colubriformis on day 63 and slaughtered on day 81. The STER lambs were given dexamethasone trimethylacetate from day 49 to 81 to determine effects of immunity on parasite infection. From day 35 an establishment group (EST) on each herbage was fed a common pelleted lucerne diet and slaughtered on day 56 to determine nematode establishment during trickle-infection. Diet did not affect FECs but feeding lucerne increased (P<0.05) numbers of T. colubriformis in CONTROL lambs compared to those fed sulla. O. circumcincta numbers were lower (P<0.05) in UN lambs fed sulla than lucerne. The sulla diet was associated with higher (P<0.05) antibody titres against secretory-excretory antigens to adult O. circumcincta and to adult and larval T. colubriformis, so there appeared to be some immunogenic response to the sulla diet but effects upon T. colubriformis numbers were not significant. The second experiment involved 48 Romney lambs grazing conventional pasture which were infected with 10,000 each of O. circumcincta and T. colubriformis larvae either 7 days before, 7 days after, or at the time they commenced grazing either sulla or lucerne. Lambs which grazed sulla had lower (P<0.05) FEC and lower (P<0.05) O. circumcincta burdens than lambs which grazed lucerne but timing of infection had no effect on FEC or worm burdens. T. colubriformis numbers were not affected by treatment or herbage. In conclusion, the sulla diet resulted in lower O. circumcincta numbers compared to lucerne outdoors and some evidence of an immunogenic response was obtained indoors. However, neither the herbage nor the immunogenic response reduced T. colubriformis numbers in either experiment.     

Bronchopulmonary helminths of roe deer (Capreolus capreolus) in the northwest of Spain

From 1993 to 1995, 148 hunter killed roe deer (Capreolus capreolus L.) from game reserves in Lugo (northwestern Spain) were examined for lungworm infection. The overall prevalence of infection was high (66.2%). Infections were comprised to two species, Varestrongylus capreoli and Dictyocaulus noerneri with a prevalence of 62.0 and 18.2%, respectively. Significant differences in the prevalence and larval burdens in lungs and faecal samples were observed between different locations. The highest overall prevalence of lungworm infection was observed in the large reserve at Ancares (78%) in comparison to that in smaller reserves (61.7%). Considering that the species recorded in this study are highly host-specific, it is unlikely that roe deer represent a significant reservoir of lungworm transmissible to domestic ruminants in northwestern Spain.     

Preliminary observations on lungworms in farmed and feral red deer (Cervus elaphus) in Denmark

Deer farming is on its increase in Denmark. Based on experiences from other countries, lungworm infection is expected to cause severe problems in farmed deer. Therefore, in the present paper, which is the first one to deal with pathogens in Danish deer farms, the faecal larval excretion in red deer is examined.     

Effects of concurrent copper deficiency and gastro-intestinal nematodiasis on circulating copper and protein levels, liver copper and bodyweight in sheep

Sheep were rendered hypocupraemic using parenteral ammonium tetrathiomolybdate (ATM). Fifteen thousand third stage larvae of Trichostrongylus axei and T. colubriformis in the ratio 1:1 were administered three times per week for six weeks, starting four weeks after cessation of ATM treatment. The changes in liver and plasma copper (Cu), caeruloplasmin activity, serum proteins, faecal nematode egg counts and total nematode counts were measured in the sheep for 10 weeks after infection. Decreases in liver Cu, plasma Cu and caeruloplasmin activities were detected soon after infection. There was a significant (P less than 0.05) interaction of the effects of Cu deficiency and nematode infection on these changes. Hypoproteinaemia, attributed to serum albumin loss, was demonstrated seven weeks after infection, but this was not associated with the interaction of Cu deficiency and nematode infection. No changes in serum globulins were detected. Although the results support the contention that gastro-intestinal nematodiasis can significantly exacerbate an existing Cu deficiency in sheep, there was no evidence that hypocuprosis would predispose sheep to higher nematode burdens.     

Efficacy of slow-release albendazole capsules in controlling lungworms and gastro-intestinal nematodes in red deer (Cervus elaphus)

One hundred and fifteen young red deer (Cervus elaphus), heavily infected with lungworm (Dictyocaulus viviparus) and lightly infected with gastro-intestinal nematodes, were divided into three groups. One group of 50 animals was treated with one adult sheep dose of a slow-release albendazole capsule, another group of 50 was dosed orally five times with liquid albendazole and 15 were left as untreated controls. The capsule eliminated faecal lungworm larvae during the 103-day trial period There was a highly significant difference in faecal larval counts between the capsule-treated and control group. Over the trial period, the mean body weight gain of the untreated, liquid albendazole and capsule-treated animals was 0.1 kg, 4.5 kg and 7.8 kg respectively.     

Effects of grazing undrenched weaner deer on chicory or perennial ryegrass/white clover pasture on the viability of gastrointestinal nematodes and lungworms

This study determined the in vitro effects on the viability of internal parasites of grazing undrenched weaner deer on either chicory (Cichorium intybus) or perennial ryegrass (Lolium perenne)/white clover (Trifolium repens) pasture. One experiment investigated the hatching and development of gastrointestinal nematode eggs and larvae, and the development and motility of L1 lungworm (Dictyocaulus eckerti) larvae, and a second experiment used larval migration inhibition assays to test the viability of L1 lungworm larvae extracted from the faeces of weaner deer grazed on either chicory or pasture when they were incubated with rumen and abomasal fluids from fistulated deer also grazing on chicory or pasture. The incubations were undertaken with and without added condensed tannins purified from chicory and with or without polyethylene glycol (PEG) to bind the tannins. Chicory had no effect on the hatching and development of gastrointestinal nematode eggs and larvae. Grazing chicory reduced the number of lungworm larvae developing to the L3 stage, and L1 lungworm larvae from the faeces of chicory-grazed deer were less viable in rumen and abomasal fluid than larvae from pasture-grazed animals. Abomasal fluid was significantly (P < 0.001) less inhibitory to the migration of L1 lungworms than rumen fluid. When the larvae were incubated in rumen and abomasal fluids from chicory-grazed deer, their passage through sieves was significantly (P < 0.001) reduced in comparison with when they were incubated in the fluids from pasture-grazed deer Adding condensed tannins to rumen fluid increased the inhibition of the migration of L1 lungworm larvae but PEG removed this inhibition; this effect was not observed with abomasal fluid.     

Efficacy of short-term feeding of sulla (Hedysarum coronarium) to young goats against a mixed burden of gastrointestinal nematodes

The aim was to investigate the efficacy of feeding sulla to young goats (<6 months of age) against a naturally acquired infection of gastrointestinal nematodes. Eleven goats were removed from the field, housed and were randomly divided into two treatment groups. Group 1 (n = 5) was fed a diet comprising lucerne-based pellets and aged hay. Group 2 (n = 6) were fed a diet of only sulla offered ad lib. The sulla contained 2.6% free condensed tannins (CT), 1.8% protein-bound CT and 0.1% fibre-bound CT. Goats in Gp 2 ate the sulla very readily from the first day. The goats were fed these diets for 10 days, then killed and total worm counts obtained. The arithmetic mean worm counts (in parentheses) for Gp 1 and Gp 2, respectively, were Teladorsagia circumcincta (5792, 5690), Trichostrongylus colubriformis (272, 262), T. vitrinus (1060, 1804) and Trichuris spp. (32, 30). There were no significant differences (p > 0.05) between any of these treatments. Short-term feeding of sulla had no effect on mixed burdens of gastrointestinal nematodes.     

Efficacy of slow-release albendazole capsules in controlling lungworms and gastro-intestinal nematodes in red deer (Cervus elaphus)

One hundred and fifteen young red deer (Cervus elaphus), heavily infected with lungworm (Dictyocaulus viviparus) and lightly infected with gastro-intestinal nematodes, were divided into three groups. One group of 50 animals was treated with one adult sheep dose of a slow-release albendazole capsule, another group of 50 was dosed orally five times with liquid albendazole and 15 were left as untreated controls. The capsule eliminated faecal lungworm larvae during the 103-day trial period. There was a highly significant difference in faecal larval counts between the capsule-treated and control group. Over the trial period, the mean body weight gain of the untreated, liquid albendazole and capsule-treated animals was 0.1 kg, 4.5 kg and 7.8 kg respectively.     

Experimental infections with Dictyocaulus viviparus in vaccinated and unvaccinated red deer

Four of eight red deer calves which had been artificially reared and were lungworm free were vaccinated with bovine lungworm oral vaccine when eight weeks old; the other four were not vaccinated. Three of each category were challenged daily with 500 Dictyocaulus viviparus infective stage larvae per kg liveweight for 17 days when six months old while one in each category was left as an unchallenged control. The effects of challenge were monitored and all challenged deer and one control were killed for post mortem assessment. Challenge with D viviparus was associated with reduced food intakes and weight gains but vaccinated calves were less affected than unvaccinated ones. The reaction of the alveolar tissue of red deer lung to D viviparus was mild in vaccinated and unvaccinated animals and differed from that of bovine lung in that alveolar epithelialisation was limited and hyaline membrane formation and interstitial emphysema were not seen. The disease was most evident in and around airways and was less in vaccinated calves. It was concluded that young red deer are tolerant to D viviparus but will readily acquire infection.     

A pilot study of the efficacy of topical ivermectin against lungworm in young red deer (Cervus elaphus)

Three groups of ten 4-month-old red deer (Cervus elaphus) calves naturally infected with lungworm (Dictyocaulus viviparus) were treated with either oral ivermectin (200 microg/kg), topical (pour-on) ivermectin (500 microg/kg) or oral oxfendazole (5 mg/kg). Faecal larval counts for lungworm were undetectable or very low for 14 days after treatment with oxfendazole, 28 days after treatment with oral ivermectin and for 49 days after treatment with topical ivermectin. This pilot study suggests that the topical formulation of ivermectin was very effective against lungworm and had a more persistent action than the oral ivermectin formulation in young red deer.     

Anthelmintic control of lungworm in donkeys

A field study was designed to investigate the re-establishment of patent lungworm infections in donkeys following an anthelmintic treatment regime which was effective against Dictyocaulus arnfieldi. In April 1979 faecal samples from 259 donkeys were examined and each animal classified as a negative, low positive or high positive excretor of lungworm larvae. During the summer the control group of 126 donkeys showed an increase in the number of excretors from 80 per cent in April to 91 per cent in October. At the same time there was a rise in the faecal larval output of individual animals so that by October 59 per cent were classified as high positive compared with only 20 per cent in April. The treated group of 133 donkeys received 3.5 g mebendazole daily for 5 days during April and as a result the number of excretors fell from 66 per cent pretreatment to 23 per cent one month after treatment. Despite exposure to infected pastures throughout the summer this figure was maintained at a comparatively low level and by October patent infections had been re-established in only 15 per cent of the donkeys that were negative after treatment.     

Reduced efficacy of moxidectin and abamectin in young red deer (Cervus elaphus) after 20 years of moxidectin pour-on use on a New Zealand deer farm

A study was undertaken on weaned 4–5 month old farmed red deer to test the efficacy of moxidectin and abamectin anthelmintics, given by three different routes of administration, compared with an untreated control. Faecal samples were collected on days 0, 7 and 14 for a faecal egg count reduction test (FECRT), blood samples were collected on days 0, 0.5, 1, 2, 3, 5, 7, 10 and 14 for pharmacokinetics, and the deer were killed on days 14 or 15 for total nematode count.The control group averaged 1264 adult Ostertagia-type nematode parasite species and treatment efficacy was 77.4% for moxidectin injection, 26% for oral moxidectin and 27.6% for pour-on moxidectin, while the treatment efficacy was 72.4% for abamectin injection, 70.1% for oral abamectin (Hi-Mineral) and 34.1% for pour-on abamectin. Both moxidectin and abamectin injections were significantly more efficacious than their equivalent pour-ons. There was a significant difference in efficacy between oral abamectin (Hi-Mineral) and oral moxidectin (P < 0.01).The control group averaged 2956 adult lungworm (Dictyocaulus eckerti) and 50 Oesophagostomum venulosum in the large intestine and treatment efficacy against these nematodes was 100% for all treatments. There were negligible numbers of other gastro-intestinal nematodes.At slaughter, there was a significant correlation (P = 0.02) between FEC and Ostertagia-type nematodes in the untreated controls. Relatively few eggs were found in faeces from treated animals at 7 and 14 days post-treatment despite significant worm burdens in all six treatment groups, suggesting egg-laying suppression in resistant nematodes, and all three different FECRT calculations tended to overestimate the efficacy of the treatments compared with actual nematode counts.Peak plasma concentrations (C_max) for both actives were measured 12 h after treatment for injection and oral and at 5 days for pour-on. C_max (ng/ml) for moxidectin injection, oral and pour-on were 71.8, 8.3 and 0.4, respectively, and for abamectin injection, oral and pour-on were 62.1, 30.3 and 10.0, respectively. Area under the curve (AUC) estimates for moxidectin injection, oral and pour-on were 106.6, 12.9 and 6.1, respectively, and for abamectin injection, oral and pour-on were 162.7, 57.5 and 74.3, respectively.The results demonstrate that significant anthelmintic resistance to moxidectin and abamectin is present on this deer farm. However, the injection was the most effective route of administration in young deer for both anthelmintics, although <80% efficacious. We conclude that the FECRT is unreliable in deer when anthelmintic resistance is present.     

Efficacy of moxidectin 2 per cent gel against naturally acquired strongyle infections in horses, with particular reference to larval cyathostomes

The efficacy of moxidectin 2 per cent equine gel against naturally acquired strongyle infections was assessed in 18 ponies which had grazed on contaminated pasture before being housed for eight weeks. Twenty-four hours before the treatment, two randomly selected ponies were euthanased and their worm burdens were determined. Eight of the remaining 16 ponies were treated with moxidectin 2 per cent gel while the other eight were given a placebo gel. Eight weeks later the 16 animals were necropsied and their worm burdens established. A 100 per cent efficacy was recorded against adult and lumenal L4 cyathostomes and adult Strongylus and Triodontophorus species. Digest recoveries of larval cyathostomes indicated a 90.8 per cent (P<0.002) reduction in early L3 and a 99.9 per cent (P<0.001) reduction in developing stages. There was a reduction in faecal egg output of between 96 and 100 per cent in the treated animals compared with the controls.