A survey of nematode control measures used by milking goat farmers and of anthelmintic resistance on their farms

Forty-seven milking goat herds, located throughout New Zealand, were surveyed for anthelmintic usage and for gastrointestinal nematodes resistant to anthelmintics. Most farmers (62%) followed a predetermined drenching programme and usually (68%) had a policy of alternating between drench families. Alternation was generally within the farming year. Kids were on average being drenched 12.5 times during their first year (range 2-34). Does aged greater than one year were all being drenched at the same frequency (average 13.4, range 2-34) irrespective of age. On each of the 47 farms, a group of goats was treated with a benzimidazole (BZ) drench (oxfendazole, OFZ, at 4.5 mg/kg on 36 farms and thiabendazole, TBZ at 66 mg/kg on 11 farms); a second group was treated with a "cell membrane depolarizing" (CMD) drench (levamisole, LEV, at 8 mg/kg on 35 farms and morantel citrate, MOR, at 10 mg/kg on 12 farms); a third group remained untreated as controls. Faecal egg counts and larval cultures were done before dosing and one week later. Faecal egg count depressions of <80% were taken as being suggestive of anthelmintic resistance. On this basis resistance was found on 79% of farms surveyed. Resistance to BZs alone occurred on 36% of farms, resistance to CMDs alone on 4% and resistance to both on 38% of farms. On 23% of farms one or other of the drenches was without any apparent effect and on one farm both of the drenches tested failed to reduce the egg counts. Post-drenching larval cultures showed Trichostrongylus, Haemonchus and Ostertagia to be the most prevalent genera remaining after drenching with BZ on 14,11, and 8 farms, respectively. After drenching with LEV Ostertagia was the dominant species on 10 farms, Trichostrongylus on 2 and on one farm the two genera were equally common. Following treatment with MOR Trichostrongylus was the dominant species on 3 farms, Haemonchus on 2 and on one farm Trichostrongylus and Ostertagia were equally common. There was a positive association between drenching frequency and the presence of resistance on farms. Possible interpretations of this association are discussed.     

Multiple species of nematodes resistant to ivermectin and a benzimidazole-levamisole combination on a sheep farm in New Zealand

AIM: To confirm the presence of multiple anthelmintic resistance on a sheep farm in New Zealand. METHODS: Three groups of 10 weaned Romney-cross lambs were treated either with an oral dose of ivermectin (0.2 mg/kg), or a benzimidazole/levamisole (BZ/LEV) combination (4.75 albendazole and 7.5 mg/kg levamisole), or were left untreated. Ten days later, animals were necropsied, and adult worms recovered and identified from the abomasa and small intestines. Pre- and post-treatment faecal nematode egg counts (FEC) were recorded, and larval cultures were performed. RESULTS: In a faecal egg count reduction test (FECRT), adjusted to reflect pre- and post-treatment larval culture results, ivermectin resistance was detected in Teladorsagia (Ostertagia), Trichostrongylus and Haemonchus spp, while BZ/LEV combination- resistant Teladorsagia and Trichostrongylus spp were also present. Adult worm counts confirmed these results, and identified the species involved as Teladorsagia circumcincta, Trichostrongylus colubriformis and H. contortus. CONCLUSION: Multiple, multi-generic anthelmintic resistance was confirmed on a sheep property in New Zealand. This included the first confirmed case of ivermectin resistance in T. colubriformis from sheep in New Zealand.     

Multiple anthelmintic resistance in Trichostrongylus colubriformis

Following the failure of anthelmintic treatment to control an outbreak of trichostrongylosis in sheep, multiple resistance to levamisole and oxfendazole was confirmed in field strains of Trichostrongylus colubriformis at the CSIRO Pastoral Research Laboratory, Armidale. Resistance in Trichostrongylus spp to levamisole was also confirmed on an adjoining farm. From the results of an experiment where lambs were treated at the recommended dose rate with one or both anthelmintics, it was estimated that 32% of T. colubriformis were resistant to levamisole, 19% to oxfendazole, and 12% to both drugs. Simultaneous administration of levamisole and oxfendazole resulted in an additive anthelmintic effect. Naphthalophos (36.6 to 51.2 mg/kg) was 93% efficient against the multiple resistant strain. The similar histories of anthelmintic usage at the CSIRO Pastoral Research Laboratory and on the northern tablelands of New South Wales generally, suggest that multiple anthelmintic resistance in T. colubriformis may soon emerge as a problem on the northern tablelands.     

Anthelmintic resistance in the field: Changes in resistance status of parasitic populations in response to anthelmintic treatment

Changes in anthelmintic resistance in nematode parasites were monitored in sheep grazing on 2 separate farms, but with the same anthelmintic treatment program, over 16 years. High levels of benzimidazole resistance emerged in Ostertagia and Trichostrongylus spp populations on both farms following 9 years of continuous use of this class of drug. Subsequently, variations in the levels of resistance occurred for the same species between farms and between species on the same farm. A change to levamisole for 2 years resulted in a significant reversion towards benzimidazole susceptibility, but a concomitant rise in levamisole resistance, in Ostertagia on one farm. However, benzimidazole resistance increased rapidly following the re-introduction of oxfendazole into the anthelmintic treatment program. Results from both farms illustrate the pitfalls of using one anthelmintic class for an extended period and provide indirect support for the alternation of anthelmintic classes at approximately yearly intervals.     

MULTIPLE AND MULTIGENERIC ANTHELMINTIC RESISTANCE ON A SHEEP FARM IN KENYA

The anthelmintic efficacy of benzimidazoles (albendazole, fenbendazole and oxfendazole), levamisole, oral ivermectin and closantel was evaluated on a farm in Kenya using faecal egg count reduction test, larval cultures and a controlled slaughter trial. The results of this study indicated simultaneous resistance of Haemonchus contortus against benzimidazoles, levamisole and ivermectin, and of Trichostrongylus colubriformis and Oesophagostomum spp. against levamisole on the same farm. Ivermectin resistance developed to 47% within 15 months of first use. Closantel was effective against the benzimidazoles, levamisole and ivermectin resistant H. contortus.     

A survey of anthelmintic resistance on ten goat farms in the Manawatu region in 1988

A survey of anthelmintic resistance on ten goat farms was carried out. The criterion for resistance was a faecal egg count reduction (FECR) of <90 percent based on arithmetic means of 11 to 19 goats per group. It was found that nine of the ten farms harboured nematodes resistant to oxfendazole when used at 5mg/kg although on two of these, the FECR's were 89.2 percent and 89.8 percent. Post treatment larval cultures indicated Haemonchus, Ostertagia and Trichostrongylus were the resistant genera involved. On none of the ten farms was resistance to oral ivermectin at 0.2mg/kg detected.     

Trichostrongylus colubriformis and Ostertagia circumcincta resistant to levamisole, morantel tartrate and thiabendazole: occurrence of field strains

Field strains of Trichostrongylus colubriformis and Ostertagia circumcincta, designated PF4 and PF5 respectively, were recovered from a farm on which the sole use of levamisole over a preceding 12 year period led to the development of anthelmintic resistance. The results of field observations and preliminary critical trials in both Merino and crossbred sheep showed that both species have varying degrees of resistance to three major anthelmintics; levamisole, morantel tartrate and thiabendazole. Mean worm count reductions for adult T colubriformis (PF4) for therapeutic doses of morantel tartrate, thiabendazole and levamisole in crossbreds were 45.7 per cent, 97.3 per cent and zero respectively, and for Merinos 80.7 per cent, 88.3 per cent and 92.0 per cent respectively. Against O circumcincta the corresponding reductions for crossbreds were 51.4 percent, 95.4 per cent and 20.3 per cent and for Merinos, 52.5 per cent, 73.1 per cent and 29.8 per cent. There was no statistically significant difference in the responses of both parasite species to either levamisole or morantel. This result suggests that resistance to the two chemically unrelated drugs may be co-inherited.     

The prevalence of anthelmintic resistance in sheep nematodes on the central tablelands of New South Wales

A survey was undertaken to assess the prevalence of anthelmintic resistance in sheep nematode populations on 40 commercial farms distributed throughout the central tablelands of New South Wales. Representatives of the 2 major groups of broad spectrum anthelmintics with different modes of action (thiabendazole and levamisole) were used at the manufacturer's recommended dose rates. Efficacy was assessed on the basis of the reduction in faecal strongyle egg counts 7 days after treatment. An efficacy of less than 90% using both anthelmintics was obtained on 4 farms. Thiabendazole had an efficacy of less than 90% on a further 21 farms and levamisole had an efficacy of less than 90% on an additional 4 farms. There was no evidence of anthelmintic resistance on 8 farms, while the remaining 3 had insignificant parasite burdens. Based on larval cultures from faeces, Ostertagia and Trichostrongylus were the most significant species in resistant populations. Haemonchus burdens were sporadic and levels of resistance relatively low. Nematodirus burdens were widespread but no evidence of resistance was detected.     

The efficacy of mixtures of albendazole sulphoxide and levamisole against sheep nematodes resistant to benzimidazole and levamisole

Faecal egg count reduction tests and an anthelmintic efficiency assay were used to assess the efficacy of combinations of albendazole sulphoxide and levamisole against populations of Ostertagia and Trichostrongylus sp. which contained different proportions of worms resistant to both benzimidazole and levamisole anthelmintics. Compared to the effects of either drug alone, significantly greater efficacy was obtained using combinations which included dose rates similar to those recommended for the separate components. At these dose rates, the mixtures reduced mean faecal egg counts by 95% or more, and caused a reduction of 68% in adult Ostertagia sp. and more than 95% for 4th stage Ostertagia and T colubriformis. The increased efficacy of the mixtures could be accounted for by actions of the drugs acting independently.     

Prevalence of anthelmintic resistance on sheep farms in New Zealand

AIM: To establish the prevalence of anthelmintic resistance in parasitic nematodes on sheep farms in New Zealand. METHODS: A cross-sectional prevalence study was conducted, using a standardised faecal nematode egg count (FEC) reduction (FECR) test (FECRT) for ivermectin, at a full (0.2 mg/kg) and half (0.1 mg/kg) dose rate, and albendazole, levamisole and albendazole-levamisole in combination, on 60 lambs (n=10 per group) on farms selected from throughout New Zealand. Farms that conformed with selection criteria were chosen at random (n=80) or with a history of suspected resistance to macrocyclic lactone (ML) anthelmintics (n=32). Resistance to an anthelmintic was inferred when there was <95% reduction in FEC 7-10 days after treatment. Larval cultures were performed for all control groups and for treated groups for which resistance was evident. RESULTS: Of the farms randomly selected, 36% showed > or =95% FECR for all anthelmintics tested; resistance to ivermectin at 0.1 and 0.2 mg/kg liveweight was evident on 36% and 25% of these farms, respectively. Resistance to both ivermectin (0.2 mg/kg) and levamisole was evident on 8/80 (10%) farms, to ivermectin and albendazole on 10/80 (13%) farms, and to ivermectin, levamisole and albendazole on 6/80 (8%) farms. The prevalence of resistance to a half dose of ivermectin tended to be more prevalent on farms with a history of suspected ML resistance (p=0.06). Resistance to albendazole was seen across all the main parasite genera, and to levamisole in Nematodirus, Ostertagia (= Teladorsagia) and Trichostrongylus species. Resistance to ivermectin was dominated by Ostertagia spp, although Cooperia, Nematodirus and Trichostrongylus species were also implicated. CONCLUSION: Anthelmintic resistance in parasitic nematodes of sheep is common in New Zealand. Not only was resistance to albendazole and levamisole common, but resistance to the ML, ivermectin, was at a higher prevalence than expected. Sheep farmers and advisors in New Zealand need to re-evaluate the way they manage parasites, and more research is urgently needed if the steady decline in anthelmintic susceptibility is to be halted.     

Resistance of Trichostrongylus colubriformis to levamisole and morantel: differences in relation to selection history

Two field strains of Trichostrongylus colubriformis were tested by in vitro and in vivo methods for resistance to morantel, levamisole and thiabendazole and compared with an anthelmintic-naive laboratory-passaged strain (McM). One field strain (TAS) was isolated from a dairy goat herd which had experienced severe helminthiasis despite intensive anthelmintic usage. The other (BCK) was isolated from sheep which had been treated solely with levamisole over a 6-year period. The BCK strain had very high levels of both levamisole and morantel resistance. In contrast the TAS strain was resistant to morantel but highly susceptible to levamisole. This finding is contrary to the expectation that selection with morantel automatically confers resistance to levamisole, the converse of which was shown to apply in the BCK strain. Although the TAS strain was exposed to levamisole prior to isolation, examination of the drug's pharmacokinetics in goats indicated that it exerted little if any anthelmintic effect, and therefore selection pressure, on the parasite population. This study suggests that the mechanism of levamisole resistance covers a wide spectrum, and embraces that for morantel. It also suggests that in order to conserve the effectiveness of the levamisole/morantel group of broad spectrum anthelmintics, morantel should be used to the exclusion of levamisole until resistance is detected, at which time levamisole may be introduced to re-establish high levels of control.     

Field studies investigating anthelmintic resistance in young cattle on five farms in New Zealand

AIM: To investigate the efficacy of pour-on anthelmintics against field strains of parasitic nematodes in young cattle on five farms in New Zealand. METHODS: Faecal nematode egg count (FEC) reduction (FECR) tests were carried out on five calf-rearing farms using pour-on formulations of levamisole, ivermectin, eprinomectin, and the simultaneous administration of levamisole and ivermectin. Faecal samples were collected per rectum before treatment and about 7, 14, 21 and 28 days after treatment, for FEC and faecal nematode larval culture. RESULTS: Resistance (i.e. <95% reduction in FEC) of Cooperia oncophora to ivermectin and eprinomectin was identified on all five farms. There was limited evidence of possible emerging resistance in Ostertagia spp to ivermectin but not eprinomectin, in short-tailed larvae of Cooperia spp to ivermectin and eprinomectin, and in Trichostrongylus spp to ivermectin, eprinomectin and levamisole used separately. Levamisole was effective against C. oncophora, but had variable efficacy against Ostertagia spp in the calves in this study. Simultaneous treatment with levamisole and ivermectin pour-on formulations were effective against all genera on all farms. CONCLUSIONS: To effectively manage roundworm parasites in their calves farmers need to be aware of the resistance status of the parasites on their farms. Levamisole is likely to be an effective anthelmintic on most farms at times of the year when the impact of Ostertagia spp is not high. Simultaneous administration of levamisole and ivermectin pour-on anthelmintics to cattle is likely to control both ML-resistant C. oncophora and stages of Ostertagia spp that are not controlled by levamisole alone.     

A microlarval development assay for the detection of anthelmintic resistance in sheep nematodes.

A microlarval development test for the detection of anthelmintic resistance in nematodes is described. Haemonchus contortus, Teladorsagia circumcincta and Trichostrongylus colubriformis eggs were cultured to third stage larvae in the presence of Earle's balanced salt solution, yeast extract and bacteria in a total volume of 150 microliters. Good dose-response data were obtained with thiabendazole, levamisole, pyrantel tartrate and ivermectin allowing the determination of the 50 per cent lethal concentration and of resistance factors when resistant strains were available. The test was found to be accurate, sensitive, easy to carry out and applicable to the routine detection of resistance.     

Avermectin-resistance in gastrointestinal nematodes of Boer goats and Dorper sheep in Switzerland

Anthelmintic resistance in gastrointestinal nematodes among small ruminants is widespread in South Africa and Dorper sheep and Boer goats have been imported into Switzerland from this country on a number of occasions. Therefore, this study aimed to investigate the occurrence of avermectin (AVM) resistant gastrointestinal nematodes (GIN) in these breeds in Switzerland. A total of 24 Boer goat farms and 12 Dorper sheep farms participated in the study. According to the faecal egg count reduction test (FECRT) AVM-resistant GIN populations were confirmed in 7 of the 24 Boer goat farms and suspected in a further 8 farms. Likewise AVM-resistance was confirmed in 2 of 12 Dorper sheep farms and suspected in a further 6 farms. Haemonchus contortus and Trichostrongylus spp. were the dominant resistant species according to larval cultures. In the farms with detected AVM-resistance the animals were additionally treated with levamisole after natural reinfection. With the exception of one farm with a 'close-to cutoff-result' the FECRT gave no indication for resistance against levamisole. The results indicate that AVM-resistance is widespread in Swiss small ruminant farms keeping Boer goats and Dorper sheep. The common tradition of grazing animals from different farms on prealpine and alpine pastures could favour the spread of resistant populations within the country.     

Controlled trials of the anthelmintic oxfendazole in ewes and lambs naturally infected with gastrointestinal nematodes.

Oxfendazole doses at a rate of 5 mg per kg, before or after lambing, reduced nematode egg output to insignificant levels in ewes, most of which were not exposed to re-infection. Ewes treated with oxfendazole had a significantly lower egg output than those treated with levamisole, although the latter anthelmintic was also highly effective. In lambs, oxfendazole at a dose rate of 5 mg per kg, showed 100 per cent efficacy for Ostertagia circumcincta, O trifurcata, Teledorsagia davtiani, Trichostrongylus axei, T vitrinus, T colubriformis, Nematodirus battus, N filicollis, immature Nematodirus, Chabertia ovina, and 93 per cent efficacy for Trichuris spp. Levamisole showed similar efficacies but did not remove Trichuris.     

Prevalence of benzimidazole resistance of nematodes in sheep in The Netherlands

A survey was carried out in The Netherlands to determine the prevalence of benzimidazole resistance in sheep nematodes. It was shown that 47 per cent of the 59 investigated flocks harboured trichostrongylid populations with resistance to benzimidazoles, as demonstrated by an LD50 value of 0.12 micrograms ml-1 thiabendazole or higher in an in vitro egg hatch assay. On these farms Haemonchus contortus was found to be the dominant species. In two flocks resistant Ostertagia and, or, Trichostrongylus species populations were found. Farms with resistance were revisited to determine the anthelmintic efficacy in vivo by means of treatment and egg count. In only four of the 19 flocks which showed resistance in vitro was an efficacy of less than 95 per cent in vivo achieved. This means that there is a discrepancy between the in vivo and in vitro results. Resistance was found more frequently on pure sheep farms than on mixed farms. It is suggested that mixed farms offer more refuge for susceptible H contortus populations.     

Multiple anthelmintic resistance and the possible contributory factors in Beetal goats in an irrigated area (Pakistan)

This paper presents the first report of multiple anthelmintic resistance in the gastrointestinal nematodes of goats and its possible contributory factors in an irrigated area (Pakistan). A total of 18 privately owned Beetal goat flocks were selected in order to determine the anthelmintic resistance against commonly used anthelmintics. Forty to 48 animals from each flock were selected according to their weight and egg count. The three anthelmintics viz., oxfendazole, levamisole and ivermectin, were given to three groups at manufacturer’s recommended dose while one group was kept as untreated control. Anthelmintic resistance was determined through faecal egg count reduction and egg hatch tests while assessment of the contributory factors of anthelmintic resistance was measured through the rural participatory approach. Faecal egg count reduction test revealed high prevalence of anthelmintic resistance (83.3%) and it was either single (levamisole) or multiple (oxfendazole and levamisole). Egg hatch test confirmed the resistance against oxfendazole as detected with faecal egg count reduction test. None of the goat flocks was resistant to ivermectin. Copro-cultures revealed that Haemonchus contortus, Trichostrongylus colubriformis and Teladorsagia circumcincta were the most common species exhibiting resistance to levamisole and oxfendazole. Step-wise logistic regression of the data on worm control practices revealed significant role of under-dosing, low-protein diets, healthcare supervision by the traditional healers and mass treatments.     

Survey of anthelmintic resistance in Western Australian sheep flocks 1. Prevalence

Between July 1981 and December 1983, 116 randomly selected sheep farms in the south west of Western Australian were surveyed for resistance to anthelmintics. A faecal worm egg count reduction test was carried out on each farm. Anthelmintics tested were thiabendazole (44 mg/kg) and levamisole (7.5 mg/kg) given by intra-ruminal injection and comparisons were made with an untreated group on each farm. Successful tests were carried out on 84 farms and 68% of these had resistant worms present. The prevalence of thiabendazole resistant populations was for H. contortus 18%; Teladorsagia, 41% and Trichostrongylus, 48% and for levamisole resistant populations H. contortus, 10%; Teladorsagia, 41%; Trichostrongylus, 24%, and Nematodirus, 10%. Multiple resistant populations were found on 17% of farms. Although the distribution of nematode genera varied between the 400 to 750 mm and the greater than 750 mm rainfall zones there was no significant difference in the prevalence of resistance between zones. About one third of resistant populations were severely resistant (less than 60% reduction). It is likely that resistant worms were present on many farms without causing clinical disease and continued anthelmintic selection pressure will result in further development of resistance.     

Anthelmintic resistance in Australian sheep nematode populations

SUMMARY The resistance status of gastro–intestinal nematodes to anthelmintics was evaluated on 881 sheep farms throughout Australia during 1991–92. Resistance was shown to be widespread. Overall, 85% of farms had sheep infected with nematodes resistant to benzimidazole, 65% to levamisole and 34% to combination (benzimidazole + levamisole) products. Resistance to ivermectin was not detcted. On only 9% of farms did all anthelmintic groups reduce egg counts by greater than or equal to 95%. The culture of faeces from untreated sheep showed Telodorsagia circumcincta, Trichostrongylus spp, Chabertia ovina and Haemonchus contortus to be the principal species. The nature and prevalence of resistance was not significantly correlated with stocking rate. However, resistance to combination products was almost twice as prevalent on farms in areas with an average annual rainfall of greater than 500 mm.     

The comparative efficacy of four broad spectrum anthelmintics against some experimentally induced trichostrongylid infections in sheep and goats

A controlled slaughter trial was undertaken to compare the efficacies of oxfendazole (5 mg/kg), morantel citrate (10 mg/kg), levamisole (8 mg/kg) and ivermectin (0.2 mg/kg) against experimentally induced infections of adult Haemonchus contortus, Ostertagia spp., Trichostrongylus colubriformis and Cooperiacurticei in sheep and goats. Ivermectin and oxfendazole achieved similar levels of efficacy in both hosts against all four worm genera as did levamisole and mortantel against H. contortus and C. curticei. Against Ostertagia spp. and T. colubriformis, however, the latter two drugs were less effective in goats than sheep. Neither the numbers of Ostertagia spp. removed from goats by levamisole (81% reduction) nor the numbers of T. colubriformis removed from goats by morantel (56% reduction) were statistically significant (P>0.05).