The effect of ruminoreticulum bypass in yarded lambs on
the ef®cacy of oxfendazole against resistant
Trichostrongylus
spp. helminths
N.D. Sargison
*, K.J. Stafford, D.M. West, W.E. Pomroy
Institute of Veterinary, Animal and Biomedical Sciences, Massey University, Palmerston North, New Zealand
Accepted 10 July 1999
Abstract
An observational study was performed to investigate the effects of yarding and ruminoreticulum bypass on the ef®cacy of
oxfendazole against resistant Trichostrongylus spp. helminths. Ruminoreticulum bypass was observed in 9-month old
Perendale lambs using video-taped ¯uoroscopy and the ef®cacy of oxfendazole was estimated using the faecal egg count reduction test. Yarding and withholding feed for 24 h before drenching with oxfendazole signi®cantly enhanced the faecal egg
count reduction for resistantTrichostrongylusspp. parasites (p< 0.05), but ruminoreticulum bypass of the drench in the yarded
animals had no negative effect on anthelmintic ef®cacy (p> 0.05). The effect of ruminoreticulum bypass on the ef®cacy of
oxfendazole may depend on the resistant parasite species present. The positive effects of yarding sheep for 24 h before
drenching, on the ef®cacy of oxfendazole against resistantTrichostrongylusspp., probably outweigh any negative effects of
ruminoreticulum bypass. However further studies are required, with different resistant parasite genera present, before ®rm
recommendations can be made.#2000 Elsevier Science B.V. All rights reserved.
Keywords:Oxfendazole; Trichostrogylus; Ruminoreticulum
1. Introduction
When lambs over the age of 6 months are drenched soon after gathering from pasture, oral anthelmintics do not normally pass directly to the abomasum (Sar-gison et al., 1998). However, yarding and withdrawal of feed but not water for 24 h before drenching has been shown to stimulate ruminoreticulum bypass in approximately 35% of 9-month old lambs (Sargison et al., 1998). This high incidence of ruminoreticulum
bypass would be expected to in¯uence adversely the ef®cacy of oxfendazole (Prichard and Hennessy, 1981), and appears to contradict the recommendation (Ali and Hennessy, 1995b) that sheep should be yarded for 12±24 h before drenching. However, it is possible that in yarded sheep the positive effect on anthelmintic ef®cacy of the residence time of the drug±digesta complex in the rumen may outweigh any negative effect of ruminoreticulum bypass. The aim of this study was to investigate the hypothesis that the positive effect of yarding sheep and withdrawal of feed for 24±36 h before drenching with oxfendazole is
*Corresponding author.
reduced when the drench bypasses the ruminoreticu-lum.
2. Materials and methods
A ¯ock of 9-month old Perendale (New Zealand RomneyCheviot) lambs with a history of benzimi-dazole resistance was used for this study. Soon after removal from pasture, 13 individually identi®ed lambs were selected at random, weighed and drenched with 5 mg/kg oxfendazole (Systamex, Mallinckrodt). Fae-cal samples were collected from each animal at the time of drenching and 8 and 13 days post-treatment. A further 36 individually tagged, randomly-selected lambs were faecal sampled and then yarded for 24 h without feed but with free access to water, before drenching to the back of the mouth with 5 mg/kg oxfendazole (Systamex, Mallinckrodt) mixed with 49% w/v barium sulphate suspension to a volume of 3 ml/10 kg. The distribution of the oxfendazole between the ruminoreticulum and abomasum was determined by video-taped ¯uoroscopy (Sargison et al., 1998). Faecal samples were collected from each lamb 8 and 13 days after drenching.
Faecal egg counts were performed on each sample using the modi®ed McMaster technique where each egg counted represents 50 eggs per gram. The faecal egg count reduction was calculated for the 13 lambs which were drenched soon after removal from pasture, for seven yarded lambs in which >80% (20%) of the drench entered the abomasum, and for 26 yarded lambs in which all of the drench entered the ruminor-eticulum. Three animals in which a proportion of the drench <80% (20%) entered the abomasum were removed from the study.
Bulk pre- and post-treatment faecal cultures were incubated at 278C for 7 days to provide infective larvae for identi®cation. Faecal egg count reductions were calculated for the resistant parasite genus by allocating egg counts to genera based on the results of these larval cultures (McKenna, 1996, 1997).
Individual faecal egg count reductions for Trichos-trongylusspp. were calculated. A one way analysis of variance by ranks (non-parametric) was performed for these reductions using the Kruskal±Wallis test. Com-parisons were then made between groups by the Mann±Whitney test, using the Statistical Product and Service Solutions software, version 8.0 (SPSS).
3. Results
3.1. Lambs drenched with oxfendazole soon after removal from pasture
The pre- and post-treatment faecal egg counts are presented in Table 1. The mean reduction in strongylid faecal egg counts (exceptNematodirusspp.) 8 and 13 days after drenching were 77% and 53% respectively, which con®rmed the presence of benzimidazole resis-tance.
The bulk pre- and post-treatment larval culture results are presented in Table 2. The mean faecal egg count reductions forTrichostrongylusspp., which were calculated using the pre- and post-treatment larval culture results, 8 and 13 days after drenching with 5 mg/kg of oxfendazole were 67% and 34% respectively.
3.2. Lambs drenched with oxfendazole 24 h after removal from pasture
The mean reduction in strongylid faecal egg counts of 26 lambs, 8 and 13 days after drenching to the ruminoreticulum were 85% and 73% respectively (Table 1). The mean reduction in Trichostrongylus spp. faecal egg counts, 8 and 13 days after drenching to the ruminoreticulum were 78% and 62% respec-tively.
The mean reduction in strongylid faecal egg counts of seven lambs, 8 and 13 days after drenching to the abomasum were 75% and 73% respectively (Table 1). The mean reduction in Trichostrongylus spp. faecal egg counts, 8 and 13 days after drenching to the abomasum were 65% and 62% respectively.
3.3. Summary of results
Yarding for 24 h before drenching with 5 mg/kg of oxfendazole signi®cantly improved the reduction in Trichostrongylusspp. faecal egg counts 13 days after drenching from 34% (off pasture) to 62% (yarded) (p< 0.05). In the lambs that had been yarded before drenching, ruminoreticulum bypass had no signi®cant effect (p> 0.05) on the faecal egg count reduction of Trichostrongylusspp.
Pre- and post-treatment strongylid faecal egg counts (eggs/gram) of lambs drenched with 5 mg/kg oxfendazole soon after removal from pasture and of lambs which had been yarded for 24 h before drenching to the ruminoreticulum or abomasum
Off pasture Yarded/ruminoreticulum Yarded/abomasum
Pre-treatment
8 days post-treatment
13 days post-treatment
Pre-treatment
8 days post-treatment
13 days post-treatment
Pre-treatment
8 days post-treatment
13 days post-treatment
600 300 250 2050 250 550 1100 300 300
100 0 750 950 300 50 450 250 250
1300 150 800 1250 150 2800 1350 50 350
600 0 300 1150 100 50 1550 100 200
1900 400 1000 450 250 100 450 200 100
250 200 200 3800 250 50 1650 650 500
300 No samplea 300 6350 150 50 450 200 200
1150 100 450 450 150 250
600 600 400 1050 300 No samplea
1300 200 50 3250 150 350
50 250 500 700 750 125
1200 150 200 450 200 No samplea
4250 550 1200 1400 300 700
600 300 400
850 100 No samplea 2100 200 300
450 250 No samplea
450 100 200
1350 150 250 1850 200 150 1150 400 250
550 0 250
450 200 200
1100 200 900 1000 200 150
1000 0 50
Mean 1046 242 492 1392 215 372 1000 250 271
Reduction 77% 53% 85% 73% 75% 73%
Reduction of Trichostron-gylusspp.
67% 34% 78% 62% 65% 62%
aNo faeces were present in the rectum and a sample could not be obtained.
N.D.
Sar
gison
et
al.
/
Small
Ruminant
Resear
ch
35
(2000)
213±217
4. Discussion
Yarding for 24 h before drenching with 5 mg/kg oxfendazole had a positive effect on the day 13 reduction in strongylid faecal egg counts (excluding Nematodirus spp.), although this effect was not sta-tistically signi®cant. Yarding lambs for 24 h before drenching signi®cantly improved theTrichostrongylus spp. faecal egg count reduction from 34% (off pasture) to 62% (yarded) (p< 0.05). These results support the recommendation of Ali and Hennessy (1995b); that the ef®cacy of oxfendazole against resistant parasites could be enhanced in ®eld conditions ``by holding sheep in a paddock or yard with little or no feed for 12±24 h before and after drenching''.
In the lambs, which had been yarded before drench-ing, ruminoreticulum bypass had no signi®cant effect on the reduction in faecal egg counts. However, Prichard and Hennessy (1981) showed that when 12-month old sheep were infected with a known number of benzimidazole resistantH. contortus and T. colubriformisbefore drenching with oxfendazole, the faecal egg counts were reduced to a signi®cantly greater extent (p< 0.05) in six sheep showing sub-stantial ruminoreticulum bypass than in ®ve sheep showing minimal bypass. The post mortem counts of H. contortus, but notT. colubriformis, were negatively correlated (p< 0.05) with ruminoreticulum bypass (Prichard and Hennessy, 1981). It is possible, there-fore, that the extended plasma kinetics of oxfendazole may be more important for the control of resistant, dose-limiting, haematophagous Haemonchus spp. than for the control of mucosal feeding Trichostron-gylusspp., which included the predominant resistant species in the current study.
The absence of any negative effect of ruminoreti-culum bypass on anthelmintic ef®cacy should be interpreted with caution, due to the limitations of
the faecal egg count reduction test and the resistant helminth species present. However, the result does raise a question about the importance of the ruminor-eticulum residence time of oxfendazole to its ef®cacy against resistant helminths. The extended plasma kinetics and improved ef®cacy of oxfendazole in animals which have been yarded for a period of 12±36 h before drenching has been largely attributed to the inverse relationship between feed intake and rumen residence time of particle-bound drug (Ali and Chick, 1992; Ali and Hennessy, 1995a,b). However, if rumen residence time alone is responsible for the improved drug ef®cacy in yarded animals, ruminor-eticulum bypass would have been expected to result in reduced anthelmintic ef®cacy. It is possible, therefore, that the extended plasma kinetics of oxfendazole in sheep which have been yarded for 24 h before drench-ing may be partly due to enhanced small intestinal absorption, hepatic conjugation, or large intestinal bacterial hydrolysis of the drug associated with reduced intestinal motility, irrespective of its rumen residence time.
On the basis of the results of previous studies (Sargison et al., 1998) it could be assumed that ruminoreticulum bypass did not occur in the sheep which were drenched soon after removal from pasture. Suppression of strongylid egg production between 8 and 13 days by oxfendazole was, therefore, only observed when the drench was deposited mostly in the ruminoreticulum, but not when the drench was deposited in the abomasum. The relevance of this observation is unknown.
The hypothesis was disproved; that the positive effect of yarding sheep for 24±36 h before drenching with oxfendazole is reduced when the drench bypasses the ruminoreticulum. However, only resistant Trichos-trongylusspp. were present in this study and a differ-ent situation may pertain to other resistant strongylid genera.
References
Ali, D.N., Chick, B.F., 1992. The effect of feed type on the pharmacokinetic disposition of oxfendazole in sheep. Res. Vet. Sci. 52, 382±383.
Ali, D.N., Hennessy, D.R., 1995a. The effect of level of feed intake on the pharmacokinetic disposition of oxfendazole in sheep. Int. J. Parasitol. 25, 63±70.
Table 2
Bulk pre- and post-treatment larval culture results Pre-treatment Post-treatment
69%Trichostrongylusspp. 97%Trichostrongylusspp. 17%Haemonchusspp. 2%Chabertiaspp. 9%Ostertagiaspp. 1%Haemonchusspp. 4%Cooperiaspp.
1%Chabertia/Oesophagostomumspp.
Ali, D.N., Hennessy, D.R., 1995b. The effect of reduced feed intake on the ef®cacy of oxfendazole against benzimidazole resistant
Haemonchus contortusand Trichostrongylus colubriformisin sheep. Int. J. Parasitol. 25, 71±74.
McKenna, P.B., 1996. Potential limitations of the undifferentiated faecal egg count reduction test for the detection of anthelmintic resistance in sheep. N. Z. Vet. J. 44, 73±75.
McKenna, P.B., 1997. Further potential limitations of the undifferentiated faecal egg count reduction test for the detection of anthelmintic resistance in sheep. N. Z. Vet. J. 45, 244±246.
Prichard, R.K., Hennessy, D.R., 1981. Effect of oesophageal groove closure on the pharmacokinetic behaviour and ef®cacy of oxfendazole in sheep. Res. Vet. Sci. 30, 22±27.