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Addressing sustainable sheep farming: Application of a targeted selective treatment approach for anthelmintic use on a commercial farm
Small Ruminant Research 110 (2013) 100–103
Contents lists available at SciVerse ScienceDirect
Small Ruminant Research journal homepage: www.elsevier.com/locate/smallrumres
Addressing sustainable sheep farming: Application of a targeted selective treatment approach for anthelmintic use on a commercial farm夽 V. Busin a,∗ , F. Kenyon b , N. Laing c , M.J. Denwood a , D. McBean b , N.D. Sargison d , K. Ellis a a Scottish Centre for Production Animal Health and Food Safety, School of Veterinary Medicine, College of Medical Veterinary and Life Sciences, University of Glasgow, Bearsden Road, Glasgow G61 1QH, United Kingdom b Moredun Research Institute, Pentlands Science Park, Bush Loan, Penicuik EH26 0PZ, United Kingdom c Clyde Veterinary Group, New Lanark Market, Lanark ML11 9SZ, United Kingdom d University of Edinburgh, Royal (Dick) School of Veterinary Studies, Easter Bush Veterinary Centre, Roslin, Midlothian EH25 9RG, United Kingdom
a r t i c l e
i n f o
Article history: Available online 5 December 2012 Keywords: Anthelmintic resistance Growth Lamb Nematode Sheep Targeted selective treatment
a b s t r a c t Sustainable control of nematode parasites in small ruminant production is a worldwide ambition. Development of anthelmintic resistance can severely impair small ruminant production. A practical approach to reduce selection pressure for anthelmintic resistance is to treat only a proportion of the flock (Targeted Selective Treatment), leaving a proportion of the nematode population untreated. The aim of this study was to compare the sustainability and efficacy of a performance-based marker, the Happy FactorTM , a monitor of nutrient utilisation efficiency, with a routine whole flock anthelmintic treatment. In a commercial flock in the South West of Scotland, 183 Texel cross lambs were split into two matched but co-grazing groups: one group managed as routinely for the farm (RT group) and the other subjected to targeted selective treatment (TST group). All lambs from the RT group were drenched every 6 weeks during the grazing season, while anthelmintic administration in the TST group was restricted to animals that failed to reach pre-determined weight gain targets, based on an estimate of their efficiency of gross energy utilisation. Animal performance and parasitological data were recorded every two weeks. In the 20 week period of the study, anthelmintic treatments were reduced by approximately 50% in the TST group compared to a routine anthelmintic administration that would have been applied, whilst epg counts were always <500 throughout the study in both groups. Finally, there was no discernible difference in the mean bodyweight gain between the two groups. Crown Copyright © 2012 Published by Elsevier B.V. All rights reserved.
1. Introduction Parasitic infections cause significant health problems and decreased productivity in livestock throughout the
夽 This paper is part of the special issue entitled “Lectures of the 1st European Conference on Small Ruminant Health Management”, held in Athens, Greece, October 2011. Guest Edited by G.C. Fthenakis. ∗ Corresponding author. E-mail address: [email protected] (V. Busin).
world. In the United Kingdom, the problems caused by them appear to increase in the future, as the trend for warmer, wetter winters facilitates more rapid nematode development on pasture (Kenyon et al., 2009a; Morgan and van Dijk, 2012). Nematodes of sheep are currently controlled by administration of anthelmintics (Sargison, 2011, 2012); however, suppressive control strategies can select strongly for the development of anthelmintic resistant in parasites (Taylor, 2012), which threatens sustainability of sheep farming worldwide (Papadopoulos et al., 2012; Torres-Acosta et al., 2012). A major determinant of the rate
0921-4488/$ – see front matter. Crown Copyright © 2012 Published by Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.smallrumres.2012.11.013
V. Busin et al. / Small Ruminant Research 110 (2013) 100–103
2. Materials and methods 2.1. Experimental design In total, 183 spring-born Texel-cross lambs were included in the study. At the age of approx. 6 weeks, all lambs were fitted with an electronically readable ear tag (Allflex, DFW airport, TX, USA) and treated with fenbendazole (Panacur; MSD Animal Health, Summit, NJ, USA) at the dose rate of 5 mg kg−1 bodyweight (bw), to clear spring Nematodirus spp. Lambs were assigned at random to two treatment groups, a routine treatment group (RT group) and a targeted selective treatment group (TST group), which were balanced for bodyweight, sex and numbers of single/twin/triplet lambs. Ten lambs from the RT group and 17 lambs from the TST group died during the first 2 months of life and have not been considered into the data management of the study. All lambs in the RT group were treated with ivermectin oral drench (Oramec; Merial Animal Health, Duluth, GE, USA) at the dose rate of 0.2 mg kg−1 bw, every 6 weeks (6th, 12th and 18th week of the study), following the routine health management in that farm. Treatments in the TST group were based on the identification of individual animals, which were likely to benefit from anthelmintic intervention using the decision
100 90
Number of lambs in the study
of development of anthelmintic resistance is the proportion of the parasite population exposed to anthelmintics (Martin et al., 1981). Treating only animals in need of therapy (targeted selective treatment) has been proposed to slow development of anthelmintic resistance, based on the recognised importance of the refugia concept (Van Wyk, 2001). Methods suggested to selectively target anthelmintic treatments range from visual inspection to parasite-based or pathophysiological markers; an ideal targeted selective treatment indicator would be cost-effective, simple to use, require minimal operator training and allow treatment decisions to be made ‘sheep-side’ (Kenyon et al., 2009b). A variety of indicators have been tested in recent years, with the FAMACHA chart for the control of Haemonchus contortus (Van Wyk and Bath, 2002) and milk yield in dairy goats (Hoste et al., 2002, 2012) internationally recognised as valid diagnostic markers. In the Scottish climate, the predominant parasite genera detected on farms are Teladorsagia circumcincta and Trichostrongylus spp. (Bartley et al., 2003), the major effects of which are reduction in voluntary food intake and reduced feed conversion efficiency (Coop et al., 1977). This is of particular significance, as sheep enterprises in Scotland are mainly based on meat production. In this context, bodyweight gain could be a sensitive marker, as a major factor affecting performance in parasitised animals is anorexia and its use is relevant to farm economics. Moreover, the reduction in bodyweight gain occurs early in infection, prior to the appearance of clinical signs (Coop et al., 1977). Recent experimental work has demonstrated promise for the targeted selective treatment approach, by using production efficiency as the individual animal treatment indicator (Greer et al., 2009). The present study aimed to apply targeted selective treatment, by using the Moredun-developed production efficiency based decision support system, Happy FactorTM (which is based on lamb growth rates) in a commercial setting. The intention was to study applicability of the use of bodyweight gain as a targeted selective treatment indicator, in comparison to the standard anthelmintic administration practice on a commercial farm, by quantifying the number of anthelmintic treatments and assessing lamb production.
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Week of the study Fig. 1. Progressive decrease of numbers of lambs from the study, as they were withdrawn for sale when they reached the desired bodyweight (>40 kg); 8 animals in the routine anthelmintic treatment group (RT group, marked with ) and 5 lambs in the targeted selective anthelmintic treatment group (TST group, marked with ) were maintained throughout a 20 week study period. support model developed by Moredun researchers (Greer et al., 2009); minimum bodyweight gains that were required to achieve the suggested efficiency threshold of 0.66, were estimated for each animal within the TST regime prior to each fortnightly visit and any animal that had not reached that target received an anthelmintic treatment with ivermectin oral drench (Oramec; Merial Animal Health, Duluth, GE, USA) at the dose rate of 0.2 mg kg−1 bw. Field efficacy of anthelmintics on the farm had been confirmed prior to the study, by using the faecal egg count reduction test (Coles et al., 1992), in which no evidence of anthelmintic resistance had been detected, with efficacy for fenbendazole, levamisole and ivermectin reaching 97.0%, 99.7% and 99.8%, respectively. All lambs grazed on the same pasture until they reached the desired bodyweight (>40 kg), at which point, if sold, they were removed from the study. Eight animals in the RT group and five lambs in the TST group were maintained throughout the study, as they were to be maintained in the flock as replacement breeding animals (Fig. 1); proportion of lambs withdrawn did not differ significantly among the two groups (P > 0.21). Lamb bodyweight was measured at fortnightly intervals throughout the grazing season, for a total of 20 weeks. Faecal samples were collected directly from the rectum from all animals in the TST group, as well as from 10% of animals in the RT group, for faecal epg counting, as detailed by Christie and Jackson (1982). In addition, pasture mass (expressed in kg dry matter [DM] hectare−1 [ha−1 ]) was measured every two weeks, by using a Grassmaster II pasture probe (Tru-test Ltd., Auckland, New Zealand) that had been calibrated to local conditions (R2 = 0.80, n = 49). Pasture quality was visually estimated at the time of pasture mass measurements, whilst data for ambient temperature were collected from the United Kingdom’s Meteorological Office. The data were used to calculate the minimum bodyweight gain that might have been achieved by each animal at each sampling point, as described by Greer et al. (2009). 2.2. Statistical analysis The number of anthelmintic administrations per animal in the RT group was compared to the number of anthelmintic administrations per animal the TST group, using a paired Wilcoxon signed-rank test. Because of the difficulty in directly comparing RT and TST groups, due to progressive reduction in the number of lambs in each group, observed number of treatments in the TST group was also compared to the estimated number of administrations that would have been given in the same group under routine management conditions. The Wilcoxon signed-rank test was used to compare time to slaughter between RT and TST groups. An auto-regressive generalised linear model (GLAMM), with normal response distribution was used to describe the bodyweight gain data, with fixed effects of sex and RT versus TST group. The model was fitted to the data using Bayesian MCMC.
V. Busin et al. / Small Ruminant Research 110 (2013) 100–103
Table 1 Number of lambs and frequency of anthelmintic administration in a routine treatment group (RT group) and a targeted selective treatment group (TST group) in a sheep flock throughout a 20 week study period. Frequency of treatment
Number of lambs RT group n
TST group
%
n
%
No treatment Once Twice Thrice
6 46 32 11
6 48 34 12
33 43 9 3
38 49 10 3
Total lambs
95
100
88
100
Total number of anthelmintic administrations
143
70
Cumulative bodyweight gain of lambs (kg)
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35 30 25 20 15 10 5 0 0
4
6
8
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12
13
16
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20
Week of the study Fig. 3. Cumulative weight gain (kg) in lambs in a routine anthelmintic treatment group (RT group, marked with ) or in a targeted selective anthelmintic treatment group (TST group, marked with ) throughout a 20 week study period.
4. Discussion 3. Results In total, 143 anthelmintic administrations were carried out in lambs of RT group and 70 anthelmintic administrations were carried out in lambs of TST group (P < 0.001). The estimated number of anthelmintic administrations that would have been carried out in lambs of TST group under the same routine programme, as in lambs of RT group, was 139 (P < 0.001) (Table 1). Faecal nematode egg counts in the two groups are shown in Fig. 2. Their pattern was similar in the two groups, with higher mean epg counts recorded in TST group lambs (110 epg versus 57 epg in RT group lambs). Cumulative bodyweight gain was similar in the two groups throughout the study (Fig. 3). Mean bodyweight gain (±standard error of the mean) for all lambs into each group, across all sampling points was 263 (±6.2) and 257 (±7.1) g day−1 for RT group and TST group lambs, respectively. By using the statistical model of daily bodyweight gain, we found a 0.609 probability that growth rate was lower in lambs of the TST group than in those of the RT group and a 0.391 probability of the converse; moreover, the probability that female lambs had a lower growth rate than male lambs was 0.988.
Lamb faecal egg counts
200 180 160 140 120 100 80 60 40 20 0 4
6
8
10
12
14
16
18
20
Week of the study Fig. 2. Mean faecal nematode epg counts in lambs in a routine anthelmintic treatment group (RT group, marked with ) or in a targeted selective anthelmintic treatment group (TST group, marked with ) throughout a 20 week study period; arrows on the graph indicate times of anthelmintic treatment carried out in the RT group.
The concept of leaving a proportion of animals untreated, with the aim to maintain parasite populations in refugia is now widely accepted as the best means of preserving anthelmintic susceptibility within the parasite population (Van Wyk, 2001; Besier, 2008; Jackson and Waller, 2008; Jackson et al., 2009). However, the key matter, which has so far delayed the application of this concept, is absence of a convenient and accurate method to identify animals suffering from levels of infection causing detectable production losses or adverse health effects (Malan et al., 2001). Previous studies have shown that the main impact of parasites, such as T. circumcincta or Trichostrongylus spp., is reflected in reduced bodyweight gain (Sykes and Coop, 1976, 1977). Animal performance is the factor of main interest to farmers, especially in mutton-type production systems. Because of that and as daily bodyweight gain can be easily and objectively measured in field situations, the Happy FactorTM decision support system (Greer et al., 2009) has been developed, to estimate target weight gain for individual animals. Animals that fail to reach the calculated target weight receive an anthelmintic treatment, leaving those who have achieved the expected performance untreated. Although this approach may appear effective, it has not been tested extensively in clinical situations. The objective of the present study was, therefore, to study the applicability of this approach, using short-interval weight changes, as a reliable indicator of subclinical parasitism in a commercial farm. Such an approach was considered to be feasible if it would sustain two main targets: (a) significant reduction in the number of anthelmintic administrations and (b) absence of adverse effects on animal performance. Use of targeted selective treatments resulted in a reduction by about 50% in number of anthelmintic administrations. Moreover, number of animals that did not receive any anthelmintic treatment was higher in the TST group (33% of animals in the group versus 6% of animals in the RT group). Despite the reduced number of anthelmintic administrations, mean epg counts during the study never exceeded 500 epg, considered to be a clinically important threshold (Love and Hutchinson, 2003). According to mathematical models by Barnes et al. (1995), at least 20% of animals should be left untreated throughout the
V. Busin et al. / Small Ruminant Research 110 (2013) 100–103
grazing season, in order potentially reduce development of anthelmintic resistance. Hence, the current approach may be usefully applied. Targeted anthelmintic administrations did not have any adverse effects on lamb growth. Both groups performed similarly, with comparable weight gains during the study period and with no difference in time to reach slaughter weight. Demonstration of the feasibility of targeted anthelmintic administrations in a flock is a first step in developing and implementing anthelmintic programmes, as part of flock health management. However, it is noteworthy that farmers still have varying opinions regarding the practicality and usefulness of the approach, which may not always coincide with those of the scientific community (Berrag et al., 2009; Cabaret et al., 2009). 5. Concluding comments It is concluded that use of production efficiency as an indicator for targeted selective anthelmintic administrations is suitable for commercial farm settings. The approach presents a valid tool to slow down development of anthelmintic resistance, by reducing the number of anthelmintic treatments required to maintain animal performance. Conflict of interest statement The authors declare that no financial or personal relationship with other people or organisations could have inappropriately influenced our work. Acknowledgement The authors gratefully acknowledge the help and cooperation of staff at Moredun Research Institute and Merial Animal Health for material supply. References Barnes, E.H., Dobson, R.J., Barger, I.A., 1995. Worm control and anthelmintic resistance: adventures with a model. Parasitol. Today 11, 56–63. Bartley, D.J., Jackson, E., Johnston, K., Coop, R.L., Mitchell, G.B.B., Sales, J., Jackson, F., 2003. A survey of anthelmintic resistant nematode parasites in Scottish sheep flocks. Vet. Parasitol. 117, 61–71. Berrag, B., Ouzir, M., Cabaret, J., 2009. A survey on meat sheep farms in two regions of Morocco on farm structure and the acceptability of the targeted selective treatment approach to worm control. Vet. Parasitol. 164, 30–35. Besier, B., 2008. Targeted treatment strategies for sustainable worm control in sheep. Trop. Biomed. 25, 9–17. Cabaret, J., Benoit, M., Laignel, G., Nicourt, C., 2009. Current management of farms and internal parasites by conventional and organic meat sheep French farmers and acceptance of targeted selective treatments. Vet. Parasitol. 164, 21–29.
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Christie, M., Jackson, F., 1982. Specific identification of strongyle eggs in small samples of sheep faeces. Res. Vet. Sci. 32, 113–117. Coles, G.C., Bauer, C., Borgsteede, F.H.M., Geerts, S., Klei, T.R., Taylor, M.A., Waller, P.J., 1992. World Association for the Advancement of Veterinary Parasitology (W.A.A.V.P.) methods for the detection of anthelmintic resistance in nematodes of veterinary importance. Vet. Parasitol. 44, 35–44. Coop, R.L., Sykes, A.R., Angus, K.W., 1977. The effect of a daily intake of Ostertagia circumcincta larvae on body weight, food intake and concentration of serum constituents in sheep. Res. Vet. Sci. 23, 76–83. Greer, A.W., Kenyon, F., Bartley, D.J., Jackson, E.B., Gordon, Y., Donnan, A.A., McBean, D.W., Jackson, F., 2009. Development and field evaluation of a decision support model for anthelmintic treatments as part of a targeted selective treatment (TST) regime in lambs. Vet. Parasitol. 164, 12–20. Hoste, H., Le Frileux, Y., Pommaret, A., 2002. Comparison of selective and systematic treatments to control nematode infection of the digestive tract in dairy goats. Vet. Parasitol. 106, 345–355. Hoste, H., Sotiraki, S., Torres-Acosta, J.F.J., 2012. Control of endoparasitic nematode infections in goats. Vet. Clin. North Am. Food Anim. Pract. 27, 163–173. Jackson, F., Bartley, D., Bartley, Y., Kenyon, F., 2009. Worm control in sheep in the future. Small Rumin. Res. 86, 40–45. Jackson, F., Waller, P., 2008. Managing refugia. Trop. Biomed. 25, 34–40. Kenyon, F., Greer, A.W., Coles, G.C., Cringoli, G., Papadopoulos, E., Cabaret, J., Berrag, B., Varady, M., Van Wyki, J.A., Thomas, E., Vercruysse, J., Jackson, F., 2009b. The role of targeted selective treatments in the development of refugia-based approaches to the control of gastrointestinal nematodes of small ruminants. Vet. Parasitol. 164, 3–11. Kenyon, F., Sargison, N.D., Skuce, P.J., Jackson, F., 2009a. Sheep helminth parasitic disease in south eastern Scotland arising as a possible consequence of climate change. Vet. Parasitol. 163, 293–297. Love, S.C.J., Hutchinson, G.W., 2003. Pathology and diagnosis of internal parasites in ruminants. In: Gross Pathology of Ruminants, Proceedings 350, Post Graduate Foundation in Veterinary Science, University of Sydney, pp. 309–338 (Chapter 16). Malan, F.S., Van Wyk, J.A., Wessels, C.D., 2001. Clinical evaluation of anaemia in sheep: early trials. Onderstepoort J. Vet. Res. 68 (3), 165–174. Martin, P.J., Le Jambre, L.F., Claxton, J.H., 1981. The impact of refugia on the development of thiabendazole resistance in Haemonchus contortus. Int. J. Parasitol. 11, 35–41. Morgan, E.R., van Dijk, J., 2012. Climate and the epidemiology of gastrointestinal nematode infections of sheep in Europe. Vet. Parasitol. 189, 8–14. Papadopoulos, E., Gallidis, E., Ptochos, S., 2012. Anthelmintic resistance in sheep in Europe: a selected review. Vet. Parasitol. 189, 85–88. Sargison, N.D., 2011. Pharmaceutical control of endoparasitic helminth infections in sheep. Vet. Clin. North Am. Food Anim. Pract. 27, 139–156. Sargison, N.D., 2012. Pharmaceutical treatments of gastrointestinal nematode infections of sheep – future of anthelmintic drugs. Vet. Parasitol. 189, 79–84. Sykes, A.R., Coop, R.L., 1976. Intake and utilisation of food by growing lambs with parasitic damage to the small intestine caused by daily dosing with Trichostrongylus colubriformis larvae. J. Agric. Sci. 86, 507–515. Sykes, A.R., Coop, R.L., 1977. Intake and utilisation of food by growing sheep with abomasal damage caused by daily dosing with Ostertagia circumcincta larvae. J. Agric. Sci. 88, 671–677. Taylor, M.A., 2012. Emerging parasitic diseases of sheep. Vet. Parasitol. 189, 2–7. Torres-Acosta, J.F.J., Mendoza-de-Gives, P., Aguilar-Caballero, A.J., CuéllarOrdaz, J.A., 2012. Anthelmintic resistance in sheep farms: update of the situation in the American continent. Vet. Parasitol. 189, 89–96. Van Wyk, A., 2001. Refugia – overlooked as perhaps the most potent factor concerning the development of anthelmintic resistance. Onderstepoort J. Vet. Res. 68 (1), 55–67. Van Wyk, J.A., Bath, G.F., 2002. The FAMACHA© system for managing haemonchosis in sheep and goats by clinically identifying individual animals for treatment. Vet. Res. 33, 509–529.
Contents lists available at SciVerse ScienceDirect
Small Ruminant Research journal homepage: www.elsevier.com/locate/smallrumres
Addressing sustainable sheep farming: Application of a targeted selective treatment approach for anthelmintic use on a commercial farm夽 V. Busin a,∗ , F. Kenyon b , N. Laing c , M.J. Denwood a , D. McBean b , N.D. Sargison d , K. Ellis a a Scottish Centre for Production Animal Health and Food Safety, School of Veterinary Medicine, College of Medical Veterinary and Life Sciences, University of Glasgow, Bearsden Road, Glasgow G61 1QH, United Kingdom b Moredun Research Institute, Pentlands Science Park, Bush Loan, Penicuik EH26 0PZ, United Kingdom c Clyde Veterinary Group, New Lanark Market, Lanark ML11 9SZ, United Kingdom d University of Edinburgh, Royal (Dick) School of Veterinary Studies, Easter Bush Veterinary Centre, Roslin, Midlothian EH25 9RG, United Kingdom
a r t i c l e
i n f o
Article history: Available online 5 December 2012 Keywords: Anthelmintic resistance Growth Lamb Nematode Sheep Targeted selective treatment
a b s t r a c t Sustainable control of nematode parasites in small ruminant production is a worldwide ambition. Development of anthelmintic resistance can severely impair small ruminant production. A practical approach to reduce selection pressure for anthelmintic resistance is to treat only a proportion of the flock (Targeted Selective Treatment), leaving a proportion of the nematode population untreated. The aim of this study was to compare the sustainability and efficacy of a performance-based marker, the Happy FactorTM , a monitor of nutrient utilisation efficiency, with a routine whole flock anthelmintic treatment. In a commercial flock in the South West of Scotland, 183 Texel cross lambs were split into two matched but co-grazing groups: one group managed as routinely for the farm (RT group) and the other subjected to targeted selective treatment (TST group). All lambs from the RT group were drenched every 6 weeks during the grazing season, while anthelmintic administration in the TST group was restricted to animals that failed to reach pre-determined weight gain targets, based on an estimate of their efficiency of gross energy utilisation. Animal performance and parasitological data were recorded every two weeks. In the 20 week period of the study, anthelmintic treatments were reduced by approximately 50% in the TST group compared to a routine anthelmintic administration that would have been applied, whilst epg counts were always <500 throughout the study in both groups. Finally, there was no discernible difference in the mean bodyweight gain between the two groups. Crown Copyright © 2012 Published by Elsevier B.V. All rights reserved.
1. Introduction Parasitic infections cause significant health problems and decreased productivity in livestock throughout the
夽 This paper is part of the special issue entitled “Lectures of the 1st European Conference on Small Ruminant Health Management”, held in Athens, Greece, October 2011. Guest Edited by G.C. Fthenakis. ∗ Corresponding author. E-mail address: [email protected] (V. Busin).
world. In the United Kingdom, the problems caused by them appear to increase in the future, as the trend for warmer, wetter winters facilitates more rapid nematode development on pasture (Kenyon et al., 2009a; Morgan and van Dijk, 2012). Nematodes of sheep are currently controlled by administration of anthelmintics (Sargison, 2011, 2012); however, suppressive control strategies can select strongly for the development of anthelmintic resistant in parasites (Taylor, 2012), which threatens sustainability of sheep farming worldwide (Papadopoulos et al., 2012; Torres-Acosta et al., 2012). A major determinant of the rate
0921-4488/$ – see front matter. Crown Copyright © 2012 Published by Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.smallrumres.2012.11.013
V. Busin et al. / Small Ruminant Research 110 (2013) 100–103
2. Materials and methods 2.1. Experimental design In total, 183 spring-born Texel-cross lambs were included in the study. At the age of approx. 6 weeks, all lambs were fitted with an electronically readable ear tag (Allflex, DFW airport, TX, USA) and treated with fenbendazole (Panacur; MSD Animal Health, Summit, NJ, USA) at the dose rate of 5 mg kg−1 bodyweight (bw), to clear spring Nematodirus spp. Lambs were assigned at random to two treatment groups, a routine treatment group (RT group) and a targeted selective treatment group (TST group), which were balanced for bodyweight, sex and numbers of single/twin/triplet lambs. Ten lambs from the RT group and 17 lambs from the TST group died during the first 2 months of life and have not been considered into the data management of the study. All lambs in the RT group were treated with ivermectin oral drench (Oramec; Merial Animal Health, Duluth, GE, USA) at the dose rate of 0.2 mg kg−1 bw, every 6 weeks (6th, 12th and 18th week of the study), following the routine health management in that farm. Treatments in the TST group were based on the identification of individual animals, which were likely to benefit from anthelmintic intervention using the decision
100 90
Number of lambs in the study
of development of anthelmintic resistance is the proportion of the parasite population exposed to anthelmintics (Martin et al., 1981). Treating only animals in need of therapy (targeted selective treatment) has been proposed to slow development of anthelmintic resistance, based on the recognised importance of the refugia concept (Van Wyk, 2001). Methods suggested to selectively target anthelmintic treatments range from visual inspection to parasite-based or pathophysiological markers; an ideal targeted selective treatment indicator would be cost-effective, simple to use, require minimal operator training and allow treatment decisions to be made ‘sheep-side’ (Kenyon et al., 2009b). A variety of indicators have been tested in recent years, with the FAMACHA chart for the control of Haemonchus contortus (Van Wyk and Bath, 2002) and milk yield in dairy goats (Hoste et al., 2002, 2012) internationally recognised as valid diagnostic markers. In the Scottish climate, the predominant parasite genera detected on farms are Teladorsagia circumcincta and Trichostrongylus spp. (Bartley et al., 2003), the major effects of which are reduction in voluntary food intake and reduced feed conversion efficiency (Coop et al., 1977). This is of particular significance, as sheep enterprises in Scotland are mainly based on meat production. In this context, bodyweight gain could be a sensitive marker, as a major factor affecting performance in parasitised animals is anorexia and its use is relevant to farm economics. Moreover, the reduction in bodyweight gain occurs early in infection, prior to the appearance of clinical signs (Coop et al., 1977). Recent experimental work has demonstrated promise for the targeted selective treatment approach, by using production efficiency as the individual animal treatment indicator (Greer et al., 2009). The present study aimed to apply targeted selective treatment, by using the Moredun-developed production efficiency based decision support system, Happy FactorTM (which is based on lamb growth rates) in a commercial setting. The intention was to study applicability of the use of bodyweight gain as a targeted selective treatment indicator, in comparison to the standard anthelmintic administration practice on a commercial farm, by quantifying the number of anthelmintic treatments and assessing lamb production.
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80 70 60 50 40 30 20 10 0 0
4
6
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18
20
Week of the study Fig. 1. Progressive decrease of numbers of lambs from the study, as they were withdrawn for sale when they reached the desired bodyweight (>40 kg); 8 animals in the routine anthelmintic treatment group (RT group, marked with ) and 5 lambs in the targeted selective anthelmintic treatment group (TST group, marked with ) were maintained throughout a 20 week study period. support model developed by Moredun researchers (Greer et al., 2009); minimum bodyweight gains that were required to achieve the suggested efficiency threshold of 0.66, were estimated for each animal within the TST regime prior to each fortnightly visit and any animal that had not reached that target received an anthelmintic treatment with ivermectin oral drench (Oramec; Merial Animal Health, Duluth, GE, USA) at the dose rate of 0.2 mg kg−1 bw. Field efficacy of anthelmintics on the farm had been confirmed prior to the study, by using the faecal egg count reduction test (Coles et al., 1992), in which no evidence of anthelmintic resistance had been detected, with efficacy for fenbendazole, levamisole and ivermectin reaching 97.0%, 99.7% and 99.8%, respectively. All lambs grazed on the same pasture until they reached the desired bodyweight (>40 kg), at which point, if sold, they were removed from the study. Eight animals in the RT group and five lambs in the TST group were maintained throughout the study, as they were to be maintained in the flock as replacement breeding animals (Fig. 1); proportion of lambs withdrawn did not differ significantly among the two groups (P > 0.21). Lamb bodyweight was measured at fortnightly intervals throughout the grazing season, for a total of 20 weeks. Faecal samples were collected directly from the rectum from all animals in the TST group, as well as from 10% of animals in the RT group, for faecal epg counting, as detailed by Christie and Jackson (1982). In addition, pasture mass (expressed in kg dry matter [DM] hectare−1 [ha−1 ]) was measured every two weeks, by using a Grassmaster II pasture probe (Tru-test Ltd., Auckland, New Zealand) that had been calibrated to local conditions (R2 = 0.80, n = 49). Pasture quality was visually estimated at the time of pasture mass measurements, whilst data for ambient temperature were collected from the United Kingdom’s Meteorological Office. The data were used to calculate the minimum bodyweight gain that might have been achieved by each animal at each sampling point, as described by Greer et al. (2009). 2.2. Statistical analysis The number of anthelmintic administrations per animal in the RT group was compared to the number of anthelmintic administrations per animal the TST group, using a paired Wilcoxon signed-rank test. Because of the difficulty in directly comparing RT and TST groups, due to progressive reduction in the number of lambs in each group, observed number of treatments in the TST group was also compared to the estimated number of administrations that would have been given in the same group under routine management conditions. The Wilcoxon signed-rank test was used to compare time to slaughter between RT and TST groups. An auto-regressive generalised linear model (GLAMM), with normal response distribution was used to describe the bodyweight gain data, with fixed effects of sex and RT versus TST group. The model was fitted to the data using Bayesian MCMC.
V. Busin et al. / Small Ruminant Research 110 (2013) 100–103
Table 1 Number of lambs and frequency of anthelmintic administration in a routine treatment group (RT group) and a targeted selective treatment group (TST group) in a sheep flock throughout a 20 week study period. Frequency of treatment
Number of lambs RT group n
TST group
%
n
%
No treatment Once Twice Thrice
6 46 32 11
6 48 34 12
33 43 9 3
38 49 10 3
Total lambs
95
100
88
100
Total number of anthelmintic administrations
143
70
Cumulative bodyweight gain of lambs (kg)
102
35 30 25 20 15 10 5 0 0
4
6
8
10
12
13
16
18
20
Week of the study Fig. 3. Cumulative weight gain (kg) in lambs in a routine anthelmintic treatment group (RT group, marked with ) or in a targeted selective anthelmintic treatment group (TST group, marked with ) throughout a 20 week study period.
4. Discussion 3. Results In total, 143 anthelmintic administrations were carried out in lambs of RT group and 70 anthelmintic administrations were carried out in lambs of TST group (P < 0.001). The estimated number of anthelmintic administrations that would have been carried out in lambs of TST group under the same routine programme, as in lambs of RT group, was 139 (P < 0.001) (Table 1). Faecal nematode egg counts in the two groups are shown in Fig. 2. Their pattern was similar in the two groups, with higher mean epg counts recorded in TST group lambs (110 epg versus 57 epg in RT group lambs). Cumulative bodyweight gain was similar in the two groups throughout the study (Fig. 3). Mean bodyweight gain (±standard error of the mean) for all lambs into each group, across all sampling points was 263 (±6.2) and 257 (±7.1) g day−1 for RT group and TST group lambs, respectively. By using the statistical model of daily bodyweight gain, we found a 0.609 probability that growth rate was lower in lambs of the TST group than in those of the RT group and a 0.391 probability of the converse; moreover, the probability that female lambs had a lower growth rate than male lambs was 0.988.
Lamb faecal egg counts
200 180 160 140 120 100 80 60 40 20 0 4
6
8
10
12
14
16
18
20
Week of the study Fig. 2. Mean faecal nematode epg counts in lambs in a routine anthelmintic treatment group (RT group, marked with ) or in a targeted selective anthelmintic treatment group (TST group, marked with ) throughout a 20 week study period; arrows on the graph indicate times of anthelmintic treatment carried out in the RT group.
The concept of leaving a proportion of animals untreated, with the aim to maintain parasite populations in refugia is now widely accepted as the best means of preserving anthelmintic susceptibility within the parasite population (Van Wyk, 2001; Besier, 2008; Jackson and Waller, 2008; Jackson et al., 2009). However, the key matter, which has so far delayed the application of this concept, is absence of a convenient and accurate method to identify animals suffering from levels of infection causing detectable production losses or adverse health effects (Malan et al., 2001). Previous studies have shown that the main impact of parasites, such as T. circumcincta or Trichostrongylus spp., is reflected in reduced bodyweight gain (Sykes and Coop, 1976, 1977). Animal performance is the factor of main interest to farmers, especially in mutton-type production systems. Because of that and as daily bodyweight gain can be easily and objectively measured in field situations, the Happy FactorTM decision support system (Greer et al., 2009) has been developed, to estimate target weight gain for individual animals. Animals that fail to reach the calculated target weight receive an anthelmintic treatment, leaving those who have achieved the expected performance untreated. Although this approach may appear effective, it has not been tested extensively in clinical situations. The objective of the present study was, therefore, to study the applicability of this approach, using short-interval weight changes, as a reliable indicator of subclinical parasitism in a commercial farm. Such an approach was considered to be feasible if it would sustain two main targets: (a) significant reduction in the number of anthelmintic administrations and (b) absence of adverse effects on animal performance. Use of targeted selective treatments resulted in a reduction by about 50% in number of anthelmintic administrations. Moreover, number of animals that did not receive any anthelmintic treatment was higher in the TST group (33% of animals in the group versus 6% of animals in the RT group). Despite the reduced number of anthelmintic administrations, mean epg counts during the study never exceeded 500 epg, considered to be a clinically important threshold (Love and Hutchinson, 2003). According to mathematical models by Barnes et al. (1995), at least 20% of animals should be left untreated throughout the
V. Busin et al. / Small Ruminant Research 110 (2013) 100–103
grazing season, in order potentially reduce development of anthelmintic resistance. Hence, the current approach may be usefully applied. Targeted anthelmintic administrations did not have any adverse effects on lamb growth. Both groups performed similarly, with comparable weight gains during the study period and with no difference in time to reach slaughter weight. Demonstration of the feasibility of targeted anthelmintic administrations in a flock is a first step in developing and implementing anthelmintic programmes, as part of flock health management. However, it is noteworthy that farmers still have varying opinions regarding the practicality and usefulness of the approach, which may not always coincide with those of the scientific community (Berrag et al., 2009; Cabaret et al., 2009). 5. Concluding comments It is concluded that use of production efficiency as an indicator for targeted selective anthelmintic administrations is suitable for commercial farm settings. The approach presents a valid tool to slow down development of anthelmintic resistance, by reducing the number of anthelmintic treatments required to maintain animal performance. Conflict of interest statement The authors declare that no financial or personal relationship with other people or organisations could have inappropriately influenced our work. Acknowledgement The authors gratefully acknowledge the help and cooperation of staff at Moredun Research Institute and Merial Animal Health for material supply. References Barnes, E.H., Dobson, R.J., Barger, I.A., 1995. Worm control and anthelmintic resistance: adventures with a model. Parasitol. Today 11, 56–63. Bartley, D.J., Jackson, E., Johnston, K., Coop, R.L., Mitchell, G.B.B., Sales, J., Jackson, F., 2003. A survey of anthelmintic resistant nematode parasites in Scottish sheep flocks. Vet. Parasitol. 117, 61–71. Berrag, B., Ouzir, M., Cabaret, J., 2009. A survey on meat sheep farms in two regions of Morocco on farm structure and the acceptability of the targeted selective treatment approach to worm control. Vet. Parasitol. 164, 30–35. Besier, B., 2008. Targeted treatment strategies for sustainable worm control in sheep. Trop. Biomed. 25, 9–17. Cabaret, J., Benoit, M., Laignel, G., Nicourt, C., 2009. Current management of farms and internal parasites by conventional and organic meat sheep French farmers and acceptance of targeted selective treatments. Vet. Parasitol. 164, 21–29.
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