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Duration of activity of topical eprinomectin against experimental infections with Teladorsagia circumcincta and Trichostrongylus colubriformis in goats
Veterinary Parasitology 125 (2004) 415–419 www.elsevier.com/locate/vetpar
Short communication
Duration of activity of topical eprinomectin against experimental infections with Teladorsagia circumcincta and Trichostrongylus colubriformis in goats Christophe Chartier*, Isabelle Pors AFSSA Site de Niort, Laboratoire d’Etudes et de Recherches Caprines, 60 Rue de Pied de Fond, B.P. 3081, 79012 Niort Cedex, France Received 30 March 2004; received in revised form 13 July 2004; accepted 25 July 2004
Abstract The immediate as well as the persistent anthelmintic efficacies of topically applied eprinomectin were evaluated in goats against induced infections with Teladorsagia circumcincta (2800 L3) and Trichostrongylus colubriformis (6000 L3). Twenty-three culled dairy goats were allocated to the following groups: control animals (group 1), animals treated 21 days prior to nematode infection (group 2), animals treated 7 days prior to nematode infection (group 3) and animals treated 21 days after nematode infection (group 4). Eprinomectin was applied at twice the cattle dose rate (1.0 mg/kg BW). According to the groups, necropsies were undertaken 28 days after nematode infection (groups 1–3) or 14 days after the anthelmintic treatment (group 4). Worm counts were determined for abomasum and small intestine. The curative anthelmintic efficacy of eprinomectin at 1.0 mg/kg BW on existing worm burdens was 100% against T. circumcincta and T. colubriformis. Quite similar worm burdens reductions were observed when eprinomectin was administered 7 days before infection whereas they were only 52.4 and 17.8% for T. circumcincta and T. colubriformis, respectively, for an administration of the drug 21 days prior to the nematode infection. # 2004 Elsevier B.V. All rights reserved. Keywords: Teladorsagia circumcincta; Trichostrongylus colubriformis; Nematodes; Goat; Topical eprinomectin; Anthelmintic
* Corresponding author. Tel.: +33 5 49 79 61 28; fax: +33 5 49 79 42 19. E-mail address: [email protected] (C. Chartier). 0304-4017/$ – see front matter # 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.vetpar.2004.07.022
416
C. Chartier, I. Pors / Veterinary Parasitology 125 (2004) 415–419
1. Introduction Eprinomectin is a potent anthelmintic belonging to the family of macrocyclic lactones. Excellent nematocidal activity has been described in cattle by previous workers against natural or induced infections: >99–100% efficacy was recorded against adult strongyles of Ostertagia spp., Haemonchus spp., Nematodirus spp., Oesophagostomum spp. and inhibited larval strongyles of Ostertagia spp., when given topically at 0.5 mg/kg body weight (Gogolewski et al., 1997; Pitt et al., 1997; Shoop et al., 1996; Williams et al., 1997; Yazwinski et al., 1997). Because of its partitioning profile between serum and milk (Alvinerie et al., 1999b), it is the only endectocide approved for dairy cattle with a zero milk-withdrawal period. There are few anthelmintics that can be used during the lactating period with a zero milk-withdrawal period in dairy goats in France and all of them belong to the family of benzimidazoles (fenbendazole, oxfenbendazole, febantel). Moreover, benzimidazole resistant nematodes have become very prevalent in goats in France (Cabaret et al., 1995; Chartier et al., 1998; 2001) and in several geographic areas, the use of this last anthelmintic family is no longer relevant. Preliminary results indicated that pour-on eprinomectin was effective against experimental nematode infections in goats (Chartier et al., 1999). Nevertheless, the less than complete efficacy against the small intestinal nematode, Trichostrongylus colubriformis, suggested that the standard cattle dose rate of 0.5 mg/kg BW would be a suboptimal dosage. In this study we present the results of a controlled trial in goats which evaluated the immediate as well as the persistent efficacy of eprinomectin given topically at the dose rate of 1.0 mg/kg BW against induced infections with Teladorsagia circumcincta and T. colubriformis.
2. Materials and methods Twenty-three 2–5-year-old culled female French Alpine goats weighing 36–67 kg were used. Animals, previously raised in a zero-grazing system, were not pregnant, nonlactating and free of trichostrongyle infections at the beginning of the experiment. Goats were housed in concrete pens and were fed barley hay with commercial concentrates. In order to evaluate both the persistent and immediate anthelmintic efficacy of eprinomectin, animals were weighed and allocated as follows: group 1 (n = 6) infected with nematodes and left as untreated (control) group, group 2 (n = 5) treated 21 days prior to nematode infection, group 3 (n = 6) treated 7 days prior to nematode infection, group 4 (n = 6) treated 21 days after nematode infection. Experimental infection consisted of T. circumcincta and T. colubriformis of INRA (Institut National de la Recherche Agronomique, Nouzilly, France) strains of sheep origin. On the same day, each goat was inoculated orally with 2800 T. circumcincta and 6000 T. colubriformis infective larvae (L3). Eprinomectin (0.5%, w/v) was applied topically with a syringe from the base of the tail to the neck at a dose rate of 1.0 mg/kg BW (2 ml/10 kg BW). For groups 1–3, necropsies were undertaken 28 days after nematode infection. For group 4, goats were slaughtered 14 days after the anthelmintic treatment. Each abomasum and small intestine was removed for worm recovery. Nematode
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counts were performed on 1:10 aliquots. The efficacy of the treatment was determined using the formula: [(C T)/C] 100, where C is the arithmetic mean count for untreated control and T the arithmetic mean count for goat treated with eprinomectin. Worm burden comparisons between groups were made by a Mann–Whitney test (Systat 9 for Windows1, SPSS, 1998).
3. Results No general or local adverse reactions were noted following the topical treatment. The number of each parasite found in individual goats together with arithmetic group means, percentage reductions and statistical significances according to the different groups are shown in Table 1. The curative anthelmintic efficacy of eprinomectin at 1.0 mg/kg BW on existing worm burdens was 100% against T. circumcincta and T. colubriformis as well. Similar worm burdens reductions were observed when eprinomectin was administered 7 days before infection whereas they were only 52.4 and 17.8% for T. circumcincta and T. colubriformis, respectively, for an administration of the drug 21 days prior to the nematode infection. These two last differences were not statistically significant.
4. Discussion This study clearly indicated a very high efficacy of eprinomectin against T. circumcincta and T. colubriformis in goats when given topically at 1.0 mg/kg BW. Our previous results have shown that the cattle standard dose rate of 0.5 mg/kg BW when applied to goats gave a less than complete efficacy against the dose-limiting species, T. colubriformis (Chartier et al., 1999). Similarly, Gawor et al. (2000) recorded faecal egg count reductions ranging from 59.5 to 89.9% after eprinomectin treatment at 0.5 mg/kg BW of naturally infected goats. By increasing the dose rate to 1.0 mg/kg, the same authors observed faecal egg count reductions between 88.5 and 97.6%. Such deficits in anthelmintic activity in goats compared to other ruminants when given at the standard dose rate have been suggested with other macrocyclic lactones as ivermectin or moxidectin particularly with T. colubriformis (McKenna, 1991; Pearson and Rutherford, 1988; Torres-Acosta and Jacobs, 1999). Previous pharmacokinetic investigations also revealed some specificity in goats. When compared with dairy cattle, the systemic availability of eprinomectin to goats was considerably lower with a bioavailability (AUC) of 72 ng day/ml compared to 239 ng day/ ml at the similar standard dose rate of 0.5 mg/kg (Alvinerie et al., 1999a, 1999b). At 1.0 mg/kg in goats, the systemic availability was two times higher than for 0.5 mg/kg and the maximum level of residue in milk remained below the maximum acceptable level of 30 ng ml 1 permitted in lactating cattle (Dupuy et al., 2001). Another relevant question pointed out by Lespine et al. (2003) concerns the possible mode of administration of eprinomectin as these authors have demonstrated that a subcutaneous administration was 2.5 times more effective than a pour-on administration in terms of bioavailability. Anthelmintic efficacy studies remain to be done to confirm such differences between subcutaneous and topical routes.
418
C. Chartier, I. Pors / Veterinary Parasitology 125 (2004) 415–419
Table 1 Postmortem worm counts, group means and percentage reductions with eprinomectin applied topically (1.0 mg/ kg) compared with control goats Group
Tag number
Untreated control
9289 7093 5058 7222 8391 5091
Group mean Eprinomectin 1.0 mg/kg (21 days before infection)
8310 7035 5078 6071 8180
Group mean Reduction (%) Eprinomectin 1.0 mg/kg (7 days before infection)
9049 7053 9207 9313 5130 9022
Group mean Reduction (%)
4145 7190 9017 8054 5186 1104
T. colubriformis
700 990 530 100 440 570
2490 2622 2240 2320 4150 4340
555a
3027a
360 30 10 210 710
2490 110 2760 2790 4280
264a 52.4
2486a 17.8
0 0 0 0 0 0
10 0 0 0 0 10
0b 100
Group mean Reduction (%) Eprinomectin 1.0 mg/kg (21 days after infection)
T. circumcincta
3.3b 99.8
0 0 0 0 0 0
0 0 0 0 0 0
0b 100
0b 100
Means in the same column with different superscripts (a, b) are significantly different (P < 0.05).
Eprinomectin treatment at 1.0 mg/kg totally prevented T. circumcincta and T. colubriformis infection for 7 days whereas the effect was only partial and restricted to T. circumcincta for 21 days. Similarly, Torres-Acosta and Jacobs (1999) recorded a 96– 100% prevention of Haemonchus contortus and T. circumcincta infection for 15 days with oral moxidectin in goats whereas no efficacy was seen for T. colubriformis. These results clearly illustrate the relatively poor efficacy of endectocide anthelmintics against the intestinal nematodes as it has been well documented with Cooperia oncophora in cattle (Taylor et al., 2001). Efficacy data, pharmacokinetic considerations as well as milk residue studies indicate that topically eprinomectin has to be used at the dose rate of 1.0 mg/kg in goats.
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Acknowledgements We thank Jacques Cabaret (Station de Pathologie Aviaire et de Parasitologie, INRA, Nouzilly, France) for providing the larvae. The study was funded by the Conseil Re´ gional Poitou-Charentes, France. References Alvinerie, M., Lacoste, E., Sutra, J.F., Chartier, C., 1999a. Some pharmacokinetic parameters of eprinomectin in goats following pour-on administration. Vet. Res. Commun. 23, 449–455. Alvinerie, M., Sutra, J.F., Galtier, P., Mage, C., 1999b. Pharmacokinetics of eprinomectin in plasma and milk following topical administration to lactating dairy cattle. Res. Vet. Sci. 67, 229–232. Cabaret, J., Baudet, H.M., Devos, J., Hubert, J., Cortet, J., Sauve´ , C., 1995. Studies on multispecific resistance of gastro-intestinal nematodes to benzimidazoles on dairy-goat farms. Vet. Parasitol. 60, 331–337. Chartier, C., Etter, E., Pors, I., Alvinerie, M., 1999. Activity of eprinomectin in goats against experimental infections with Haemonchus contortus, Teladorsagia circumcincta and Trichostrongylus colubriformis. Vet. Rec. 144, 99–100. Chartier, C., Pors, I., Hubert, J., Rocheteau, D., Benoit, C., Bernard, N., 1998. Prevalence of anthelmintic resistant nematodes in sheep and goats in Western France. Small Rumin. Res. 29, 33–41. Chartier, C., Soubirac, F., Pors, I., Silvestre, A., Hubert, J., Couquet, C., Cabaret, J., 2001. Prevalence of anthelmintic resistance in gastrointestinal nematodes of dairy goats under extensive management conditions in southwestern France. J. Helminthol. 75, 325–330. Dupuy, J., Chartier, C., Sutra, J.F., Alvinerie, M., 2001. Eprinomectin in dairy goats: dose influence on plasma levels and excretion in milk. Parasitol. Res. 87, 294–298. Gawor, J., Borecka, A., Malczewski, A., 2000. Use of eprinomectin (Eprinex pour-on) to control natural infection by gastro-intestinal nematodes in goats. Medycyna Wet. 56, 398–400 (in Polish). Gogolewski, R.P., Slacek, B., Familton, A.S., Paterson, B., Langholff, W.K., Allerton, G.R., McAnulty, R., Eagleson, J.S., 1997. Efficacy of a topical formulation of eprinomectin against endoparasites of cattle in New Zealand. NZ Vet. J. 45, 1–3. Lespine, A., Sutra, J.F., Dupuy, J., Alvinerie, M., 2003. Eprinomectin in goat: assessment of subcutaneous administration. Parasitol. Res. 89, 120–122. McKenna, P.B., 1991. Update on anthelmintics in goats. Publication Veterinary Continuing Education, Massey University, pp. 93–96. Pearson, A.B., Rutherford, D.M., 1988. Ivermectin injection less effective in goats than oral treatments. Surveillance 15, 22. Pitt, S.R., Langholff, W.K., Eagleson, J.S., Rehbein, S., 1997. The efficacy of eprinomectin against induced infections of immature (fourth larval stage) and adult nematode parasites in cattle. Vet. Parasitol. 73, 119–128. Shoop, W.L., Egerton, J.R., Eary, C.H., Haines, H.W., Michael, B.F., Mrozik, H., Eskola, P., Fisher, M.H., Slayton, L., Ostlind, D.A., Skelly, B.J., Fulton, R.K., Barth, D., Costa, S., Gregory, L.W., Campbell, W.C., Selward, R.L., Turner, M.J., 1996. Eprinomectin: a novel avermectin for use as a topical endectocide for cattle. Int. J. Parasitol. 26, 1237–1242. Taylor, S.M., Le Stang, J.P., Kenny, J., 2001. Persistent efficacy of doramectin and moxidectin against Cooperia oncophora infections in cattle. Vet. Parasitol. 96, 323–328. Torres-Acosta, J.F., Jacobs, D.E., 1999. Duration of activity of oral moxidectin against Haemonchus contortus, Teladorsagia circumcincta and Trichostrongylus colubriformis in goats. Vet. Rec. 144, 648–649. Williams, J.C., Stuedemann, J.A., Bairden, K., Kerboeuf, D., Ciorda, H., Hubert, J., Broussard, S.D., Plue, R.E., Alvavaldes, R., Baggott, D.G., Pinkall, N., Eagleson, J.S., 1997. Efficacy of a pour-on formulation of eprinomectin (MK-397) against nematode parasites of cattle, with emphasis on inhibited early fourth-stage larvae of Ostertagia spp. Am. J. Vet. Res. 58, 379–383. Yazwinski, T.A., Johnson, E.G., Thompson, D.R., Drag, M.D., Zimmerman, G.L., Langholff, W.K., Holste, J.E., Eagleson, J.S., 1997. Nematocidal efficacy of eprinomectin, delivered topically, in naturally infected cattle. Am. J. Vet. Res. 58, 612–614.
Short communication
Duration of activity of topical eprinomectin against experimental infections with Teladorsagia circumcincta and Trichostrongylus colubriformis in goats Christophe Chartier*, Isabelle Pors AFSSA Site de Niort, Laboratoire d’Etudes et de Recherches Caprines, 60 Rue de Pied de Fond, B.P. 3081, 79012 Niort Cedex, France Received 30 March 2004; received in revised form 13 July 2004; accepted 25 July 2004
Abstract The immediate as well as the persistent anthelmintic efficacies of topically applied eprinomectin were evaluated in goats against induced infections with Teladorsagia circumcincta (2800 L3) and Trichostrongylus colubriformis (6000 L3). Twenty-three culled dairy goats were allocated to the following groups: control animals (group 1), animals treated 21 days prior to nematode infection (group 2), animals treated 7 days prior to nematode infection (group 3) and animals treated 21 days after nematode infection (group 4). Eprinomectin was applied at twice the cattle dose rate (1.0 mg/kg BW). According to the groups, necropsies were undertaken 28 days after nematode infection (groups 1–3) or 14 days after the anthelmintic treatment (group 4). Worm counts were determined for abomasum and small intestine. The curative anthelmintic efficacy of eprinomectin at 1.0 mg/kg BW on existing worm burdens was 100% against T. circumcincta and T. colubriformis. Quite similar worm burdens reductions were observed when eprinomectin was administered 7 days before infection whereas they were only 52.4 and 17.8% for T. circumcincta and T. colubriformis, respectively, for an administration of the drug 21 days prior to the nematode infection. # 2004 Elsevier B.V. All rights reserved. Keywords: Teladorsagia circumcincta; Trichostrongylus colubriformis; Nematodes; Goat; Topical eprinomectin; Anthelmintic
* Corresponding author. Tel.: +33 5 49 79 61 28; fax: +33 5 49 79 42 19. E-mail address: [email protected] (C. Chartier). 0304-4017/$ – see front matter # 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.vetpar.2004.07.022
416
C. Chartier, I. Pors / Veterinary Parasitology 125 (2004) 415–419
1. Introduction Eprinomectin is a potent anthelmintic belonging to the family of macrocyclic lactones. Excellent nematocidal activity has been described in cattle by previous workers against natural or induced infections: >99–100% efficacy was recorded against adult strongyles of Ostertagia spp., Haemonchus spp., Nematodirus spp., Oesophagostomum spp. and inhibited larval strongyles of Ostertagia spp., when given topically at 0.5 mg/kg body weight (Gogolewski et al., 1997; Pitt et al., 1997; Shoop et al., 1996; Williams et al., 1997; Yazwinski et al., 1997). Because of its partitioning profile between serum and milk (Alvinerie et al., 1999b), it is the only endectocide approved for dairy cattle with a zero milk-withdrawal period. There are few anthelmintics that can be used during the lactating period with a zero milk-withdrawal period in dairy goats in France and all of them belong to the family of benzimidazoles (fenbendazole, oxfenbendazole, febantel). Moreover, benzimidazole resistant nematodes have become very prevalent in goats in France (Cabaret et al., 1995; Chartier et al., 1998; 2001) and in several geographic areas, the use of this last anthelmintic family is no longer relevant. Preliminary results indicated that pour-on eprinomectin was effective against experimental nematode infections in goats (Chartier et al., 1999). Nevertheless, the less than complete efficacy against the small intestinal nematode, Trichostrongylus colubriformis, suggested that the standard cattle dose rate of 0.5 mg/kg BW would be a suboptimal dosage. In this study we present the results of a controlled trial in goats which evaluated the immediate as well as the persistent efficacy of eprinomectin given topically at the dose rate of 1.0 mg/kg BW against induced infections with Teladorsagia circumcincta and T. colubriformis.
2. Materials and methods Twenty-three 2–5-year-old culled female French Alpine goats weighing 36–67 kg were used. Animals, previously raised in a zero-grazing system, were not pregnant, nonlactating and free of trichostrongyle infections at the beginning of the experiment. Goats were housed in concrete pens and were fed barley hay with commercial concentrates. In order to evaluate both the persistent and immediate anthelmintic efficacy of eprinomectin, animals were weighed and allocated as follows: group 1 (n = 6) infected with nematodes and left as untreated (control) group, group 2 (n = 5) treated 21 days prior to nematode infection, group 3 (n = 6) treated 7 days prior to nematode infection, group 4 (n = 6) treated 21 days after nematode infection. Experimental infection consisted of T. circumcincta and T. colubriformis of INRA (Institut National de la Recherche Agronomique, Nouzilly, France) strains of sheep origin. On the same day, each goat was inoculated orally with 2800 T. circumcincta and 6000 T. colubriformis infective larvae (L3). Eprinomectin (0.5%, w/v) was applied topically with a syringe from the base of the tail to the neck at a dose rate of 1.0 mg/kg BW (2 ml/10 kg BW). For groups 1–3, necropsies were undertaken 28 days after nematode infection. For group 4, goats were slaughtered 14 days after the anthelmintic treatment. Each abomasum and small intestine was removed for worm recovery. Nematode
C. Chartier, I. Pors / Veterinary Parasitology 125 (2004) 415–419
417
counts were performed on 1:10 aliquots. The efficacy of the treatment was determined using the formula: [(C T)/C] 100, where C is the arithmetic mean count for untreated control and T the arithmetic mean count for goat treated with eprinomectin. Worm burden comparisons between groups were made by a Mann–Whitney test (Systat 9 for Windows1, SPSS, 1998).
3. Results No general or local adverse reactions were noted following the topical treatment. The number of each parasite found in individual goats together with arithmetic group means, percentage reductions and statistical significances according to the different groups are shown in Table 1. The curative anthelmintic efficacy of eprinomectin at 1.0 mg/kg BW on existing worm burdens was 100% against T. circumcincta and T. colubriformis as well. Similar worm burdens reductions were observed when eprinomectin was administered 7 days before infection whereas they were only 52.4 and 17.8% for T. circumcincta and T. colubriformis, respectively, for an administration of the drug 21 days prior to the nematode infection. These two last differences were not statistically significant.
4. Discussion This study clearly indicated a very high efficacy of eprinomectin against T. circumcincta and T. colubriformis in goats when given topically at 1.0 mg/kg BW. Our previous results have shown that the cattle standard dose rate of 0.5 mg/kg BW when applied to goats gave a less than complete efficacy against the dose-limiting species, T. colubriformis (Chartier et al., 1999). Similarly, Gawor et al. (2000) recorded faecal egg count reductions ranging from 59.5 to 89.9% after eprinomectin treatment at 0.5 mg/kg BW of naturally infected goats. By increasing the dose rate to 1.0 mg/kg, the same authors observed faecal egg count reductions between 88.5 and 97.6%. Such deficits in anthelmintic activity in goats compared to other ruminants when given at the standard dose rate have been suggested with other macrocyclic lactones as ivermectin or moxidectin particularly with T. colubriformis (McKenna, 1991; Pearson and Rutherford, 1988; Torres-Acosta and Jacobs, 1999). Previous pharmacokinetic investigations also revealed some specificity in goats. When compared with dairy cattle, the systemic availability of eprinomectin to goats was considerably lower with a bioavailability (AUC) of 72 ng day/ml compared to 239 ng day/ ml at the similar standard dose rate of 0.5 mg/kg (Alvinerie et al., 1999a, 1999b). At 1.0 mg/kg in goats, the systemic availability was two times higher than for 0.5 mg/kg and the maximum level of residue in milk remained below the maximum acceptable level of 30 ng ml 1 permitted in lactating cattle (Dupuy et al., 2001). Another relevant question pointed out by Lespine et al. (2003) concerns the possible mode of administration of eprinomectin as these authors have demonstrated that a subcutaneous administration was 2.5 times more effective than a pour-on administration in terms of bioavailability. Anthelmintic efficacy studies remain to be done to confirm such differences between subcutaneous and topical routes.
418
C. Chartier, I. Pors / Veterinary Parasitology 125 (2004) 415–419
Table 1 Postmortem worm counts, group means and percentage reductions with eprinomectin applied topically (1.0 mg/ kg) compared with control goats Group
Tag number
Untreated control
9289 7093 5058 7222 8391 5091
Group mean Eprinomectin 1.0 mg/kg (21 days before infection)
8310 7035 5078 6071 8180
Group mean Reduction (%) Eprinomectin 1.0 mg/kg (7 days before infection)
9049 7053 9207 9313 5130 9022
Group mean Reduction (%)
4145 7190 9017 8054 5186 1104
T. colubriformis
700 990 530 100 440 570
2490 2622 2240 2320 4150 4340
555a
3027a
360 30 10 210 710
2490 110 2760 2790 4280
264a 52.4
2486a 17.8
0 0 0 0 0 0
10 0 0 0 0 10
0b 100
Group mean Reduction (%) Eprinomectin 1.0 mg/kg (21 days after infection)
T. circumcincta
3.3b 99.8
0 0 0 0 0 0
0 0 0 0 0 0
0b 100
0b 100
Means in the same column with different superscripts (a, b) are significantly different (P < 0.05).
Eprinomectin treatment at 1.0 mg/kg totally prevented T. circumcincta and T. colubriformis infection for 7 days whereas the effect was only partial and restricted to T. circumcincta for 21 days. Similarly, Torres-Acosta and Jacobs (1999) recorded a 96– 100% prevention of Haemonchus contortus and T. circumcincta infection for 15 days with oral moxidectin in goats whereas no efficacy was seen for T. colubriformis. These results clearly illustrate the relatively poor efficacy of endectocide anthelmintics against the intestinal nematodes as it has been well documented with Cooperia oncophora in cattle (Taylor et al., 2001). Efficacy data, pharmacokinetic considerations as well as milk residue studies indicate that topically eprinomectin has to be used at the dose rate of 1.0 mg/kg in goats.
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