- Email: [email protected]
Observations of benzimidazole efficacies against Ascaridia dissimilis, Ascaridia galli, and Heterakis gallinarum in naturally infected poultry
©2013 Poultry Science Association, Inc.
Observations of benzimidazole efficacies against Ascaridia dissimilis, Ascaridia galli, and Heterakis gallinarum in naturally infected poultry T. A. Yazwinski,*1 C. A. Tucker,* E. Wray,* L. Jones,* and F. D. Clark† *Department of Animal Science, and †Department of Poultry Science, University of Arkansas, Fayetteville 72701 Primary Audience: Poultry Flock Managers, Veterinarians, Nutritionists SUMMARY Two studies were conducted to provide current efficacy evaluation for benzimidazoles used in poultry. In the first study, naturally infected laying hens from an organic, free-range facility were treated with fenbendazole as an oral drench at the rate of 5.0 mg·kg−1 of BW. Based on treatment group, geometric means for all stages combined, fenbendazole was 85.5 and 89.5% effective for the removal of Ascaridia galli and Heterakis gallinarum populations, respectively. In the second study, naturally infected turkeys from a commercial grower were treated with albendazole as an oral suspension at the rate of 10 mg·kg −1 of BW, treated with fenbendazole as an oral suspension at the rate of 5 mg·kg −1 of BW, treated with fenbendazole for 6 d with feed medicated at the concentration of 16 ppm, or left as control. Based on treatment group geometric means for all stages combined, efficacies for A. dissimilis were 0, 71.4, and 83.3% for albendazole drench, fenbendazole drench, and fenbendazole-medicated feed, respectively. Key words: chicken, turkey, nematode infection, efficacy, fenbendazole, albendazole 2013 J. Appl. Poult. Res. 22:75–79 http://dx.doi.org/10.3382/japr.2012-00606
DESCRIPTION OF THE PROBLEM Helminth infections of poultry are both varied and common [1]. Treatment of these infections is also extremely varied, dependent upon production type, stage of production, type of bird, and producer preferences. Periodic evaluation of anthelmintics used in poultry is desirable so that producers can formulate effective strategies for helminth control and thereby improve feed efficiencies, production performance, and overall bird health. Additionally, anthelmintic efficacies must be constantly monitored so that the transition of product efficacies from 1
Corresponding author: [email protected]
effective (≥90% efficacy) to less than effective (<90% efficacy) can be determined and treatment/husbandry strategies be implemented which might provide remedy. Helminth parasitisms of domestic animals are most commonly dealt with via chemical intervention, a practice which invariably results in resistance by the targeted parasites; a situation that is the norm in horse, cattle, and small ruminant production [2]. With these other animal industries, the emphasis has been on monitoring the extent of anthelmintic resistance, and formulation of strategies that might deal with the developing problem (searching for new compounds, studies on the feasibil-
JAPR: Research Report
76 ity of combination therapy, revisiting husbandry means of control, nutraceutical usage, and so on). The same approach would seem to be advisable for the poultry industry. Recently, depressed levels of effectiveness were detected for benzimidazoles used in the treatment of turkeys harboring artificial infections with Ascaridia dissimilis [3]. Given these findings, the current research was undertaken as a means to validate the former findings with natural infections. Additionally, given the growing popularity of organic and natural production of poultry and poultry products, determining the effectiveness of anthelmintics used in the salvage treatment of birds originating from these industries was indicated.
MATERIALS AND METHODS First Study (Chickens) Approximately 40 chickens (Bovan Brown) from an organic, free-range egg production operation in Arkansas were obtained at the time of scheduled depopulation (bird age of 77 to 79 wk). Upon delivery to the research facility, the birds were evenly divided via a random process into 2 adjacent pens. After a 7 d acclimation period, unhealthy birds were culled and the remaining birds were weighed, sorted via a random process into treatment groups within each pen, and treated accordingly. Control birds (10 per pen) were left unmedicated. Treated birds (7 per pen) were orally administered fenbendazole [4] in suspension at the rate of 5 mg·kg −1 of BW, with the total dose given in halves at 0900 and 1600 h. Seven days posttreatment, all birds were killed for parasite collection and enumeration. Second Study (Turkeys) Approximately fifty 8-wk-old turkeys were obtained from a commercial turkey operation in Arkansas immediately before their initial, scheduled anthelmintic treatment. Upon delivery to the research facility, they were evenly divided via random process into 4 adjacent pens. After an 11-d acclimation period, unhealthy birds were culled and the remaining birds were given an experimental treatment (one treatment group per pen). Control birds were left unmedi-
cated. Birds treated with albendazole [5] were given the product on d 3 at the dose rate of 10 mg·kg −1 of BW, as an oral suspension, with the total dose given in halves at 0900 and 1600 h. Birds treated with fenbendazole as an oral suspension [4] were treated on d 3 at the dose rate of 5 mg·kg −1 of BW, with the total dose given in halves at 0900 and 1600 h. Birds treated with fenbendazole in the feed [6] were supplied ration medicated with fenbendazole at a concentration of 16 ppm. Medicated ration was supplied ad libitum for 6 continuous days (d 0 to 6), after which time the ration was replaced with the standard, unmedicated feed. All study birds were killed on d 9. Parasitology Feed was withheld from all birds for 12 h before they were killed. At necropsy, the intestine from gizzard to vent (with ceca for chickens only) was removed from each bird, stripped of mesentery, and opened lengthwise. The opened tract (with contents and washings) was then placed into one container and refrigerated overnight. The following morning, the tract was withdrawn from the container through a clenched fist to express all contents and mucosal slurry. All collected materials in the container were then washed over a 75-μm-aperture sieve, and the residue was collected and preserved with formalin until inspection at 10× to 70× magnification for nematode identifications and counts. This procedure is compliant with current guidelines for poultry anthelmintic studies [7], and parasite descriptions used in this study for nematode identifications can be found elsewhere [1]. Statistics A mixed-model analysis was performed on the data using the MIXED procedure of SAS [8]. Each individual bird was an experimental unit with fixed effects sourced by treatment group (the only source of variance). Prior to ANOVA, species-specific parasite counts were transformed to the log10 of (x + 1). For all counts, all developmental stages for a particular species were combined, because only a small number of larval stages was detected for the birds. Treatment effect was determined to be significant (P
Yazwinski et al.: BENZIMIDAZOLE EFFICACY ≤ 0.05) with an F-test (2 treatment groups) or a significant F-test followed by repeated t-tests (3 treatment groups). Bird Welfare Both studies were conducted after review of the protocols by the University of Arkansas Animal Use and Welfare Committee. All birds were monitored at a minimum of twice daily for health and well-being. Lighting was constant for both studies, water availability was ad libitum throughout, and feed deprivation was likewise ad libitum until overnight withdrawal before birds were killed by cervical dislocation.
RESULTS AND DISCUSSION First Study (Chickens) The nematode levels determined for the penfree chickens are given in Table 1, specific to nematode species and treatment group. Only Ascaridia galli and Heterakis gallinarum were found, a finding dissimilar to birds sourced from other farms of this same cooperative wherein pen-free birds were infected with these 2 nematodes plus 2 cestodes (Raillietina cesticillus and Choanataenia infundibulum) and a trematode (Echinostoma sp.; T. A. Yazwinski and C. A. Tucker, unpublished data). Based on geometric means, anthelmintic efficacy for fenbendazole (delivered orally at the
77
rate of 5 mg·kg −1 of BW in 1 d) was 85.5% for A. galli and 89.5% of H. gallinarum. These levels of effectiveness are lower than the 90% threshold which is required for a product to be considered effective [7]. Because this was an off-label dose rate and means of administration for fenbendazole, no general conclusions can be made from these data relative to the effectiveness of any future label-indicated regimen of fenbendazole in the treatment of roundworm and cecal worm infections in chickens. However, this dose rate and regimen have been a standard in this laboratory for assessing anthelmintic effectiveness of various products in poultry, with previous levels of efficacy for fenbendazole at 100% for A. galli [9]. The reason(s) for this depressed level of efficacy for fenbendazole in the treatment of these common nematode parasites of the chicken can only be speculated upon at this time. Resistance is not indicated, because anthelmintics have never been used at the source facility. Clearly, additional control studies with infected chickens are warranted so that effective products (or combinations thereof) can be identified for use in the future. Second Study (Turkeys) The levels of A. dissimilis as determined for commercial turkeys subjected to experimental treatment are given in Table 2. As delivered in this study, neither benzimidazole was shown to be ≥90% effective. Treatment with albendazole
Table 1. Nematode levels by treatment group for naturally infected chickens Nematode Treatment group Nonmedicated
Fenbendazole
a,b
Parameter Arithmetic mean Range SD Geometric mean Number Arithmetic mean Range SD Geometric mean Number Anthelmintic efficacy (%)1
Ascaridia galli 18.6 2–73 18.4 12.4a 20 3.9 0–17 5.4 1.8b 14 85.5
Geometric means in the same column with different superscripts are different (P ≤ 0.05). Based on geometric means.
1
Heterakis gallinarum 62.7 2–191 65.0 32.4a 20 5.7 0–24 6.6 3.4b 14 89.5
JAPR: Research Report
78
Table 2. Levels of Ascaridia dissimilis by treatment group (and calculated efficacies) for naturally infected turkeys Treatment group Control Albendazole Fenbendazole Oral Feed
A. dissimilis (all stages combined) Range
AM1
0–11 1–17
5.4 5.8
0–5 0–37
1.6 3.9
GM1
% efficacy
3.5 4.8
4.2a 4.6a
— 0
1.6 11.6
1.2b 0.7b
71.4 83.3
SD
a,b
Geometric means with different superscripts are different (P < 0.05). AM = arithmetic mean; GM = geometric mean.
1
at 10 mg·kg −1 of BW resulted in 0% efficacy. Treatment with fenbendazole, either in the feed (16 ppm for 6 d) or as an oral drench (5 mg·kg −1 of BW in 1 d), significantly depressed worm counts, but neither regimen resulted in ≥90% effectiveness. Historically, fenbendazole has been shown to be highly efficacious when targeting A. dissimilis [10, 11]. This apparent reduction in effectiveness coincident with extensive use over time is not surprising, because resistance to benzimidazoles is a common observation in other farm animal–parasite models [12, 13]. Given the previous work at this laboratory documenting <90% efficacy for benzimidazoles in the treatment of multiply-sourced A. dissimilis [3], combined with the these data attesting to depressed benzimidazole efficacy in the treatment of commercial turkeys for ascaridiasis, it appears that resistance has become established in the United States commercial turkey population. This population of turkeys, however, is not homogeneous, with quite divergent patterns of anthelmintic usage and parasite challenge on a per farm basis—factors that would ultimately determine the current levels of anthelmintic effectiveness that exist.
CONCLUSIONS AND APPLICATIONS Anthelmintic effectiveness was evaluated for benzimidazoles in 2 diverse populations of naturally-infected poultry; organic/pen-free laying hens and commercial turkeys. With both host–parasite models, products were found to be consistently <90% efficacious. This level of effectiveness is surprising, because all previous work at this laboratory has documented excellent efficacy for benzimidazoles against both as-
carids and cecal worms. Given the ubiquity and pathogenicities of these nematode parasites, and the need for effective treatment for their parasitic infections, producers should determine the levels of infection and product efficacies that have developed over time at their operations, and implement control measures (chemical, nonchemical, or both) accordingly.
REFERENCES AND NOTES 1. Yazwinski, T. A., and C. A. Tucker. 2008. Nematodes and acanthocephalans. Pages 1025–1056 in Diseases of Poultry. 12th ed. Y. M. Saif, ed. Blackwell Publishing, Cambridge, MA. 2. Kaplan, R. M., and A. N. Vidyashankar. 2012. An inconvenient truth: Global worming and anthelmintic resistance. Vet. Parasitol. 186:70–78. 3. Perkins, J., T. A. Yazwinski, and C. A. Tucker. 2012. Efficacies of fenbendazole and albendazole in the treatment of commercial turkeys artificially infected with Ascaridia dissimilis. Discovery. 13:61–66. 4. Safe-Guard, Intervet Inc., Summit, NJ. 5. Valbazen, Pfizer Animal Health, Kalamazoo, MI. 6. Safe-Guard medicated pre-mix (EZ Scoop), Intervet Inc., Summit, NJ. 7. Yazwinski, T. A., H. D. Chapman, R. B. Davis, T. Letonja, L. Pote, L. Maes, J. Vercuysse, and D. E. Jacobs. 2003. World Association for the Advancement of Veterinary Parasitology guidelines for evaluating the effectiveness of anthelmintics in chickens and turkeys. Vet. Parasitol. 116:159–173. 8. Littell, R. C., G. A. Milliken, W. W. Stroup, and R. D. Wolfinger. 1996. SAS System for Mixed Models. SAS Inst. Inc., Cary, NC. 9. Yazwinski, T. A., C. Tucker, H. Featherston, Z. Johnson, and K. Wilson. 1994. A summary on a potpourri of parasite projects from Arkansas. Page 13 in Proc. Anim. Dis. Res. Workers in Southern States, Conf. on Animal Parasites. Abstr. No. 74. 10. Yazwinski, T. A., M. Rosenstein, R. Schwartz, K. Wilson, and Z. Johnson. 1993. The use of fenbendazole in the treatment of commercial turkeys infected with Ascaridia dissimilis. Avian Pathol. 22:177–181.
Yazwinski et al.: BENZIMIDAZOLE EFFICACY 11. Yazwinski, T. A., C. Tucker, A. Stelzleni, Z. Johnson, J. Robins, K. Downum, M. Fincher, J. Matlock, and H. Chapman. 2002. Subclinical effects and fenbendazole treatment of turkey ascaridiasis under simulated field conditions. Avian Dis. 46:886–892. 12. Silvestre, A., and J. Cabaret. 2002. Mutation in position 167 of isotype 1 beta-tubulin gene of trichostrongylid nematodes: Role in benzimidazole resistance? Mol. Biochem. Parasitol. 120:297–300.
79
13. Drogemuller, M., T. Schneider, and G. von SamsonHimmelstjerna. 2004. Effect of repeated benzimidazole treatments with increasing dosages on the phenotype of resistance and the beta-tubulin codon 200 genotype distribution in a benzimidazole-resistant cyathostomin population. Vet. Parasitol. 123:201–213.
Observations of benzimidazole efficacies against Ascaridia dissimilis, Ascaridia galli, and Heterakis gallinarum in naturally infected poultry T. A. Yazwinski,*1 C. A. Tucker,* E. Wray,* L. Jones,* and F. D. Clark† *Department of Animal Science, and †Department of Poultry Science, University of Arkansas, Fayetteville 72701 Primary Audience: Poultry Flock Managers, Veterinarians, Nutritionists SUMMARY Two studies were conducted to provide current efficacy evaluation for benzimidazoles used in poultry. In the first study, naturally infected laying hens from an organic, free-range facility were treated with fenbendazole as an oral drench at the rate of 5.0 mg·kg−1 of BW. Based on treatment group, geometric means for all stages combined, fenbendazole was 85.5 and 89.5% effective for the removal of Ascaridia galli and Heterakis gallinarum populations, respectively. In the second study, naturally infected turkeys from a commercial grower were treated with albendazole as an oral suspension at the rate of 10 mg·kg −1 of BW, treated with fenbendazole as an oral suspension at the rate of 5 mg·kg −1 of BW, treated with fenbendazole for 6 d with feed medicated at the concentration of 16 ppm, or left as control. Based on treatment group geometric means for all stages combined, efficacies for A. dissimilis were 0, 71.4, and 83.3% for albendazole drench, fenbendazole drench, and fenbendazole-medicated feed, respectively. Key words: chicken, turkey, nematode infection, efficacy, fenbendazole, albendazole 2013 J. Appl. Poult. Res. 22:75–79 http://dx.doi.org/10.3382/japr.2012-00606
DESCRIPTION OF THE PROBLEM Helminth infections of poultry are both varied and common [1]. Treatment of these infections is also extremely varied, dependent upon production type, stage of production, type of bird, and producer preferences. Periodic evaluation of anthelmintics used in poultry is desirable so that producers can formulate effective strategies for helminth control and thereby improve feed efficiencies, production performance, and overall bird health. Additionally, anthelmintic efficacies must be constantly monitored so that the transition of product efficacies from 1
Corresponding author: [email protected]
effective (≥90% efficacy) to less than effective (<90% efficacy) can be determined and treatment/husbandry strategies be implemented which might provide remedy. Helminth parasitisms of domestic animals are most commonly dealt with via chemical intervention, a practice which invariably results in resistance by the targeted parasites; a situation that is the norm in horse, cattle, and small ruminant production [2]. With these other animal industries, the emphasis has been on monitoring the extent of anthelmintic resistance, and formulation of strategies that might deal with the developing problem (searching for new compounds, studies on the feasibil-
JAPR: Research Report
76 ity of combination therapy, revisiting husbandry means of control, nutraceutical usage, and so on). The same approach would seem to be advisable for the poultry industry. Recently, depressed levels of effectiveness were detected for benzimidazoles used in the treatment of turkeys harboring artificial infections with Ascaridia dissimilis [3]. Given these findings, the current research was undertaken as a means to validate the former findings with natural infections. Additionally, given the growing popularity of organic and natural production of poultry and poultry products, determining the effectiveness of anthelmintics used in the salvage treatment of birds originating from these industries was indicated.
MATERIALS AND METHODS First Study (Chickens) Approximately 40 chickens (Bovan Brown) from an organic, free-range egg production operation in Arkansas were obtained at the time of scheduled depopulation (bird age of 77 to 79 wk). Upon delivery to the research facility, the birds were evenly divided via a random process into 2 adjacent pens. After a 7 d acclimation period, unhealthy birds were culled and the remaining birds were weighed, sorted via a random process into treatment groups within each pen, and treated accordingly. Control birds (10 per pen) were left unmedicated. Treated birds (7 per pen) were orally administered fenbendazole [4] in suspension at the rate of 5 mg·kg −1 of BW, with the total dose given in halves at 0900 and 1600 h. Seven days posttreatment, all birds were killed for parasite collection and enumeration. Second Study (Turkeys) Approximately fifty 8-wk-old turkeys were obtained from a commercial turkey operation in Arkansas immediately before their initial, scheduled anthelmintic treatment. Upon delivery to the research facility, they were evenly divided via random process into 4 adjacent pens. After an 11-d acclimation period, unhealthy birds were culled and the remaining birds were given an experimental treatment (one treatment group per pen). Control birds were left unmedi-
cated. Birds treated with albendazole [5] were given the product on d 3 at the dose rate of 10 mg·kg −1 of BW, as an oral suspension, with the total dose given in halves at 0900 and 1600 h. Birds treated with fenbendazole as an oral suspension [4] were treated on d 3 at the dose rate of 5 mg·kg −1 of BW, with the total dose given in halves at 0900 and 1600 h. Birds treated with fenbendazole in the feed [6] were supplied ration medicated with fenbendazole at a concentration of 16 ppm. Medicated ration was supplied ad libitum for 6 continuous days (d 0 to 6), after which time the ration was replaced with the standard, unmedicated feed. All study birds were killed on d 9. Parasitology Feed was withheld from all birds for 12 h before they were killed. At necropsy, the intestine from gizzard to vent (with ceca for chickens only) was removed from each bird, stripped of mesentery, and opened lengthwise. The opened tract (with contents and washings) was then placed into one container and refrigerated overnight. The following morning, the tract was withdrawn from the container through a clenched fist to express all contents and mucosal slurry. All collected materials in the container were then washed over a 75-μm-aperture sieve, and the residue was collected and preserved with formalin until inspection at 10× to 70× magnification for nematode identifications and counts. This procedure is compliant with current guidelines for poultry anthelmintic studies [7], and parasite descriptions used in this study for nematode identifications can be found elsewhere [1]. Statistics A mixed-model analysis was performed on the data using the MIXED procedure of SAS [8]. Each individual bird was an experimental unit with fixed effects sourced by treatment group (the only source of variance). Prior to ANOVA, species-specific parasite counts were transformed to the log10 of (x + 1). For all counts, all developmental stages for a particular species were combined, because only a small number of larval stages was detected for the birds. Treatment effect was determined to be significant (P
Yazwinski et al.: BENZIMIDAZOLE EFFICACY ≤ 0.05) with an F-test (2 treatment groups) or a significant F-test followed by repeated t-tests (3 treatment groups). Bird Welfare Both studies were conducted after review of the protocols by the University of Arkansas Animal Use and Welfare Committee. All birds were monitored at a minimum of twice daily for health and well-being. Lighting was constant for both studies, water availability was ad libitum throughout, and feed deprivation was likewise ad libitum until overnight withdrawal before birds were killed by cervical dislocation.
RESULTS AND DISCUSSION First Study (Chickens) The nematode levels determined for the penfree chickens are given in Table 1, specific to nematode species and treatment group. Only Ascaridia galli and Heterakis gallinarum were found, a finding dissimilar to birds sourced from other farms of this same cooperative wherein pen-free birds were infected with these 2 nematodes plus 2 cestodes (Raillietina cesticillus and Choanataenia infundibulum) and a trematode (Echinostoma sp.; T. A. Yazwinski and C. A. Tucker, unpublished data). Based on geometric means, anthelmintic efficacy for fenbendazole (delivered orally at the
77
rate of 5 mg·kg −1 of BW in 1 d) was 85.5% for A. galli and 89.5% of H. gallinarum. These levels of effectiveness are lower than the 90% threshold which is required for a product to be considered effective [7]. Because this was an off-label dose rate and means of administration for fenbendazole, no general conclusions can be made from these data relative to the effectiveness of any future label-indicated regimen of fenbendazole in the treatment of roundworm and cecal worm infections in chickens. However, this dose rate and regimen have been a standard in this laboratory for assessing anthelmintic effectiveness of various products in poultry, with previous levels of efficacy for fenbendazole at 100% for A. galli [9]. The reason(s) for this depressed level of efficacy for fenbendazole in the treatment of these common nematode parasites of the chicken can only be speculated upon at this time. Resistance is not indicated, because anthelmintics have never been used at the source facility. Clearly, additional control studies with infected chickens are warranted so that effective products (or combinations thereof) can be identified for use in the future. Second Study (Turkeys) The levels of A. dissimilis as determined for commercial turkeys subjected to experimental treatment are given in Table 2. As delivered in this study, neither benzimidazole was shown to be ≥90% effective. Treatment with albendazole
Table 1. Nematode levels by treatment group for naturally infected chickens Nematode Treatment group Nonmedicated
Fenbendazole
a,b
Parameter Arithmetic mean Range SD Geometric mean Number Arithmetic mean Range SD Geometric mean Number Anthelmintic efficacy (%)1
Ascaridia galli 18.6 2–73 18.4 12.4a 20 3.9 0–17 5.4 1.8b 14 85.5
Geometric means in the same column with different superscripts are different (P ≤ 0.05). Based on geometric means.
1
Heterakis gallinarum 62.7 2–191 65.0 32.4a 20 5.7 0–24 6.6 3.4b 14 89.5
JAPR: Research Report
78
Table 2. Levels of Ascaridia dissimilis by treatment group (and calculated efficacies) for naturally infected turkeys Treatment group Control Albendazole Fenbendazole Oral Feed
A. dissimilis (all stages combined) Range
AM1
0–11 1–17
5.4 5.8
0–5 0–37
1.6 3.9
GM1
% efficacy
3.5 4.8
4.2a 4.6a
— 0
1.6 11.6
1.2b 0.7b
71.4 83.3
SD
a,b
Geometric means with different superscripts are different (P < 0.05). AM = arithmetic mean; GM = geometric mean.
1
at 10 mg·kg −1 of BW resulted in 0% efficacy. Treatment with fenbendazole, either in the feed (16 ppm for 6 d) or as an oral drench (5 mg·kg −1 of BW in 1 d), significantly depressed worm counts, but neither regimen resulted in ≥90% effectiveness. Historically, fenbendazole has been shown to be highly efficacious when targeting A. dissimilis [10, 11]. This apparent reduction in effectiveness coincident with extensive use over time is not surprising, because resistance to benzimidazoles is a common observation in other farm animal–parasite models [12, 13]. Given the previous work at this laboratory documenting <90% efficacy for benzimidazoles in the treatment of multiply-sourced A. dissimilis [3], combined with the these data attesting to depressed benzimidazole efficacy in the treatment of commercial turkeys for ascaridiasis, it appears that resistance has become established in the United States commercial turkey population. This population of turkeys, however, is not homogeneous, with quite divergent patterns of anthelmintic usage and parasite challenge on a per farm basis—factors that would ultimately determine the current levels of anthelmintic effectiveness that exist.
CONCLUSIONS AND APPLICATIONS Anthelmintic effectiveness was evaluated for benzimidazoles in 2 diverse populations of naturally-infected poultry; organic/pen-free laying hens and commercial turkeys. With both host–parasite models, products were found to be consistently <90% efficacious. This level of effectiveness is surprising, because all previous work at this laboratory has documented excellent efficacy for benzimidazoles against both as-
carids and cecal worms. Given the ubiquity and pathogenicities of these nematode parasites, and the need for effective treatment for their parasitic infections, producers should determine the levels of infection and product efficacies that have developed over time at their operations, and implement control measures (chemical, nonchemical, or both) accordingly.
REFERENCES AND NOTES 1. Yazwinski, T. A., and C. A. Tucker. 2008. Nematodes and acanthocephalans. Pages 1025–1056 in Diseases of Poultry. 12th ed. Y. M. Saif, ed. Blackwell Publishing, Cambridge, MA. 2. Kaplan, R. M., and A. N. Vidyashankar. 2012. An inconvenient truth: Global worming and anthelmintic resistance. Vet. Parasitol. 186:70–78. 3. Perkins, J., T. A. Yazwinski, and C. A. Tucker. 2012. Efficacies of fenbendazole and albendazole in the treatment of commercial turkeys artificially infected with Ascaridia dissimilis. Discovery. 13:61–66. 4. Safe-Guard, Intervet Inc., Summit, NJ. 5. Valbazen, Pfizer Animal Health, Kalamazoo, MI. 6. Safe-Guard medicated pre-mix (EZ Scoop), Intervet Inc., Summit, NJ. 7. Yazwinski, T. A., H. D. Chapman, R. B. Davis, T. Letonja, L. Pote, L. Maes, J. Vercuysse, and D. E. Jacobs. 2003. World Association for the Advancement of Veterinary Parasitology guidelines for evaluating the effectiveness of anthelmintics in chickens and turkeys. Vet. Parasitol. 116:159–173. 8. Littell, R. C., G. A. Milliken, W. W. Stroup, and R. D. Wolfinger. 1996. SAS System for Mixed Models. SAS Inst. Inc., Cary, NC. 9. Yazwinski, T. A., C. Tucker, H. Featherston, Z. Johnson, and K. Wilson. 1994. A summary on a potpourri of parasite projects from Arkansas. Page 13 in Proc. Anim. Dis. Res. Workers in Southern States, Conf. on Animal Parasites. Abstr. No. 74. 10. Yazwinski, T. A., M. Rosenstein, R. Schwartz, K. Wilson, and Z. Johnson. 1993. The use of fenbendazole in the treatment of commercial turkeys infected with Ascaridia dissimilis. Avian Pathol. 22:177–181.
Yazwinski et al.: BENZIMIDAZOLE EFFICACY 11. Yazwinski, T. A., C. Tucker, A. Stelzleni, Z. Johnson, J. Robins, K. Downum, M. Fincher, J. Matlock, and H. Chapman. 2002. Subclinical effects and fenbendazole treatment of turkey ascaridiasis under simulated field conditions. Avian Dis. 46:886–892. 12. Silvestre, A., and J. Cabaret. 2002. Mutation in position 167 of isotype 1 beta-tubulin gene of trichostrongylid nematodes: Role in benzimidazole resistance? Mol. Biochem. Parasitol. 120:297–300.
79
13. Drogemuller, M., T. Schneider, and G. von SamsonHimmelstjerna. 2004. Effect of repeated benzimidazole treatments with increasing dosages on the phenotype of resistance and the beta-tubulin codon 200 genotype distribution in a benzimidazole-resistant cyathostomin population. Vet. Parasitol. 123:201–213.