Brief Communication Communication brève Survey of gastrointestinal nematode parasites in Saskatchewan beef herds Murray Jelinski, Emily Lanigan, John Gilleard, Cheryl Waldner, Grant Royan Abstract — A survey of gastrointestinal parasites in Saskatchewan beef herds was conducted over the summer of 2014. Fecal samples were collected on 3 occasions during the summer grazing season from beef cows and calves from 14 herds. The mean number of strongylid eggs per gram of feces recovered from calves increased 9-fold (95% CI: 4.5 to 18) over the summer period, while egg counts in the cows remained constant over the same period. The prevalence and infection intensities of gastrointestinal nematode parasites in cow-calf herds in Saskatchewan were comparable to what is seen in cattle grazing in the northern regions of the United States and for which anthelmintic treatments have resulted in positive production benefits. Résumé — Enquête sur les parasites nématodes gastro-intestinaux chez les troupeaux de bovins de boucherie de la Saskatchewan. Une enquête sur les parasites gastro-intestinaux dans des troupeaux bovins de la Saskatchewan a été réalisée à l’été 2014. Des échantillons fécaux ont été prélevés à trois occasions durant la saison de pâturage de l’été auprès des bovins de boucherie et des veaux provenant de 14 troupeaux. Le nombre moyen d’œufs de strongylidés par gramme de fèces prélevées chez les veaux a augmenté de neuf fois (IC de 95 % : de 4,5 à 18) pendant la période de l’été, tandis que les numérations d’œufs chez les vaches sont demeurées constantes pendant la même période. La prévalence et l’intensité des infections par les parasites nématodes gastro-intestinaux chez les troupeaux veaux-vaches de la Saskatchewan étaient comparables à ceux des régions de pâturage du nord des États-Unis où des traitements anthelminthiques ont eu des résultats positifs sur la production. (Traduit par Isabelle Vallières) Can Vet J 2016;57:160–163
G
astrointestinal nematodes (GIN) cost the North American beef and dairy industries . $2 billion annually in additional treatment costs and suboptimal productivity (1). While overt clinical disease due to GIN infections occurs infrequently in cattle raised in the temperate regions of the northern hemisphere, sub-clinical disease can have a significant impact on the production performance of pastured beef cattle (2). Furthermore, the incidence of subclinical GIN-related parasitism may be increasing. Researchers have documented changes in the patterns of gastrointestinal nematode infections of grazing rumi-
Department of Large Animal Clinical Sciences (Jelinski, Waldner), Western College of Veterinary Medicine, University of Saskatchewan S7N 5B4; Comparative Biology and Experimental Medicine, Faculty of Veterinary Medicine, University of Calgary, Calgary T2N 1N4 (Gilleard); 826 Kenderdine Road, Saskatoon, Saskatchewan S7N 4V5 (Lanigan); Intervet Canada Corp., 16750 route Transcanadienne, Kirkland, Quebec H9H 4M7 (Royan). Address all correspondence to Dr. Murray Jelinski; e-mail: [email protected] Reprints will not be available from the authors. Use of this article is limited to a single copy for personal study. Anyone interested in obtaining reprints should contact the CVMA office ([email protected]) for additional copies or permission to use this material elsewhere. 160
nants as a result of emerging anthelmintic drug resistance (3), climatic changes (4), and changes in grazing management (5,6). Despite the potential deleterious effects of GIN on pastured cattle, there is a paucity of published research describing the epidemiology of GIN in pastured beef cattle in western Canada. In 1987, Polley and Bickis (7) examined 1400 fecal samples from cows, yearlings, and calves spread across 5 community pastures and 1 intensive rotational grazing system, all of which were located in Saskatchewan. Approximately half of the fecal samples obtained from the community pastured cows (53%), yearlings (44%), and calves (65%) tested positive for GIN eggs, whereas 63% of the cow and 95% of the calf fecal samples from the intensively managed cattle tested positive for GIN eggs. Kennedy et al (8–10) reported a few years later on 3 studies in which they evaluated the efficacy of ivermectin administered to beef cattle pastured in the province of Alberta. Ivermectin treatment had a positive effect on weight gain with fecal egg counts (FEC) in the nontreated animals being in the 15 to 20 eggs per gram (epg) range. Around the same time, Cox and Lemiski (11) sampled pastured replacement dairy heifers from 34 different operations across western Canada and reported that 93% of animals tested positive for GIN eggs, averaging 16 epg. Most other western Canadian cattle parasite studies have involved comparing the effectiveness of anthelmintic products on reducing FEC and improving performance (average daily gain and feed efficiency) in feedlot cattle. The first such study was published by Stockdale and Harries (12) in CVJ / VOL 57 / FEBRUARY 2016
Table 1. Summary table showing the number of cows (calves) sampled during each of the 3 sampling periods; the date each producer turned their cow-calf pairs onto pasture; and the date ivermectin was administered. N = 1199
A B C D E F G H I J K L M N
15 (6) 17 (2) 20 (20) 20 (13) 20 (20) 20 (20) NS NS NS NS NS NS NS NS
21 (12) 20 (21) 20 (20) 20 (20) 20 (14) 20 (20) 13 (2) 12 (5) 21 (24) 20 (12) 20 (16) 23 (18) 22 (20) 21 (22)
20 (12) 20 (20) 20 (20) 20 (20) 20 (20) 20 (20) 20 (15) 20 (20) 20 (16) 20 (20) 21 (21) 20 (20) 20 (20) NS
Totals
112 (81)
273 (228)
261 (244)
May 15 May 1 April 28 May 5 May 15 April 1 May 15–25 May 15–26 May 15–27 May 15 June 1 May 22 May 15 May 15
B R I E F C O M M U N I CAT I O N
Sampling 1 Sampling 2 Sampling 3 Ivermectin Herd Cows Cows Cows application ID (calves) (calves) (calves) Turn-out (dd/mm/yy) 08/01/13, 30/05/14 01/12/13 17/10/13 18/10/13 01/12/13 01/11/13 01/03/14 01/03/14 01/03/14 01/12/13 30/11/13; 15/06/14a 19/11/13 15/11/13 25/11/13
Sampling periods: 1 — May 30 to June 26; 2 — July 3 to July 21; 3 — July 22 to August 6. a Both cows and calves were treated with ivermectin on this date. NS — Not significant.
1979, and although treatment resulted in a dramatic reduction in FEC, there was no improvement in average daily gain. Multiple feedlot studies followed, all of which compared the relative efficacy and/or cost-effectiveness of ivermectin to an organophosphate (fenthion) product or to fenthion used in combination with a benzimidazole anthelmintic (fenbendazole or oxfendazole). The ivermectin treatment groups consistently outperformed the other groups; however, it is equivocal as to whether the improvement in performance was solely related to enhanced control of internal parasites (13–17). More recently, Colwell et al (18) reported on the annual variation in serum antibody concentrations to Ostertagia ostertagi in beef cattle pastured in southern Alberta. The following describes the results of a parasite study that was conducted over a 3-month period in the summer of 2014. Fourteen cow-calf operations, located within a 170 km radius of Saskatoon, were selected based upon geographical location, the producer’s willingness to participate, and herd size. Each producer provided data as to when the cow-calf pairs were placed on pasture, history of anthelmintic usage, timing of the calving season, and herd size. The average herd size was 102 cow-calf pairs. Fresh environmental fecal samples were collected from cows [mean: 20 6 2 standard deviation (SD)] and calves (mean: 17 6 6) from each herd on 3 different occasions 1 mo apart; no effort was made to sample the same animals. Collection involved monitoring the cattle until they defecated, at which time the sample was collected, bagged, labeled, and transported on ice to the laboratory. Samples were processed that day or stored at 4°C for a maximum of 5 d before processing. Fecal aliquots weighing 3 g were processed according to the Modified Wisconsin Sugar Flotation Technique (19); the same person interpreted all the slides. Most Trichostrongyloidea eggs have a similar appearance and hence they were recorded collectively as strongylid eggs. The exceptions are Nematodirus spp. and Trichuris spp. eggs, which CVJ / VOL 57 / FEBRUARY 2016
have distinctive morphology and hence were enumerated separately. All results were reported as epg. Coccidia were identified and scored as: “11” if there were , 10 oocysts per slide; “21” if there were 10 to 50 oocysts per field of view; and “31” if there were . 50 oocysts in most fields of view. Moniezia spp. eggs were recorded as either present or absent. The results were summarized using a commercial statistical software package (StataSE version 13; Stata, College Station, Texas, USA). Differences in strongylid egg counts, both among sample collection times and between cows and calves, were examined using generalized linear mixed models with a negative binomial distribution. Random intercepts were used to account for potential clustering of strongylid egg counts within sample for each herd and across sample times within herd. Table 1 shows the number of cow (n = 646) and calf (n = 553) samples by herd and sampling period, the dates that the herds were placed on pasture, and the history of the most recent anthelmintic treatments. All producers treated their cows with an ivermectin product (Table 1), but only 1 producer treated both cows and calves. Mean strongylid egg counts for the calves increased by 9.0 times (95% CI: 4.5 to 18) from the first to third sample period; however, there was no comparable relative increase in the mean strongylid egg counts for the cows (1.5 times, 95% CI: 0.8 to 2.8), Figure 1. The cows’ strongylid egg counts were 4.1 (95% CI: 2.5 to 6.8) and 1.4 times (95% CI: 1.0 to 1.8) higher than those of the calves at the first and second sampling periods, respectively (Figure 1). However, by the third sample period the calves’ strongylid egg counts were 1.5 times (95% CI: 1.1 to 1.9) those of the cows. The number of strongylid eggs in the calves at the third sampling varied from 0 to 143 epg. Trichuris spp. eggs were an infrequent finding with 8 calves having # 4 epg at either the first or second sampling. Similarly, Moniezia spp. eggs were identified in 20 calf samples obtained at the second and third samplings. In contrast, 22.6% (123/545) of the calf fecal samples had Nematodirus spp. eggs, 75.6% of 161
Mean eggs per gram
C O M M U N I CAT I O N B R È V E
14 12
Calves
Cows
c
10 8 6 b
4 2 0
a
Sample 1
Sample 2
Sample 3
Sampling period
Figure 1. Predicted mean (error bars indicate 95% CI) number of strongylid eggs per gram of feces based on negative binomial model that accounted for clustering of cows within sample period for each herd and sampling periods within herd. Data represent 14 herds, 545 calf fecal samples, and 646 cow fecal samples. Unmatched superscripts (a, b, and c) indicate significant differences at P , 0.001.
which had # 3 epg; all but 2 herds had calves that were passing Nematodirus spp. eggs. Approximately 40% of the calves’ fecal samples had coccidia oocysts, 88.9% of which graded 11. Unlike the calves, the adult cows had egg counts which remained low and constant over the 3 sampling periods. Two cows had 1 Trichuris spp. epg at the time of the second sample period, while 7 cows from 4 farms had # 2 Nematodirus spp. epg at either the second or third sample periods. Sixty-three cows from all 14 herds tested positive for Moniezia spp. eggs. Coccidia oocysts were found in 23.4% (151/646) of the cows’ fecal samples, 96.0% of which graded 11. The fecal egg shedding patterns were consistent with the known biology and epidemiology of GIN common to cattle raised in temperate regions (1,2,5,21). The finding that the cows had lower, and near constant FEC, across the 3 time periods was expected. These lower FEC can be attributed to the cows having acquired immunity to parasites resident on pastures (21). There was no evidence of a periparturient rise in FEC; however, most cows had calved prior to the first sampling period. In contrast to the FEC in the cows, the egg counts in the calves continued to increase as the summer months progressed, which was expected. While the biology of cattle nematodes varies by species, environmental conditions, and host immunity, the increasing FEC in the calves was similar to what has been reported in pastured beef cattle in the province of Quebec (22). Following turn-out to pasture the immunologically naïve calves would have begun ingesting infective L3 larvae, with overwintered larvae typically being the main source of infection (21). The cows would have also contributed to the pasture contamination, with eggs in the newly deposited fecal pats developing into infective larvae. The prepatent period of most GIN during the warm summer months is 28 d and hence there would have been amplification of the parasites over the ensuing summer months. Although a variety of rotational grazing schemes have been devised to decrease parasite populations, grazing management alone is insufficient for the control of GIN (5). This is largely related to the fact that the infective larvae can survive on pasture, even in harsh winter and hot summer conditions. In this instance, had the trial been extended later into the fall and early winter, then the calves’ FEC would have continued 162
to increase until late October to December, at which time most of the ingested larvae would have entered into arrested development versus continuing onto becoming adult worms. Arrested development is a survival mechanism that is triggered when the infective larvae are exposed to inclement weather, hot weather in the southern regions and cold weather in the north. While the fecal egg floatation method is a simple method for monitoring FEC at the herd level (20), FEC are an indirect (and insensitive) measure of parasite infection intensity (23). Therefore caution must be exercised when attempting to correlate egg counts to the number of larvae and adult worms within the gastrointestinal tract; egg counts are influenced by a variety of factors such as season, fecundity of the parasite species, host immunity, and the dilution effects of feces (6,20). Given these caveats, the FEC were broadly similar to what has been reported in cow-calf herds located in the major cattle grazing regions of the northern United States (21,23). Specifically, a recent multicentre study of a long-acting eprinomectin formulation administered to grazing beef cattle showed that there were significant production gains even though the mean FEC of the control groups at the end of the grazing season were relatively low: 4, 8, 17, 21, 19, and 220 epg in Wisconsin, Minnesota, Oregon, Louisiana, Missouri, and Arkansas, respectively (24). The current study was not designed to look at parasite control measures; however, it is noteworthy that all the producers were applying ivermectin in the fall, and only 3 used this product in the spring. While fall application of parasiticides is convenient and optimal for the control of ectoparasites such as grubs (Hypoderma spp.) and lice, this is a suboptimal time for controlling GIN. Ultimately, the goal of all control strategies hinges upon reducing the level of larval populations on pasture (5). This is achieved by the use of strategic deworming programs, wherein anthelmintics are used in combination with grazing management to reduce infection pressures. A common example is the use of the Weybridge system, in which the animals are dewormed and then moved onto clean pastures. However, few pastures are truly clean and hence retreatment or the use of sustained release or long-acting anthelmintics may be required. A number of factors could lead to increased parasitism of grazing beef cattle in western Canada by GIN parasites. Increased herd size and the adoption of intensive rotational grazing systems and low-cost overwintering feeding systems (i.e., swath and bale grazing) translate into higher stocking densities, which contribute to greater pasture contamination and increased infection pressure. Secondly, anthelmintic resistance is well-documented in other regions and presumably this could lead to increased parasite burdens and/or changes in parasite species distribution in western Canada (3,25). And thirdly, climatic changes have been postulated as a causal factor for changing the epidemiology of GIN infections in sheep (4), and a similar scenario could, in time, alter the epidemiology of GIN in western Canada’s grazing beef cattle. Producers have relied on applications of broad-spectrum macrocyclic lactone pour-on products to cows in the fall for many years. However, this is not an evidence-based approach and the work presented herein suggests that parasite control in western Canada is not currently optimal. Unfortunately, the CVJ / VOL 57 / FEBRUARY 2016
Acknowledgments We acknowledge Dr. Janice Berg, Glen Cartwright, and Merck Animal Health (Canada) for both logistical and financial support of this project. We also acknowledge Katrina Barth, Laura Campbell, and Tim Campbell for their assistance in sample collection and preparation. CVJ
References 1. Stromberg BE, Gasbarre LC. Gastrointestinal nematode control programs with an emphasis in cattle. Vet Clin Food Anim 2006;22: 543–565. 2. Forbes AB, Cutler KL, Rice BJ. Sub-clinical parasitism in spring-born, beef suckler calves: Epidemiology and impact on growth performance during the first grazing season. Vet Parasitol 2002;104:339–344. 3. Gasbarre LC, Smith LL, Lichtenfels JR, Pilitt PA. The identification of cattle nematode parasites resistant to multiple classes of anthelmintics in a commercial cattle population in the US. Vet Parasitol 2009; 166:281–285. 4. Morgan ER, van Dijk J. Climate and the epidemiology of gastrointestinal nematode infections of sheep in Europe. Vet Parasitol 2012;189: 8–14. 5. Stromberg BE, Averbeck GA. The role of parasite epidemiology in the management of grazing cattle. Int J Parasitol 1999;29:33–39. 6. Yazwinski TA, Tucker CA. A sampling of factors relative to the epidemiology of gastrointestinal nematode parasites of cattle in the United States. Vet Clin Food Anim 2006;22:501–527. 7. Polley L, Bickis MG. Gastrointestinal nematode parasites in Saskatchewan cattle: Egg count distributions in beef animals. Can J Vet Res 1987;51:465–469.
CVJ / VOL 57 / FEBRUARY 2016
8. Kennedy MJ, ZoBell DR. Evaluation of ivermectin on performance of beef cattle on pasture in Alberta. Can Vet J 1988;29:566–568. 9. Kennedy MJ, ZoBell DR, Goonewardene L. Effect of invermectin on weight gains in yearling steers on pasture in central Alberta. Can Vet J 1989;30:346–347. 10. Kennedy MR. Effect of invermectin on weight gain of calves on pasture in Alberta. Can Vet J 1990;31:589–590. 11. Cox WR, Lemiski D. Prevalence of gastrointestinal nematodes in dairy heifers in western Canada. Can Vet J 1989;30:666–668. 12. Stockdale PHG, Harries WN. Treatment of feedlot cattle in Alberta for gastrointestinal nematodes. Can Vet J 1979;20:223–226. 13. Bauck SW, Jim GK, Guichon T, Newcomb KM, Cox JL, Barrick R. Comparative cost-effectiveness of ivermectin versus topical organophosphate in feedlot calves. Can Vet J 1989;30:161–164. 14. Jim GK, Booker CW, Guichon PT. Comparison of a combination of oxfendazole and fenthion versus ivermectin in feedlot calves. Can Vet J 1992;33:599–604. 15. Schunicht OC, Guichon PT, Booker CW, et al. Comparative costeffectiveness of ivermectin versus topical organophosphate in feedlot yearlings. Can Vet J 2000;41:220–224. 16. Guichon PT, Jim GK, Booker CW, Schunicht OC, Wildman BK, Brown JR. Relative cost-effectiveness of treatment of feedlot calves with ivermectin versus treatment with a combination of fenbendazole, permethrin, and fenthion. J Am Vet Med Assoc 2000;216:1965–1969. 17. Bauck SW, Piche CA, Newcomb KM. Effect of antiparasitic treatment in beef replacement heifers. Can Vet J 1992;33:394–396. 18. Colwell DD, Beck MA, Goater CP, Abbas RZ. Annual variation in serum antibody concentrations against gastrointestinal nematodes in beef calves in semi-arid rangelands of western Canada. Vet Parasitol 2014;205:169–174. 19. Cox DD, Todd AC. Survey of gastrointestinal parasitism in Wisconsin dairy cattle. J Am Vet Med Assoc 1962;141:706–709. 20. Eysker M, Ploeger HW. Value of present diagnostic methods for gastrointestinal nematode infections in ruminants. Parasitology 2000;120: S109–S119. 21. Gibbs HC. The epidemiology of bovine ostertagiasis in the north temperate regions of North America. Vet Parasitol 1988;27:39–47. 22. Ranjan S, Trudeau C, Prichard RK, Piché C, Bauck S. Epidemiological study of parasite infection in a cow-calf herd in Quebec. 1992;42: 281–293. 23. Malczewski A, Jolley WR, Woodard LF. Prevalence and epidemiology of trichostrongylids in Wyoming cattle with consideration of the inhibited development of Ostertagia ostertagi. Vet Parasitol 1996;64:28–297. 24. Kunkle BN, Williams JC, Johnson EG, et al. Persistent efficacy and production benefits following use of extended-release injectable eprinomectin in grazing beef cattle under field conditions. Vet Parasitol 2013; 192:332–337. 25. Kaplan RM, Vidyashankar AN. An inconvenient truth: Global worming and anthelmintic resistance. Vet Parasitol 2012;186:70–78.
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B R I E F C O M M U N I CAT I O N
information needed to direct effective and sustainable parasite control in grazing beef cattle in western Canada is lacking, including information on the prevalence, epidemiology, and production impacts of the different parasite species as well as on the extent of anthelmintic resistance and the effectiveness of current control measures. Although there are no published data on ivermectin efficacy on cattle parasites in Canada, a recent study suggests the situation is similar to that described in the US where pour-on formulations are not fully effective in many herds. Fifteen out of 34 beef herds sampled across Alberta and Saskatchewan had less than 85% reduction of fecal egg counts following pour-on ivermectin treatment (Avramenko, Redman, Lewis, Royan, Gilleard: Manuscript in preparation). However, the extent to which this poor efficacy is attributable to ivermectin-resistant parasites is not clear; more research is needed in all these areas.
G
astrointestinal nematodes (GIN) cost the North American beef and dairy industries . $2 billion annually in additional treatment costs and suboptimal productivity (1). While overt clinical disease due to GIN infections occurs infrequently in cattle raised in the temperate regions of the northern hemisphere, sub-clinical disease can have a significant impact on the production performance of pastured beef cattle (2). Furthermore, the incidence of subclinical GIN-related parasitism may be increasing. Researchers have documented changes in the patterns of gastrointestinal nematode infections of grazing rumi-
Department of Large Animal Clinical Sciences (Jelinski, Waldner), Western College of Veterinary Medicine, University of Saskatchewan S7N 5B4; Comparative Biology and Experimental Medicine, Faculty of Veterinary Medicine, University of Calgary, Calgary T2N 1N4 (Gilleard); 826 Kenderdine Road, Saskatoon, Saskatchewan S7N 4V5 (Lanigan); Intervet Canada Corp., 16750 route Transcanadienne, Kirkland, Quebec H9H 4M7 (Royan). Address all correspondence to Dr. Murray Jelinski; e-mail: [email protected] Reprints will not be available from the authors. Use of this article is limited to a single copy for personal study. Anyone interested in obtaining reprints should contact the CVMA office ([email protected]) for additional copies or permission to use this material elsewhere. 160
nants as a result of emerging anthelmintic drug resistance (3), climatic changes (4), and changes in grazing management (5,6). Despite the potential deleterious effects of GIN on pastured cattle, there is a paucity of published research describing the epidemiology of GIN in pastured beef cattle in western Canada. In 1987, Polley and Bickis (7) examined 1400 fecal samples from cows, yearlings, and calves spread across 5 community pastures and 1 intensive rotational grazing system, all of which were located in Saskatchewan. Approximately half of the fecal samples obtained from the community pastured cows (53%), yearlings (44%), and calves (65%) tested positive for GIN eggs, whereas 63% of the cow and 95% of the calf fecal samples from the intensively managed cattle tested positive for GIN eggs. Kennedy et al (8–10) reported a few years later on 3 studies in which they evaluated the efficacy of ivermectin administered to beef cattle pastured in the province of Alberta. Ivermectin treatment had a positive effect on weight gain with fecal egg counts (FEC) in the nontreated animals being in the 15 to 20 eggs per gram (epg) range. Around the same time, Cox and Lemiski (11) sampled pastured replacement dairy heifers from 34 different operations across western Canada and reported that 93% of animals tested positive for GIN eggs, averaging 16 epg. Most other western Canadian cattle parasite studies have involved comparing the effectiveness of anthelmintic products on reducing FEC and improving performance (average daily gain and feed efficiency) in feedlot cattle. The first such study was published by Stockdale and Harries (12) in CVJ / VOL 57 / FEBRUARY 2016
Table 1. Summary table showing the number of cows (calves) sampled during each of the 3 sampling periods; the date each producer turned their cow-calf pairs onto pasture; and the date ivermectin was administered. N = 1199
A B C D E F G H I J K L M N
15 (6) 17 (2) 20 (20) 20 (13) 20 (20) 20 (20) NS NS NS NS NS NS NS NS
21 (12) 20 (21) 20 (20) 20 (20) 20 (14) 20 (20) 13 (2) 12 (5) 21 (24) 20 (12) 20 (16) 23 (18) 22 (20) 21 (22)
20 (12) 20 (20) 20 (20) 20 (20) 20 (20) 20 (20) 20 (15) 20 (20) 20 (16) 20 (20) 21 (21) 20 (20) 20 (20) NS
Totals
112 (81)
273 (228)
261 (244)
May 15 May 1 April 28 May 5 May 15 April 1 May 15–25 May 15–26 May 15–27 May 15 June 1 May 22 May 15 May 15
B R I E F C O M M U N I CAT I O N
Sampling 1 Sampling 2 Sampling 3 Ivermectin Herd Cows Cows Cows application ID (calves) (calves) (calves) Turn-out (dd/mm/yy) 08/01/13, 30/05/14 01/12/13 17/10/13 18/10/13 01/12/13 01/11/13 01/03/14 01/03/14 01/03/14 01/12/13 30/11/13; 15/06/14a 19/11/13 15/11/13 25/11/13
Sampling periods: 1 — May 30 to June 26; 2 — July 3 to July 21; 3 — July 22 to August 6. a Both cows and calves were treated with ivermectin on this date. NS — Not significant.
1979, and although treatment resulted in a dramatic reduction in FEC, there was no improvement in average daily gain. Multiple feedlot studies followed, all of which compared the relative efficacy and/or cost-effectiveness of ivermectin to an organophosphate (fenthion) product or to fenthion used in combination with a benzimidazole anthelmintic (fenbendazole or oxfendazole). The ivermectin treatment groups consistently outperformed the other groups; however, it is equivocal as to whether the improvement in performance was solely related to enhanced control of internal parasites (13–17). More recently, Colwell et al (18) reported on the annual variation in serum antibody concentrations to Ostertagia ostertagi in beef cattle pastured in southern Alberta. The following describes the results of a parasite study that was conducted over a 3-month period in the summer of 2014. Fourteen cow-calf operations, located within a 170 km radius of Saskatoon, were selected based upon geographical location, the producer’s willingness to participate, and herd size. Each producer provided data as to when the cow-calf pairs were placed on pasture, history of anthelmintic usage, timing of the calving season, and herd size. The average herd size was 102 cow-calf pairs. Fresh environmental fecal samples were collected from cows [mean: 20 6 2 standard deviation (SD)] and calves (mean: 17 6 6) from each herd on 3 different occasions 1 mo apart; no effort was made to sample the same animals. Collection involved monitoring the cattle until they defecated, at which time the sample was collected, bagged, labeled, and transported on ice to the laboratory. Samples were processed that day or stored at 4°C for a maximum of 5 d before processing. Fecal aliquots weighing 3 g were processed according to the Modified Wisconsin Sugar Flotation Technique (19); the same person interpreted all the slides. Most Trichostrongyloidea eggs have a similar appearance and hence they were recorded collectively as strongylid eggs. The exceptions are Nematodirus spp. and Trichuris spp. eggs, which CVJ / VOL 57 / FEBRUARY 2016
have distinctive morphology and hence were enumerated separately. All results were reported as epg. Coccidia were identified and scored as: “11” if there were , 10 oocysts per slide; “21” if there were 10 to 50 oocysts per field of view; and “31” if there were . 50 oocysts in most fields of view. Moniezia spp. eggs were recorded as either present or absent. The results were summarized using a commercial statistical software package (StataSE version 13; Stata, College Station, Texas, USA). Differences in strongylid egg counts, both among sample collection times and between cows and calves, were examined using generalized linear mixed models with a negative binomial distribution. Random intercepts were used to account for potential clustering of strongylid egg counts within sample for each herd and across sample times within herd. Table 1 shows the number of cow (n = 646) and calf (n = 553) samples by herd and sampling period, the dates that the herds were placed on pasture, and the history of the most recent anthelmintic treatments. All producers treated their cows with an ivermectin product (Table 1), but only 1 producer treated both cows and calves. Mean strongylid egg counts for the calves increased by 9.0 times (95% CI: 4.5 to 18) from the first to third sample period; however, there was no comparable relative increase in the mean strongylid egg counts for the cows (1.5 times, 95% CI: 0.8 to 2.8), Figure 1. The cows’ strongylid egg counts were 4.1 (95% CI: 2.5 to 6.8) and 1.4 times (95% CI: 1.0 to 1.8) higher than those of the calves at the first and second sampling periods, respectively (Figure 1). However, by the third sample period the calves’ strongylid egg counts were 1.5 times (95% CI: 1.1 to 1.9) those of the cows. The number of strongylid eggs in the calves at the third sampling varied from 0 to 143 epg. Trichuris spp. eggs were an infrequent finding with 8 calves having # 4 epg at either the first or second sampling. Similarly, Moniezia spp. eggs were identified in 20 calf samples obtained at the second and third samplings. In contrast, 22.6% (123/545) of the calf fecal samples had Nematodirus spp. eggs, 75.6% of 161
Mean eggs per gram
C O M M U N I CAT I O N B R È V E
14 12
Calves
Cows
c
10 8 6 b
4 2 0
a
Sample 1
Sample 2
Sample 3
Sampling period
Figure 1. Predicted mean (error bars indicate 95% CI) number of strongylid eggs per gram of feces based on negative binomial model that accounted for clustering of cows within sample period for each herd and sampling periods within herd. Data represent 14 herds, 545 calf fecal samples, and 646 cow fecal samples. Unmatched superscripts (a, b, and c) indicate significant differences at P , 0.001.
which had # 3 epg; all but 2 herds had calves that were passing Nematodirus spp. eggs. Approximately 40% of the calves’ fecal samples had coccidia oocysts, 88.9% of which graded 11. Unlike the calves, the adult cows had egg counts which remained low and constant over the 3 sampling periods. Two cows had 1 Trichuris spp. epg at the time of the second sample period, while 7 cows from 4 farms had # 2 Nematodirus spp. epg at either the second or third sample periods. Sixty-three cows from all 14 herds tested positive for Moniezia spp. eggs. Coccidia oocysts were found in 23.4% (151/646) of the cows’ fecal samples, 96.0% of which graded 11. The fecal egg shedding patterns were consistent with the known biology and epidemiology of GIN common to cattle raised in temperate regions (1,2,5,21). The finding that the cows had lower, and near constant FEC, across the 3 time periods was expected. These lower FEC can be attributed to the cows having acquired immunity to parasites resident on pastures (21). There was no evidence of a periparturient rise in FEC; however, most cows had calved prior to the first sampling period. In contrast to the FEC in the cows, the egg counts in the calves continued to increase as the summer months progressed, which was expected. While the biology of cattle nematodes varies by species, environmental conditions, and host immunity, the increasing FEC in the calves was similar to what has been reported in pastured beef cattle in the province of Quebec (22). Following turn-out to pasture the immunologically naïve calves would have begun ingesting infective L3 larvae, with overwintered larvae typically being the main source of infection (21). The cows would have also contributed to the pasture contamination, with eggs in the newly deposited fecal pats developing into infective larvae. The prepatent period of most GIN during the warm summer months is 28 d and hence there would have been amplification of the parasites over the ensuing summer months. Although a variety of rotational grazing schemes have been devised to decrease parasite populations, grazing management alone is insufficient for the control of GIN (5). This is largely related to the fact that the infective larvae can survive on pasture, even in harsh winter and hot summer conditions. In this instance, had the trial been extended later into the fall and early winter, then the calves’ FEC would have continued 162
to increase until late October to December, at which time most of the ingested larvae would have entered into arrested development versus continuing onto becoming adult worms. Arrested development is a survival mechanism that is triggered when the infective larvae are exposed to inclement weather, hot weather in the southern regions and cold weather in the north. While the fecal egg floatation method is a simple method for monitoring FEC at the herd level (20), FEC are an indirect (and insensitive) measure of parasite infection intensity (23). Therefore caution must be exercised when attempting to correlate egg counts to the number of larvae and adult worms within the gastrointestinal tract; egg counts are influenced by a variety of factors such as season, fecundity of the parasite species, host immunity, and the dilution effects of feces (6,20). Given these caveats, the FEC were broadly similar to what has been reported in cow-calf herds located in the major cattle grazing regions of the northern United States (21,23). Specifically, a recent multicentre study of a long-acting eprinomectin formulation administered to grazing beef cattle showed that there were significant production gains even though the mean FEC of the control groups at the end of the grazing season were relatively low: 4, 8, 17, 21, 19, and 220 epg in Wisconsin, Minnesota, Oregon, Louisiana, Missouri, and Arkansas, respectively (24). The current study was not designed to look at parasite control measures; however, it is noteworthy that all the producers were applying ivermectin in the fall, and only 3 used this product in the spring. While fall application of parasiticides is convenient and optimal for the control of ectoparasites such as grubs (Hypoderma spp.) and lice, this is a suboptimal time for controlling GIN. Ultimately, the goal of all control strategies hinges upon reducing the level of larval populations on pasture (5). This is achieved by the use of strategic deworming programs, wherein anthelmintics are used in combination with grazing management to reduce infection pressures. A common example is the use of the Weybridge system, in which the animals are dewormed and then moved onto clean pastures. However, few pastures are truly clean and hence retreatment or the use of sustained release or long-acting anthelmintics may be required. A number of factors could lead to increased parasitism of grazing beef cattle in western Canada by GIN parasites. Increased herd size and the adoption of intensive rotational grazing systems and low-cost overwintering feeding systems (i.e., swath and bale grazing) translate into higher stocking densities, which contribute to greater pasture contamination and increased infection pressure. Secondly, anthelmintic resistance is well-documented in other regions and presumably this could lead to increased parasite burdens and/or changes in parasite species distribution in western Canada (3,25). And thirdly, climatic changes have been postulated as a causal factor for changing the epidemiology of GIN infections in sheep (4), and a similar scenario could, in time, alter the epidemiology of GIN in western Canada’s grazing beef cattle. Producers have relied on applications of broad-spectrum macrocyclic lactone pour-on products to cows in the fall for many years. However, this is not an evidence-based approach and the work presented herein suggests that parasite control in western Canada is not currently optimal. Unfortunately, the CVJ / VOL 57 / FEBRUARY 2016
Acknowledgments We acknowledge Dr. Janice Berg, Glen Cartwright, and Merck Animal Health (Canada) for both logistical and financial support of this project. We also acknowledge Katrina Barth, Laura Campbell, and Tim Campbell for their assistance in sample collection and preparation. CVJ
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information needed to direct effective and sustainable parasite control in grazing beef cattle in western Canada is lacking, including information on the prevalence, epidemiology, and production impacts of the different parasite species as well as on the extent of anthelmintic resistance and the effectiveness of current control measures. Although there are no published data on ivermectin efficacy on cattle parasites in Canada, a recent study suggests the situation is similar to that described in the US where pour-on formulations are not fully effective in many herds. Fifteen out of 34 beef herds sampled across Alberta and Saskatchewan had less than 85% reduction of fecal egg counts following pour-on ivermectin treatment (Avramenko, Redman, Lewis, Royan, Gilleard: Manuscript in preparation). However, the extent to which this poor efficacy is attributable to ivermectin-resistant parasites is not clear; more research is needed in all these areas.
