Doi:10.1016/j.vetpar.2004.07.025

Veterinary Parasitology 125 (2004) 353–364 Impact of eprinomectin on grazing behaviour and performance in dairy cattle with sub-clinical gastrointestinal nematode infections under aMerial Animal Health Ltd., Sandringham House, P.O. Box 327, Harlow, Essex CM19 5TG, UK bInstitute of Grassland and Environmental Research (IGER), North Wyke, Devon EX20 2SB, UK Received 30 January 2004; received in revised form 13 July 2004; accepted 25 July 2004 Forty spring-calving cows and heifers (20 of each) were allowed to acquire infection with gastrointestinal (GI) nematodes naturally during grazing. The control group (10 cows and 10 heifers)were compared with 20 similar animals treated with eprinomectin in order to evaluate the effect of GInematodes on grazing behaviour, milk production, body condition score and live weight. The animalswere paired according to parity and milk yield during the week prior to treatment, then withinreplicate pair randomly allocated to a different treatment group. The grazing area was sub-dividedinto 20 replicated paddocks of equivalent size and topography. Grazing pairs of either control ortreated animals were randomly assigned to each paddock over the duration of the study (one pair perpaddock).
Grazing behaviour was recorded for both groups over a 10-day period commencing 4 days after treatment with eprinomectin. Milk yield was recorded daily and milk quality was recorded weekly.
Live weight and body condition score were recorded on the day of allocation, the day of initialtreatment and thereafter at weekly intervals until the end of the 4-week trial.
Faecal samples were collected from each animal prior to, and after, allocation and submitted for counts of nematode eggs. Additional faecal samples were taken at the end of the study for culture andnematode identification. Individual faecal samples were also analysed for residual digestibility.
Pasture samples for nematode larval counts were taken at the same time as faecal sampling. Theparasitological results showed low levels of faecal nematode egg output throughout the study, with * Corresponding author. Tel.: +44 1279 775861; fax: +44 1279 775888.
E-mail address: [email protected] (A.B. Forbes).
0304-4017/$ – see front matter # 2004 Elsevier B.V. All rights reserved.
doi:10.1016/j.vetpar.2004.07.025 A.B. Forbes et al. / Veterinary Parasitology 125 (2004) 353–364 the heifers having higher counts than the cows. Faecal culture yielded species of Ostertagia,Cooperia, and Trichostrongylus. Pasture larval levels were very low throughout with no valueexceeding 68 larvae/kg dry matter (DM) of herbage.
There were significant (P < 0.05) effects of treatment on grazing time, eating time, total bites, total grazing jaw movements (TGJM), idling time and mean meal duration. Treated cows and heifersgrazed for 47 and 50 min longer per day, respectively, than controls (P = 0.016). Mean meal durationwas extended as a result of anthelmintic treatment by 11 and 38 min, in cows and heifers, respectively(P = 0.012). There were no significant (P > 0.05) treatment effects on ruminating time or residualfaecal digestibility, but idling time was significantly reduced in both treated cows and heifers, by 50and 110 min, respectively (P = 0.010).
In the treated cattle, there was an increase in solids-corrected milk yield compared with the control cattle, which was significant (P < 0.05) in weeks 2 and 3 after treatment. The response wasparticularly marked in heifers, where the difference in yield between treated and controls was up to2.35 kg/day. The differences in live weight gain and condition score over 28 days post-treatment weresignificant (P < 0.05) in both cows and heifers, in favour of the treated animals.
# 2004 Elsevier B.V. All rights reserved.
Keywords: Cattle-nematoda; Eprinomectin; Grazing behaviour; Performances Reduction in appetite and feed intake are important factors that contribute to reduced performance in ruminants sub-clinically infected with gastrointestinal nematodes ) and has been demonstrated in housed animals infectedartificially with mono-specific cultures of various nematodes (). More recently, research inyoung grazing cattle has shown that a marked reduction in daily grazing time in parasitisedanimals is associated with a reduction in herbage intake and consequent production losses(Dairy cows are known to be infected with, generally, low numbers ofgastrointestinal nematodes (), but havenevertheless frequently shown production responses to anthelmintic treatment (). Recent studies with eprinomectin have shown milk yield responses followingtreatment at various stages of lactation and, additionally, improved fertility has been demonstrated in studies whentreatment was given at calving (). The mechanism underlying suchresponses has not been elucidated, but observations in young dairy heifers () prompted a study into the grazing behaviour of lactating dairy cows and heifersfollowing treatment with eprinomectin.
Forty spring-calving, Holstein–Friesian, dairy cows and heifers (20 of each type), which had calved between 24 February and 14 May 2002, were used in the study, which A.B. Forbes et al. / Veterinary Parasitology 125 (2004) 353–364 commenced in June 2002, when the cattle were between 6 and 17 weeks into lactation.
They had received no anthelmintic treatment the previous grazing season, but the cows hadbeen treated with nitroxynil for liver fluke control at the end of the previous lactation. Theanimals were blocked according to parity (primiparous versus multiparous) and milk yield2 weeks prior to allocation to treatment. Within parity, animals were ranked by milk yield,and paired sequentially: within the replicate pairs so formed individuals were randomlyallocated to a different treatment group (treated or control). The groups were checked toensure no bias in terms of calving date, milk yield or live weight.
Ten replicate pairs, each of two cows or heifers, were allocated to receive either Eprinex1(eprinomectin) pour-on, administered along the mid-line of the back at the rateof 1 ml/10 kg live weight (500 mcg eprinomectin/kg) on 26 June 2002 (treatment group),or no treatment for nematode parasites (control group).
Nematode burdens in the study cattle were derived from infections acquired naturally in previous grazing seasons and from nematode larvae ingested on the designated pasture in2002. Grazing of the pasture was limited during the previous year (2001) because ofrestrictions imposed by Foot and Mouth Disease biosecurity precautions and the pastureswere grazed by dairy cows only from August to late October. During previous grazingseasons, the pasture had been continually grazed with dairy cattle during the summer andby sheep during the winter. The swards had been established for at least 12 years.
The animals were turned out to pasture on 10 May. From turnout to mid-June the animals grazed under a continuous variable stocking system with additional cows beingused as necessary to maintain an overall mean sward surface height (SSH) of 7–8 cm acrossthe experimental area. On 26 June, the grazing area was sub-divided into 20 replicatepaddocks of equivalent size (0.55 ha) and topography. Grazing pairs of either control ortreated animals were randomly assigned to graze each paddock over the duration of thestudy (4 weeks).
Swards, which comprised mainly perennial ryegrass (Lolium perenne L.), received nitrogen fertiliser equivalent to 240 kg N/ha per annum in equal applications at intervals ofapproximately 4 weeks. All animals were maintained on pasture throughout theexperiment. All animals received 4 kg/head/day of 14% crude protein dairy concentrate,with a calculated metabolisable energy concentration of 12.8 MJ kg/DM, in two equalfeeds at milking. Water was available at all times. Animals within each treatment weregrouped together for droving at milking times, and divided into their appropriate grazingpairs for return to their paddocks. The control animals were always handled first to avoidtransfer of eprinomectin ( Following establishment of the SSH between 7 and 8 cm and treatment with eprinomectin, the area of each individual paddock remained unaltered, at 0.55 ha, with 1 Registered trademark of Merial Ltd.
A.B. Forbes et al. / Veterinary Parasitology 125 (2004) 353–364 only the allocated grazing pairs of animals being present in each paddock until the end ofJuly when the study ended.
At weekly intervals from turnout to the day of treatment, between 600 and 650 SSH measurements were taken at random sites across the entire experimental area. On the dayfollowing treatment (27 June) and on 2, 4 and 11 July, SSH was measured at more than 100sites within each paddock.
Samples were taken from freshly deposited faecal pats from each animal on four occasions in May, June and July, prior to allocation and after imposition of treatments.
Faecal sub-samples, each of 4.5 g were analysed for counts of nematode eggs at asensitivity of 50 eggs per gram (epg) using the special modification of the McMastermethod (). Subsequently, faecal samples with counts of less than 50 epgwere further analysed using a technique with a sensitivity of 1 epg, based on the sensitivecentrifugal flotation technique, using saturated salt solution as a flotation medium(Sub-samples of the faeces collected 12 days after treatment werebulked by treatment group (treated or control) for culture and nematode identification.
Pasture samples for direct larval counts were collected from each paddock at the same timeas faecal sampling. The techniques for sampling, larval recovery and larval identificationwere those described in MAFF Reference Book 418, pp. 31–32 (Pasture larval counts were expressed as the number of infective larvae per kilogram ofherbage dry matter (L3 kg/DM). Sub-samples of the 14-day, post-treatment faecal sampleswere also analysed for residual digestibility after the method of Jones and Hayward ().
On three occasions, between 4 and 14 days after treatment, solid-state behaviour recorders (were fitted to each animal to measure grazing andruminating behaviour over 24 h, commencing at 15.00 h. Recordings were analysedusing the software ‘GRAZE’ Total eating time during grazing wascalculated as the sum of the periods of grazing jaw movements (GJM), excludingintervals of jaw inactivity >3 s. Total grazing time (TGT) was the sum of the periods ofGJM activity, including any periods of jaw inactivity <5 min. Periods of jaw inactivitygreater than 5 min were interpreted as being inter-meal intervals The number of meals was calculated as the number of periods of grazing activityseparated by intervals of >5 min. Time spent eating the supplement ration was also easilyidentified from these recordings by the characteristic wave pattern (andmarked as such. Total idling time was calculated as the time within each 24 h, when cowswere not grazing or ruminating, and included time spent drinking and in socialinteraction.
The number of bites and non-biting GJM, the number of ruminative mastications and the total number of jaw movements during consumption of the supplements were countedautomatically. The term ‘non-biting grazing jaw movement’ refers to those jaw movementsnot identified as bites and therefore includes jaw movements which may have a masticativeor manipulative function. Plucked samples, representative of the herbage eaten by theanimals, were collected from each paddock on 7 July and bulked before freeze drying and A.B. Forbes et al. / Veterinary Parasitology 125 (2004) 353–364 subsequent analysis of organic matter (OM) content and OM digestibility Milk yield was recorded daily at each milking. Milk quality was recorded at four consecutive milkings each week starting with the Monday p.m. milking. Solids-correctedmilk (SCM) yields were calculated using the equation of Tyrell and Reid Animals were weighed and their body condition score (BCS) was assessed, using afive-point scale (), 24 h before and on the day of allocation, on theday of treatment and thereafter at weekly intervals until the end of the trial, when liveweight was recorded on two consecutive days.
Mean values were calculated for each grazing pair of animals, which was the experimental unit, over the three measurement days for all variates before statisticalanalysis, because of the lack of independence between animals within each pair All data were analysed by two-way analysis of variance. The mean dailySCM yield during the week before the animals were allocated to grazing pairs was used as acovariate in the analysis of SCM yields as there was a significant (P < 0.05) pre-treatmentdifference in yields from the cows and heifers. Analyses were carried out using GENSTAT4.1 for Windows.
All animals in the study remained in good health throughout the trial and there were no clinical signs of parasitic gastroenteritis in any of the animals.
The overall mean SSH measured across the experimental area on 17 June was 8.19 Æ 0.105 cm. Analysis of variance of the mean SSH on the individual paddocks on 27 June,showed no effects of treatment or parity (mean 7.59 Æ 0.072 cm). Analysis of variance ofthe mean SSH of the individual paddocks on 2, 4 and 11 July, showed differences betweenthe control- and treated-animal paddocks; 7.69 cm versus 7.39 Æ 0.081 cm (P = 0.020),7.65 cm versus 7.43 Æ 0.087 cm (P = 0.087) and 7.66 cm versus 7.34 Æ 0.090 cm (P =0.022), respectively. There were no significant differences between mean SSH of thepastures due to parity (primiparous versus multiparous). The OM content of the bulkedherbage sample collected on 7 July was 902 g/kg dry matter, with an OM digestibility of811 g/kg.
3.2. Faecal egg and pasture larval counts Of the 160 samples taken throughout the study for faecal egg counts, 29 were positive at a sensitivity of 50 epg; eight samples from the cows and 21 from the heifers. Of theremaining 131 samples (<50 epg), 60 had zero values on re-analysis at a sensitivity of A.B. Forbes et al. / Veterinary Parasitology 125 (2004) 353–364 Table 1Effect of treatment with eprinomectin and parity on grazing and ruminating behaviour measured over 24 h S.E. of treatment Significance (P) of effect parity means a Time spent eating between afternoon milking and midnight.
b Total grazing jaw movements.
c 24 h À grazing time À ruminating time.
1 epg; 43 samples from cows and 17 from heifers. Culture of the bulked faecal samplecollected from the control group in July revealed the presence of Ostertagia,Trichostrongylus and Cooperia spp., but very few larvae were recovered. No larvaewere cultured from the faecal sample collected from the group treated with eprinomectin.
Pasture larval counts were very low in all samples, with a range between 0 and 68 larvae/kgDM: Ostertagia and Cooperia species were identified.
Treatment effects on grazing behaviour are shown in . There were significant (P < 0.05) effects of treatment on daily grazing time, eating time, total grazing jawmovements (TGJM), number of bites, idling time and mean meal duration. Treated cowsgrazed for 47 min longer per day than controls, whilst in heifers the comparable figure was50 min (P = 0.016). Mean meal duration was extended as a result of anthelmintic treatmentby 11 and 38 min, in cows and heifers, respectively (P = 0.012). There were no significant A.B. Forbes et al. / Veterinary Parasitology 125 (2004) 353–364 Table 2Effect of treatment with eprinomectin and parity on mean daily solids-corrected milk yield, live weight and bodycondition score (BCS) change S.E. of treatment Significance (P) of effect parity means treatment effects on ruminating time, but treated cows and heifers spent significantly lesstime idling each day: 50 min in cows and 110 min in heifers (P = 0.010).
Cows spent significantly longer grazing and eating and performed more bites per day compared with heifers (P < 0.05). The temporal pattern of grazing meals showed nosignificant difference resulting from treatment or parity, with an overall mean of 6.6 meals/day and 317 Æ 4.9 min of grazing activity occurring between afternoon milking andmidnight. Compared with the cows, heifers demonstrated higher ruminative masticationrates and a greater number of ruminative mastications per bolus (P < 0.01) There was nosignificant effect of treatment or parity on the residual digestibility of the OM in the faeces;mean 252 Æ 6.64 g/kg OM.
Treatment had no significant effect on milk quality. Analysis of the SCM yields, adjusted by covariance for the yield before allocation, showed a significant (P < 0.05)response to eprinomectin treatment in weeks 2 and 3 after administration (Byweek 4, the significance of the treatment response had declined (P = 0.071). SCM yieldswere significantly (P < 0.001) higher for cows compared with heifers in all weeks.
3.5. Live weight and body condition score There was a significant effect of treatment on live weight change over the 28 days following treatment (The differences in total and daily live weight gain over the28-day measurement period between groups were significant (P < 0.037). However, therewas an interaction (P = 0.087) between treatment and parity, with the heifers gaining moreweight as a result of treatment with eprinomectin compared with the cows; equivalent to0.55 versus 0.06 Æ 0.134 kg/day. Analysis of variance of the changes in BCS over 28 daysshowed a significant (P < 0.05) treatment effect, with heifers demonstrating a moremarked effect than cows.
A.B. Forbes et al. / Veterinary Parasitology 125 (2004) 353–364 The faecal egg counts from heifers and cows were very low, consistent with previous results at this site and in the literature (These results confirm therelative insensitivity of the McMaster technique, at the standard sensitivity of 50 epg, indetecting low-level nematode infections in adult dairy cattle. In addition, these data suggestthat dairy heifers’ faeces have a higher concentration of nematode eggs than multiparousdairy cows, presumably reflecting differences in their levels of acquired immunity tonematode parasites. The small number of nematode species present in faecal cultures mustbe considered in the context of the very few larvae recovered, but nevertheless areconsistent with those found previously in dairy cattle on these pastures (). The very low recoveries of pasture larvae probably resulted from the limited grazingperiod during the previous year.
Heifers grazed for less time and performed fewer bites, compared with the cows, as might be expected in relation to live weight, and thus maintenance requirements, and theirslightly lower SCM yields. This was a result of shorter meal duration rather than anyreduction in the number of grazing meals. However, they exhibited higher ruminativemastication rates and more mastications per bolus than the cows, possibly reflecting alower efficiency of particle size reduction per mastication by the younger animals. Nomeans of direct measurement of digestive efficiency were available during the experiment,however, laboratory determination of the residual digestibility was used to examinewhether treatment or parity may have affected digestive efficiency, based on theassumption that there were no significant differences in the digestibility of the herbageselected. The measurements of residual faecal digestibility obtained, showed no significantdifferences in digestive efficiency because of treatment or parity.
Treatment with eprinomectin significantly affected grazing behaviour, manifested by an overall increase of about 1 h in grazing and eating times, and a commensurate increase inthe number of bites. This was achieved by an increase in meal duration rather than an effecton the number of grazing meals. Although treatment with eprinomectin had no affect onruminating time, the number of ruminative mastications or number of boluses, it producedan overall reduction in idling time of 86 min/day (P < 0.001). The lack of any significantdifferences in residual digestibility indicates that, in this study, neither treatment witheprinomectin nor the maturity of the animals significantly affected digestive efficiency.
Despite the treatment and parity effects on grazing time and mean meal duration, there were no significant effects on the number of grazing meals, the temporal patterns of mealsor the total duration of intra-meal intervals, with animals performing an average of 6.6meals each day and conducting just over half of their grazing activity between afternoonmilking and midnight. The increase in total grazing time in the cows treated witheprinomectin was accompanied by a concurrent significant (P = 0.022) reduction of meanSSH in the paddocks occupied by the treated pairs of animals, compared with the controlanimals. This is indicative of a greater herbage intake in treated cattle over themeasurement period.
Under continuous variable stocking management, bite mass and, as a consequence, short-term intake rate (IR) are constrained by sward structure, primarily height. On short A.B. Forbes et al. / Veterinary Parasitology 125 (2004) 353–364 swards, as maintained in this experiment, grazing dairy cattle attempt to overcome suchconstraints on short-term IR by increasing the time they spend grazing (The grazing and eating times recorded in this experiment in the control animalswere similar to those previously recorded with dairy cows grazing swards of 7–8 cm SSHat this time of the year (With these constraints imposed on short-term IRby sward height, any behavioural response by the animals to increase intake as aconsequence of reducing their parasitic burden, would be expected to be manifested in theduration of their grazing activity.
As a result of the increases in grazing activity following treatment, there were significant effects on SCM yield, live weight gain and BCS. These production responseswere more marked in the treated heifers than in the cows, with an SCM yield response up to+2.35 kg/day (over the second and third weeks after treatment) and an improved meandaily live weight change of +0.55 kg/day over the 28-day observation period. Although thechanges in live weight and BCS appear slightly contradictory, in that live weight changeswere generally positive whilst BCS changes were negative (except for the treated heifers)the responses to treatment with eprinomectin are generally in agreement, i.e. an increase inlive weight and BCS of heifers and a minor effect in cows. In this study the control heifersfailed to gain any weight over the 28-day measurement period and this might be consideredunusual, but no explanation for this could be found in the data. It can only be assumed thatthe nutrient intake over this period was insufficient to support significant growth after therequirements for maintenance and lactation had been met.
Previous studies during July have shown that on swards maintained at an overall mean SSH in the range 7–8 cm by continuous variable stocking management,cows are able to achieve mean, short-term OM intake rates of approximately 23 g/min. Ifsuch rates were achieved in the present experiment, control cows would have achieved adaily intake of 13.32 kg OM. Assuming a metabolisable energy (ME) concentration ofapproximately 12.0 MJ/kg herbage DM (), and a daily intake of 44.4 MJ fromthe concentrate ration, the total daily intake would have been approximately 221 MJ ofME. According to with an intake of 210 MJ of ME, cows yielding20 kg milk/day could be expected to produce 0.06 kg milk per MJ increase in ME intake.
The observed increase of 47 min in the time spent eating by the cows, would have resultedin an additional intake of 1.1 kg OM, equivalent to 14.4 MJ ME. Using the model of the predicted increase in daily SCM production would be about 1.0 kg,somewhat greater than the mean increase of 0.34 kg achieved over the 4 weeks followingtreatment with eprinomectin. Although the control and treated cows appeared to gainweight whilst losing BCS, the very small changes in BCS are difficult to interpret over aperiod of only 28 days.
Whilst the intake per bite by the heifers would be expected to be smaller than in the cows, some compensation may have been affected by the slightly higher bite rate.
Nevertheless, the slightly greater increase in eating time by the heifers, as a result oftreatment with eprinomectin, may have allowed them to achieve a similar level of increasein daily intake as the treated cows. Using the same predictive model of the milk yield response would be expected to be in the order of 1 kg/day. However, thisvalue is lower than the mean increase of 1.77 kg recorded in the heifers over the 4 weeksfollowing treatment. Taking into account the significant positive responses in live-weight A.B. Forbes et al. / Veterinary Parasitology 125 (2004) 353–364 and BCS change over the 4 weeks following treatment, it appears that, particularly in theheifers, the responses in grazing behaviour can only partially account for the increase inmilk production and growth rate. A possible explanation of these discrepancies, whichrequires further investigation, is the possible consequence to the animal, in terms of bodyenergy balance, immune responses and alimentary tissue turnover as a result ofgastrointestinal parasitism ( The precise mechanism for the increased appetite in naturally infected cattle following eprinomectin treatment is not known. There are no indications of any directpharmacological effect on feed intake from studies in parasite-free animals treated witheprinomectin or the related compound, ivermectin (Merial, unpublished data).
Additionally, a comparable increase in appetite and feed intake in cattle infected withO. ostertagi has been observed following treatment with fenbendazole, an anthelminticfrom the benzimidazole group, differing in mode of action and pharmacokinetics from theavermectins ().
In a previous study (in which both existing and new infections with parasitic nematodes were controlled to a high degree over the whole 2–3 monthsexperimental period through the use of an ivermectin sustained release bolus, it could notbe determined if the observed increase in appetite was a consequence of short- or long-termparasite control. In the current study, the measurements were made within 2 weeks ofeprinomectin treatment, at which time it can be assumed that the resident populations ofgastrointestinal nematodes had been removed, but re-infection would not have taken placedue to the persistent activity of the product (Thus, it would appear that it is the presence of adult and immature parasites within the hostthat exerts an inhibitory effect on appetite. The rapid reversal of this effect followingtreatment suggests that there may be parasite or host-derived neurochemical mediators thatfeed back peripherally or centrally to effect the observed changes. havepreviously demonstrated such a mediator role for gastrin in the expression of effects onappetite in ostertagiosis in cattle. The speed of response indicates that resolution of macro-or microscopic parasite-induced gut pathology is a less likely explanation for the increasein appetite following anthelmintic treatment.
Regardless of the mechanisms, this study has shown that adult dairy cattle, which typically have high levels of immunity to gastrointestinal nematodes and low parasiteburdens, are still subject to nematode-induced inhibitory effects on appetite. Alleviation ofthese burdens, through eprinomectin treatment, resulted in increased appetite, manifestedas increased grazing time, eating time and number of bites.
Thus, a behavioural mechanism has been demonstrated which explains, in part, the previously reported productivity responses to eprinomectin treatment in lactating dairycows.
This study demonstrated that when adult dairy cattle grazed in a system that allowed unrestricted access to herbage, albeit in swards shorter than would be expected underrotational grazing management, they expressed a behavioural response to removal of A.B. Forbes et al. / Veterinary Parasitology 125 (2004) 353–364 nematode parasites by eprinomectin treatment. This was manifest as an increase in grazingtime and a decline in idling time, similar to that seen previously in young, non-lactatingcattle. These responses resulted in a significant solids-corrected milk yield response in allanimals. In this study, the heifers showed a particularly marked yield response, whichpossibly reflects their relative immaturity and greater susceptibility to gastrointestinalnematodes.
The observed effects of treatment on live weight and conditions score may also be of importance, as the positive responses to treatment would provide a rational explanation forthe improved fertility, which has been reported in some studies with eprinomectin whenadministered to cows and heifers at calving.
The authors wish to thank the dairy staff at North Wyke for milking the cows, Miss Sophie Kerslake for milk sampling, National Milk Records for analysing the milk samples,staff of Analytical Chemistry for conducting the analysis of faecal and herbage samples,Mrs. Wendy Gibb for analysis of the behaviour recordings, M. Cranwell and staff of theVeterinary Laboratories Agency, Addlestone, Surrey for counts of nematode eggs. Thisresearch was funded by Merial Animal Health Ltd. The Institute of Grassland andEnvironmental Research is supported through the Biotechnology and Biological SciencesResearch Council. This research was carried out in accordance with the welfare standardsapproved by IGERs Ethical Review Procedure.
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