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Small Ruminant Research 90 (2010) 165–169

Contents lists available at ScienceDirect

Small Ruminant Research

journa l homepage: www.e lsev ier .com/ locate /smal l rumres

hort communication

nfluence of a Moxidectin treatment in ewes of two German sheepreeds on the growth rate of their lambs

. Moors ∗, M. Gaulyepartment of Animal Science, University of Goettingen, Albrecht-Thaer-Weg 3, 37075 Goettingen, Germany

r t i c l e i n f o

rticle history:eceived 27 June 2008eceived in revised form 8 February 2010ccepted 10 February 2010vailable online 5 March 2010

eywords:nthelmintic treatmentoxidectinrowth rateheep

a b s t r a c t

The aim of the present study was to evaluate the effect of an anthelmintic treatment in ewes(n = 133) of two German sheep breeds (German Black Head Mutton and Leine sheep) on theaverage daily weight gains (ADW) of their lambs (n = 180). Eight weeks prior to the lambingseason ewes were randomly divided into two groups: (1) no anthelmintic treatment, (2)Moxidectin (Cydectin®, Forte Dodge, USA) treatment. Starting at birth, body weights oflambs were recorded every other week until 12 weeks of age. Ewes faecal egg count (FEC)was measured 8 weeks after lambing to monitor the efficiency of anthelmintic treatment.

Log FEC was significantly lower (P < 0.001) in Moxidectin-treated ewes compared toMoxidectin-untreated ewes. German Black Head Mutton tended (P = 0.212) to have higherlog FEC compared to Leine sheep (3.08 ± 0.29 vs. 2.46 ± 0.39). Average daily weight gainswere significantly higher in German Black Head lambs compared to Leine lambs (P < 0.001),and in single born lambs compared to multiples (P < 0.001). Furthermore, in single bornGerman Black Head Mutton lambs average daily weight gains were significantly higher(P < 0.05) in the Moxidectin-treated group compared to single born lambs in the untreatedgroup.

Gastrointestinal nematode infections tended to be less severe in Leine sheep. The

anthelmintic treatment did not influence growth rates of Leine lambs, suggesting a poten-tially higher nematode resistance or tolerance in this breed. In German Black Head Mutton,single born lambs from Moxidectin-treated ewes had higher growth rates compared to sin-gle born lambs from untreated ewes, whereas no differences could be observed between

and uf differ

lambs from treatedbe a consequence o

. Introduction

The number of reared lambs is the most relevant fac-or for an economic sheep production. Higher profit will bebtained by higher growth rates in fattening lambs. How-ver, many factors influence growth rates in lambs such

s breed, sex, birth type, and health status. Furthermore,othering ability, nutrition, udder health and milk produc-

ion of the ewe have an effect on the growth rates in lambsDwyer, 2003; Nowak and Poindron, 2006).

∗ Corresponding author. Tel.: +49 551 395613; fax: +49 551 395587.E-mail address: emoors@gwdg.de (E. Moors).

921-4488/$ – see front matter © 2010 Elsevier B.V. All rights reserved.oi:10.1016/j.smallrumres.2010.02.003

ntreated ewes that had more than one lamb. These findings mayences in intake of milk, concentrate, and hay.

© 2010 Elsevier B.V. All rights reserved.

Infections with gastrointestinal parasites pose high con-straints on sheep production, as they may cause healthproblems such as anaemia, diarrhoea, reduced welfare,weight losses, or even death, due to clinical and subclini-cal infections. Lower growth rates in lambs, and therefore alower profit, are to be expected as a result of decreased milkyield of the ewes. Consequently, parasite infections areassociated with reduced income due to both lower weightgains and costs for anthelmintic treatments and controlling

procedures (Coop et al., 1985; Gauly et al., 2002).

In German sheep production systems the most com-mon endoparasites are Trichostrongylidae (Haemonchus,Ostertagia, Trichostrongylus and Cooperia) and Molineidae(Nematodirus). In addition to gastrointestinal nematodes,

166 E. Moors, M. Gauly / Small Ruminant Research 90 (2010) 165–169

Table 1Number of sheep in the different treatment groups.

Treatment group Ewes Lambs

German Black Head Leine sheep German Black Head Leine sheep

23 46 3622 65 33

45 111 69

Table 2Log FEC (LS-means ± SE) of German Black Head and Leine sheep in thedifferent treatment groups.

Treatment group German Black Head Leine sheep

a a

No treatment 40Moxidectin 48

Total 88

infections with tapeworms or Eimeria sp. are frequentlyfound, mostly in subclinical occurrences (Rehbein et al.,1998; Epe et al., 2004). Although alternative control strate-gies against endoparasite infections, such as breeding forgenetic parasite resistance, were shown to be effective(Bisset and Morris, 1996; Gauly and Erhardt, 2001; Gaulyet al., 2002), anthelmintics have to be applied in mostof the cases. Although the direct effects of anthelminticson treated animals are known, little is known about theindirect effects correlated with the economical outcome.Therefore the aim of the present study was to evaluate,whether an anthelmintic treatment (Moxidectin) of ewesindirectly influences lamb growth rates in two differentGerman sheep breeds.

2. Materials and methods

The present study was conducted at the research farm of the Uni-versity of Goettingen, Relliehausen during the lambing season 2008. Intotal 133 ewes were included in the study: 88 German Black Head Mut-ton (BH) and 45 Leine sheep (LS). Lambs (n = 180) were born betweenJanuary and February 2008. All animals were kept indoors in a barn withspace allowance of 1.5 m2 per ewe and lamb. Lambs had ad libitum accessto hay, water, and a standard concentrate (11.5 MJ ME/kg, 19.5% CP), allprovided in a lamb creep feeder. Ewes had access to a dry grass silageand water ad libitum, and the lactating ewes were additionally fed with astandard concentrate (10.6 MJ ME/kg, 18.0% CP).

In November 2007 ewes of both breeds were randomly divided intotwo groups: (1) untreated control (no anthelmintic treatment), (2) Mox-idectin treatment (Cydectin® , 1 ml/5 kg, Forte Dodge, USA). Starting withthe first treatment immediately after grouping the animals, all treatmentswere repeated throughout the experiment at intervals of 6 weeks. Table 1shows the number of animals in the two treatment groups.

The body weight of lambs was recorded every other week startingat birth until week 12 of life to calculate the average daily weight gain(ADW).

Faeces samples were collected individually from all ewes 8 weeks afterlambing (March to April 2008). Faecal egg count (FEC) was then analysed

using a modified McMaster method (Whitlock, 1948).

Statistical analyses were performed using SAS (SAS Inst. Inc., Cary, NC).For calculating ADW and log EpG (log transformed data to achieve normaldistribution), the following model was used (‘proc glm’):

Yijkl = � + Gi + Bj + Tk + Gi × Bj + eijkl

Table 3Average daily weight gain (ADW) in lambs at weeks 4, 8 and 12 post natum (LS-m

ADW week 4 (g)

Breeda

BH 280.1 ± 8.51 aLE 212.6 ± 9.40 b

Birth typeSingle 288.7 ± 11.4 aMultiple 204.0 ± 7.69 b

LS-means in a column with no common letters (a and b) differ significantly withia BH = German Black Head Mutton, LE = Leine sheep.

No treatment 5.41 ± 0.44 4.41 ± 0.54Moxidectin 0.75 ± 0.38b 0.52 ± 0.55b

LS-means in a column with no common superscript letters (a and b) differsignificantly (P < 0.001).

where Yijkl is the lth observation, � is the overall mean, Gi is the fixed effectof treatment (1 = no treatment, 2 = Moxidectin treatment), Bj is the fixedeffect of breed (BH, LS), Tk is the fixed effect of birth type (single, multiple)and Gi × Bj is the interaction between group and breed. For analysing thelamb data, sex (female, male) was incorporated as a fixed effect and birthweight as a covariate.

Growth rates of lambs were calculated with ‘proc nlin’ using the fol-lowing model:

Yt = a + bt + ct2

where Yt is the BW at day t, t is the day post natum, and a, b and c are theparameters estimated.

3. Results

Log FEC of the ewes in the two different treatmentgroups are shown in Table 2. Within the breeds, log FECdiffered significantly (P < 0.001) between the treated anduntreated animals. No significant difference (P = 0.212) wasfound in log FEC between the two breeds German Black-head Mutton (3.08 ± 0.29) and Leine sheep (2.46 ± 0.39).

Ewes with multiple born lambs had significantly higherlog FEC than ewes with single born lambs (3.31 ± 0.34 vs.2.23 ± 0.34; P = 0.023).

ADW of lambs until week 4, week 8 and week 12 weresignificantly affected by breed (P < 0.001) and birth type(P < 0.001; Table 3), however the interaction between breed

and birth type was not significant (P > 0.05).

Male lambs tended to have higher ADW com-pared to female lambs until week 8 (250.2 ± 6.19 g vs.243.0 ± 6.17 g; P = 0.395) and week 12 of age (244.1 ± 6.98 gvs. 232.0 ± 6.85 g; P = 0.199). Birth weight as a covariate

eans ± SE).

ADW week 8 (g) ADW week 12 (g)

272.7 ± 5.37 a 271.4 ± 6.11 a220.5 ± 7.22 b 204.7 ± 7.91 b

274.3 ± 7.42 a 259.2 ± 8.50 a218.8 ± 5.78 b 216.9 ± 6.19 b

n breed and birth type (P < 0.001).

E. Moors, M. Gauly / Small Ruminant Research 90 (2010) 165–169 167

F Germam ep multg d on thea to the d

hat

fwmatGwstfiot

4

a–efeT

ig. 1. (a–d) Body weight (BW, kg) of lambs by breed and birth type; (a)ultiple born lambs, (c) Leine sheep single born lambs and (d) Leine she

roup (+) and curve no. 2 (—) the treatment group (�). The curves are basend a, b and c are the parameters estimated. All curves fitted significantly

ad a significant impact on ADW until week 8 (P = 0.003)nd week 12 (P = 0.025), whereas the interaction betweenreatment group and breed was not significant (P > 0.05).

Fig. 1 shows the development of body weight in lambsrom birth until week 12 of age. The development of bodyeight was similar in treated and untreated groups, inultiple born German Black Head Mutton lambs (Fig. 1b),

s well as in Leine lambs (Fig. 1d). Differences betweenhe two treatment groups were apparent in single bornerman Black Head Mutton lambs (Fig. 1a). Lambs’ bodyeight development in the anthelmintic treatment group

howed an increase, whereas body weights in the non-reated group levelled off from day 40 of age. The bestt between measured and predicted body weights wasbtained for German Black Head Mutton lambs in the non-reated group (R2 = 0.92).

. Discussion

Ewes treated against gastrointestinal nematodes had –s expected in the absence of no anthelmintic resistance

significantly lower FEC compared to the non-treatedwes (1633.8 ± 306.8 vs. 181.2 ± 294.5 eggs per gramaeces). Applying Moxidectin orally is described as anffective anthelmintic even against Ivermectin-resistantrichostrongylus colubriformis (Gopal et al., 2001). Although,

n Black Head Mutton single born lambs, (b) German Black Head Muttoniple born lambs. In all figures curve no. 1 (- - -) indicates the non-treated

model Yt = a + bt + ct2, where Yt is the BW at day t, t is the day post natum,ata (P < 0.001).

sheep in the present study were naturally infected with dif-ferent nematodes species (74% Trichostrongylus spp., 19%Haemonchus contortus, 7% Ostertagia spp.), Moxidectin nev-ertheless seemed to be effective.

Differences in FEC between sheep breeds have beenalready described (Barger, 1989; Bisset and Morris, 1996;Woolaston and Baker, 1996; Gauly and Erhardt, 2001; Goodet al., 2006). However, in the present study no signifi-cant differences (P > 0.05) were found in log FEC betweenthe mutton breed German Blackhead and the landracebreed Leine sheep. In tendency German Blackheads hadhigher FEC in comparison to Leine sheep (1245.9 ± 258.6vs. 569.1 ± 340.1). Other studies described sheep breedsthat were developed under more extensive low-input con-ditions, which are potentially more resistant to variousdiseases (Kraus et al., 1998; Gauly and Erhardt, 2001). TheLeine sheep is known to be a robust and frugal landracebreed. According to the lower FEC this breed seems to bepotentially more resistant against infections with gastroin-testinal nematodes as compared to German Blackheads, abreed that is mainly kept in intensive management sys-

tems. Breed differences in FEC are mostly interpreted asdifferences observed in worm burden, which means thatbreed differences are under genetic control (Good et al.,2006). Since other effects influencing parasite infectionssuch as husbandry system, grazing management, and feed-

minant

168 E. Moors, M. Gauly / Small Ru

ing regimen can be excluded in the present study (all sheepwere kept together under the same conditions), there is ahigh probability that the indicated breed differences aredue to genetic differences. However, to prove this, a highernumber of animals have to be investigated.

In the present study ewes with multiple born lambshad significantly higher log FEC than ewes with single bornlambs. These findings are in agreement with previous stud-ies (Woolaston, 1992; Bishop and Stear, 2001): the numberof lambs reared and suckled significantly influenced theewes’ faecal egg counts, such that an increasing reproduc-tive burden led to higher FEC counts. Endocrinal statusduring lactation leads to a decrease of immunity and subse-quently to the ‘periparturient rise’ (O’Sullivan and Donald,1970). Also the requirement and availability of proteinsseem to play an important role in the formation of the ‘peri-parturient rise’ (Houdijk et al., 2003). It cannot be ruled outthat some of the ewes in the present study got less concen-trate than others, because it was offered to the lactatingewes once a day in open troughs. However, the peripar-turient increase in FEC is described for sheep at weeks 4–6prior until 6–8 weeks after parturition (Barger, 1993), andthe date of faeces sampling in the present study was withinthis period. Therefore the significantly higher FEC values inthe ewes with multiples may be described as an effect ofthe ‘periparturient rise’.

As expected, lambs of the mutton breed German Black-head had significantly higher daily weight gains comparedto the Leine lambs until weeks 4, 8 and 12 of age(P < 0.001). The breed German Black Head Mutton wasdeveloped about 200 years ago from crosses betweenBritish blackheaded meat breeds (i.e. Leicester, Southdownand Hampshire) and German local breeds (Mason, 1996).The breeding goal including high growth rates and goodcarcass quality contributes to this breed being one of themost favourite meat breeds in Germany. The Leine sheepis a robust landrace breed of medium size, with generallylower daily weight gains compared to mutton breeds. Dif-ferences in the average daily weight gains of 67 g/day (week4), 52 g/day (week 8), and 66 g/day (week 12) betweenthe two breeds were therefore within the expectedrange.

Sex differences in average daily weight gains havealready been described (Wylie et al., 1997), however, inthe present study no significant differences (P > 0.05) wereobserved between male and female lambs. Male lambs onlytended to have higher daily weight gains until weeks 8 and12 of age, but the small differences of 7 and 12 g/day hadno physiological relevance.

Also birth type significantly influenced the average dailyweight gains of lambs until weeks 4, 8 and 12 of age(P < 0.001). Single born lambs had higher daily weight gainscompared to multiple born lambs. Snowder and Glimp(1991) showed an increased total milk yield up to 61% inewes of suckling twins compared to ewes with single bornlambs. These findings also apply to the colostrum. It is gen-

erally known, that colostrum and milk yield in ewes withtwins is higher than in ewes with single lambs, howeverthe intake per lamb is lower in twins (McNeill et al., 1988;Hall et al., 1990). Therefore, a lower milk intake in multi-ple born lambs causes lower daily weight gains compared

Research 90 (2010) 165–169

to single born lambs. This was also found in the presentstudy.

Since birth type had a significant effect on the averagedaily weight gains of the lambs, development of weightin the two anthelmintic treatment groups were analysedseparately.

When offering different levels of dietary protein to lac-tating ewes, Houdijk et al. (2003) observed that the firstincrements of dietary metabolisable protein resulted inan increased milk production. At the time when higherincrements of protein were offered and the maximum milkproduction was obtained, a reduced worm burden could beobserved. These findings imply that in lactating ewes milkproduction takes a higher priority than reduction of wormburden. It is suggested that with a normal protein rationand high milk production, ewes have a lower margin forparasite control. In the present study, differences of thedevelopment of lambs’ body weights were found in singleborn German Blackheads between lambs from treated anduntreated ewes. While body weights in the treated groupincreased slightly, body weights in the untreated groupdecreased up to day 40 of age (Fig. 1). The peak of milkproduction in sheep is between days 20 and 30 of lacta-tion (Cardellino and Benson, 2002). It is assumed that fornew born lambs the unique source of food is colostrum andmilk, therefore no differences in the growth rates of lambsappear in the first weeks of life. Because of the limitedsource of milk for twins, they probably start earlier with theintake of concentrate and hay compared to single lambs.Therefore the growth rate of twins is less closely associ-ated with milk production than in single lambs (Snowderand Glimp, 1991). According to that, an anthelmintic treat-ment of ewes does influence the growth rate via the milkintake more directly in single lambs. In the present study,differences in the development of body weights betweensingles and multiples appear approximately from day 40.The parasite treatment resulted in a lower faecal egg out-put and possibly in an increased milk yield, which however,did not translate into higher growth rates in multipleborn lambs. Further investigations are required to deter-mine whether there are in fact differences in milk yieldbetween treated and untreated ewes. No apparent differ-ences in the development of body weight from birth untilweek 12 of age could be detected between the treated anduntreated single or multiple born Leine lambs. Because gas-trointestinal nematode infections were at a lower level inthe Leine sheep compared to the German Blackheads, itseems that anthelmintic treatment of Leine ewes had noeffect on lambs’ growth rate. The reason could possibly bea higher genetic resistance or tolerance against gastroin-testinal nematodes in Leine sheep.

When dealing with the economic viability of lamb pro-duction, costs for the production chain and the costs foranthelmintic treatments need to be considered. In thepresent study, body weights of single born Blackhead Mut-ton lambs at the age of 12 weeks were on average 9%

higher in the treatment group compared to single bornlambs from ewes of the control group. Assuming a priceof 4.00D /kg lamb carcass (ZMP, 2007) and an average car-cass weight of 12 kg/lamb at the age of 12 weeks, the profitper lamb would be 4.32D . However, there are costs for

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he anthelmintic treatment of approximately 0.90D /ewe14 ml Moxidectin/70 kg ewe). Considering these calcula-ions, a profit of 3.42D per single born lamb seems to beossible by treating ewes against gastrointestinal nema-odes. Assuming a proportion of 50% single born lambs, itan still be profitable to treat all ewes before the lamb-ng season. However, labour input for the application ofnthelmintics is not included in these calculations. Anothermportant aspect is the situation of worldwide increasingnthelmintic resistances in sheep (Waller, 1997; Hertzbergnd Bauer, 2000; Sutherland et al., 2008). Therefore, annrestricted anthelmintic treatment only for the sake ofbetter economic outcome cannot be recommended.

. Conclusion

Gastrointestinal nematodes tended to be lower in Leineheep and the anthelmintic treatment did not influencerowth rates of Leine lambs, suggesting a potentially higherematode resistance or tolerance in this breed. In Ger-an Blackheads, single born lambs of anthelmintic-treated

wes had higher growth rates compared to single lambsrom untreated ewes. However, no differences could beound between lambs from treated and untreated ewes thatad more than one lamb. The reason for this could be theossible differences in the intake of milk, concentrate anday between single born lambs and twins/triplets. Further-ore, a higher worm burden of ewes may show a more

bvious effect on the growth rates of lambs.

cknowledgements

The authors would like to thank K. Salzmann and thetaff of the research farm Relliehausen of the University ofoettingen for their technical support.

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