research article effect of moxidectin treatment at...

Research ArticleEffect of Moxidectin Treatment at Peripartum onGastrointestinal Parasite Infections in Ewes Raised underTropical Andes High Altitude Conditions

J J Vargas-Duarte12 H Lozano-Maacuterquez23

H A Grajales-Lombana3 C Manrique-Perdomo3 D A Martiacutenez-Bello4

C Saegerman5 M Raes2 and N Kirschvink2

1Genetic Institute National University of Colombia Carrera 30 No 45-03 Edificio 426 Bogota DC Colombia2Unit of Integrated Veterinary Research Department of Veterinary Medicine University of Namur rue de Bruxelles 615000 Namur Belgium3Faculty of Veterinary Medicine and Animal Science National University of Colombia Carrera 30 No 45-03Edificio 481 Bogota DC Colombia4Faculty of Veterinary Medicine Cooperative University of Colombia Calle 30 No 33-51 Bucaramanga Colombia5Research Unit of Epidemiology and Risk Analysis Applied to Veterinary Sciences (UREAR)Fundamental and Applied Research for Animal and Health (FARAH) University of Liege boulevard de Colonster 204000 Liege Belgium

Correspondence should be addressed to J J Vargas-Duarte jjvargasdunaleduco

Received 19 January 2015 Revised 15 April 2015 Accepted 22 April 2015

Academic Editor Guillermo Virkel

Copyright copy 2015 J J Vargas-Duarte et al This is an open access article distributed under the Creative Commons AttributionLicense which permits unrestricted use distribution and reproduction in any medium provided the original work is properlycited

This study tested the impact of moxidectin at peripartum on nematode fecal egg count (FEC) and clinical parameters on ewes inthe high altitude tropical Andes of Colombia FEC and clinical evaluations were performed on 9 occasions in 43 naturally infectedewes before and during gestation and after lambing Moxidectin (Mox 200 120583g kgminus1) was applied at late pregnancy (T

1

119899 = 15) or48 hours after parturition (T

2

119899 = 14) 14 untreated ewes served as controls (C) Suckling lambs (119899 = 58) remained untreated andunderwent four clinical and parasitological evaluations until 8 weeks after birth Mox efficacy equaled 993 (T

1

) and 969 (T2

)Highest mean FEC value reflecting periparturient nematode egg rise (PPER) was recorded in C ewes at 4ndash6 weeks after lambingSignificant FEC reductions were found in T

1

(948) and T2

(967) ewes (119901 lt 005) All lambs showed a significant and ewes-group independent increase in FEC before weaning (119901 lt 005) Clinical parameters (anemia and diarrhea) showed time- andtreatment-related differences (119901 lt 005) Monitoring of FEC and clinical parameters linked to gastrointestinal parasite infectionsallowed demonstrating that postpartumor preweaning are two critical periods to nematode infection for sheep raised under tropicalAndes high altitude conditions Use of Mox as anthelmintic treatment prevented PPER

1 Introduction

Sheep parasites belong to the main constraints that reducesustainability of wool milk and meat production worldwide[1ndash3] To prevent parasite dissemination in small ruminantflocks assessment of the magnitude of gastrointestinal para-site burdens in different productive categories is required [45] Indeed lambs have been described as themost susceptible

category to gastrointestinal parasites and it is assumed thatadult animals can deal with parasite infection and minimizeits pathogenic activity [5 6] However it has been shown thatperiparturient ewes are highly susceptible to gastrointestinalnematode infections and are the largest contributors topasture contamination with nematode eggs [7 8]

In mature ewes a transient loss of immunity to gas-trointestinal nematodes begins around lambing time and

Hindawi Publishing CorporationVeterinary Medicine InternationalVolume 2015 Article ID 932080 8 pageshttpdxdoiorg1011552015932080

2 Veterinary Medicine International

continues for several weeks after parturition This impairedresistance is associated with an increase in strongylid fecalegg count (FEC) commonly referred to as the periparturientnematode egg rise (PPER) [5 9ndash14] PPER has been des-cribedmainly in sheep breeds exploited in temperate regionsIndeed the flocksrsquo seasonal management allows the springcontamination of pasture with nematode eggs shed by lac-tating ewes and the concomitant infection of lambs with theinfective larvae hatched from those eggs [15 16] Althoughwell known the exact cause of PPER remains poorly under-stood Increased FEC has been also associated with variationsin hormonal profiles at peripartum (prolactin and cortisollevels) and low levels of metabolisable protein intake duringlate pregnancy and lactation [13 17ndash21]

In tropical regions of South America sheep productionis based on extensive grazing with limited managementand sanitary practices which leads to increased mortalityrates and reduced productivity due to gastrointestinal ne-matodes [22ndash24] Under these conditions the importanceof a PPER and its epidemiological consequences in smallruminants remain to be established [7 25ndash28] On the onehand infective larvae may be continuously available in thetropics and reproductive cycles and lambing are not strictlyseasonal events as in temperate countries Indeed in Colom-bian flocks lambing might occur during the entire yearbut two main annual periods of births during AprilndashJuneand November-December at the end of rainy periods aredescribed [29] On the other hand physiopathological con-sequences of PPER in lactating ewes and their offspringare believed to be important in the tropics because theinfectious pressure persists at a high level and because nutri-tional management is often heterogeneous [24 26 30 31]Consequently environmental parameters reproductive cyclefeatures and feeding management practices are fundamentaltools for rational anthelmintic treatment [3 4 32] In order tominimize nematode egg outputs and to regulate pasture con-tamination with infective third larval stages in tropical sheepproduction systems strategic treatment of highly infectedanimal groups as periparturient ewes is recommended [28 33 34]

Among the available chemical groups used to control gas-trointestinal nematodes in sheep macrocyclic lactones rep-resent the cornerstone of current anthelmintic drug control[35] Moxidectin (Mox) a macrocyclic lactone of the chemi-cal family of milbemycins has been widely used during thelast 30 years [36] However the intensive use of this broad-spectrum antiparasitic compound could lead to the emer-gence of resistance in gastrointestinal nematodes [35 36]This situation has encouraged the search for treatment strate-gies to optimize Mox potential avoiding unnecessary treat-ments particularly in geographic areas where Mox use isnot a frequent practice and resistance is not yet fully present[36 37]

The present study hypothesized (1) that PPER occursin Colombian sheep raised under Andean high altitudetropical conditions during the period of the highest lamb-ing rate (AprilndashJune) (2) that Mox is still an effectiveanthelmintic molecule at tropical Andes and (3) thatMox strategic treatment of ewes administered either at

late pregnancy or early peripartum period would preventPPER

2 Materials and Methods

The study was conducted at the Center for Sheep ResearchTechnological Development and Extension of the NationalUniversity of Colombia located inMosquera-Cundinamarca(4∘4010158405710158401015840N 74∘1210158405010158401015840W)at 2510m above sea levelThemeantemperature during the study period was 135∘C and themonthly average rainfall 86mm The protocols employedfollowed the national guidelines for care and use of animals(Colombian Law 891989) and were approved by the EthicalCommittee of the Faculty of VeterinaryMedicine andAnimalScience of National University of Colombia (CB-035-2013)

21 Animals This study enrolled 43 healthy wool ewes offour breeds (Colombian creole Romney Marsh Hampshireand Corriedale) Ewes were grazing together in Loliumperenne and Pennisetum clandestinum pastures and weresupplemented with concentrate feed hay and mineralizedsalt according to physiological requirements Fresh drinkingwater was available ad libitum Ewesrsquo clinical and para-sitological follow-up was performed during one completereproductive cycle (dry period mating period pregnancyperiod and postpartum period) Since birth lambs (119899 = 58)were keptwith their dams andunderwent the same follow-up

22 Experimental Design A longitudinal study was con-ducted during 40 weeks and included nine sampling periodswhere parasitological and clinical evaluations were per-formed in relation to ewersquos reproductive state (Figure 1)The last anthelmintic treatment was applied more than fourweeks before the beginning of the follow-up (fenbendazole10mgsdotkgminus1 once daily during three days) Ewes were investi-gated before breeding around mating (natural reproductionwith a mating period of 34 days) at midpregnancy (sim80 daysof pregnancy) at late pregnancy (7ndash29 days before lambing)at immediate peripartum (6 days before until 2 days afterlambing) at early postpartum (2ndash15 days after lambing) atintermediate postpartum (15ndash30 days after lambing) at latepostpartum (30ndash45 days after lambing) and at prewean-ing (46ndash60 days after lambing) Lambs were investigatedsince birth at the same time points as their dams At latepregnancy ewes were ranked on the basis of body weightbody score and parasite infection burden and allocated intothree groups Ewes of group 119879

1

(119899 = 15) received a singleMox (Cydectin Fort Dodge Animal Health) subcutaneousinjection of 200 120583g kgminus1 of body weight at late pregnancy(sim135 days of gestation) Ewes of group 119879

2

(119899 = 14) receiveda single Mox subcutaneous injection of 200 120583g kgminus1 bodyweight 2 days after lambing Control ewes (C group 119899 = 14)remained untreated throughout the whole study Five furtherfortnightly samplings were performed after lambing

23 Clinical and Zootechnical Parameters The animals weremonitored daily during the entire course of the exper-iment Development of clinical signs related to parasite

Veterinary Medicine International 3

D M MP

TT1

TT2

Lambing

Parasitological and clinical evaluationbefore and during pregnancy

Fortnightly parasitologicaland clinical evaluation during

peripartum and lactation

LP IPr EPp IPp LPp PW

PPERPre PWPer

T1 ewesn = 14

n = 14

n = 14

C ewes

T2 ewes

Lambsn = 58

PEMoxT1

PEMoxT2

Figure 1 Experimental design to describe periparturient nematode egg rise (PPER) of ewes naturally infectedwith gastrointestinal nematodesand to measure the efficacy and persistency of peripartum strategic treatment with moxidectin (Mox) either at the onset of late pregnancy(TT1

) or at the end of immediate peripartum (TT2

) period under tropical Andes high altitude conditions Parasitological and clinicalevaluations included FEC byMcMaster test anemia detection by FAMACHAcopy system diarrhea assessment byDag scoring bodyweight andbody condition assessment Fecal egg count reduction (FECR) was employed to test posttreatment moxidectin efficacy 15 days after treatment(PEMox1198791 and PEMox1198792 ) the prevention of PPER at late postpartum (PPERPre) period and preweaning persistency (PWPer) Ewes in controlgroup (C) and offspring of all ewes were untreated against gastrointestinal nematodes D dry ewes M mating MP midpregnancy LP latepregnancy Ipr immediate postpartum Epp early postpartum Ipp intermediate postpartum LPp late postpartum and PW preweaning

infections (depression ataxia andor submandibular edema)was monitored Body weight and body condition wererecorded monthly Except for dry period scores of anemia(FAMACHAcopy) and diarrhea (Dag score) were measured ateach sampling period according to Broughan and Wall [38]Di Loria et al [39] and Macarthur et al [21] recommenda-tions

24 Parasitological Follow-Up Parasite burden determina-tion was performed by fecal sampling in all ewes at the 9established periods and in lambs at four occasions FEC wereobtained by the modified McMaster test according to themethodology described by Henriksen and Christensen [40]with a minimum detection level of 50 eggs per gram of fecesIn cases of parasite burdens higher than 4000 strongylid eggsper gram and associated clinical signs of nematode infection(FAMACHAcopy level ge4 or elevated Dag score) C ewes andorthe untreated lambs were selectively treated and withdrawnAdditionally lambs whose fecal oocyst count was higherthan 4000 Eimeria oocysts per gram of feces received anoral toltrazuril anticoccidial treatment (Coccicalf CaliforniaCompany SA 20mg kgminus1 of body weight)

25 Statistical Analysis To estimate FEC reduction (FECR)induced by treatments the equations recommended by Dob-son et al [41] were employed to calculate the following

(1) Mox Posttreatment Efficacies Consider PEMox = 100times[1minus(11987911989415

1198791198940

) times (1198620

11986215

)] where 1198791198940

and 11987911989415

are the arithmetic

means of pretreatment and 15-day posttreatment FEC oftreated groups (119879

1

or 1198792

) and 1198620

and 11986215

are the arithmeticmeans of C group at the corresponding sampling times Moxresistance was suspected when posttreatment FECR was lessthan 95 and resistance was declared when the upper 95confidence interval of the percentage reduction was less than95 [42]

(2) PPER Prevention Induced by Mox Treatments ConsiderPPERPre = 100 times [1 minus (119879119894LPp119862LPp)] where 119879119894LPp and 119862LPpare late postpartum arithmetic means of FEC in treated (119879

1

and 1198792

) and C groups respectively

(3) Preweaning Mox Treatments Persistency ConsiderPWPer = 100 times [1 minus (119879119894PW119862PW)] where 119879119894PW and 119862PW arepreweaning arithmetic means of FEC in treated (119879

1

and 1198792

)and C groups respectively

Resampling-bootstrap method was employed to provide95 confidence intervals for anthelmintic efficacies [41]The package ldquoeggCountsrdquo in R software version 310 wasemployed [43]

Statistical analysis of data was conducted employing atwo-factor ANOVA with repeated measures on one factor inorder to evaluate the effect of both treatment and samplingtime on FEC and clinical parameters If necessary logarith-mic transformation was performed in order to achieve anormal data distribution Clinical variables as FAMACHAcopyDag score and body condition were discriminated into cat-egories and presented as median (minimum and maximum


0100020003000400050006000700080009000

10000

Dry

Mat

ing

Preg

nanc

y

Late

pr

egna

ncy

Imm

edia

te

perip

artu

m

Early

po

stpar

tum

Inte

rmed

iate

postp

artu

m

Late

po

stpar

tum

Prew

eani

ng

C ewes

a a

b b

PPER

b b

Mea

n va

lues

of Stro

ngylid

eggs

per g

ram

of f

eces

(epg

)

T2 ewesT1 ewes

(a) Fecal sampling periods for adult ewes during one reproductive cycle

0

1000

2000

3000

4000

5000

6000

7000

8000

9000

10000

Part

uriti

on

Early

postp

artu

m

Inte

rmed

iate

postp

artu

m

Late

postp

artu

m

Prew

eani

ng

C lambs

a

b

Mea

n va

lues

of Stro

ngylid

eggs

per g

ram

of f

eces

(epg

)

T2 lambsT1 lambs

(b) Fecal sampling periods for lambs after lambing

Figure 2 Mean gastrointestinal parasite burdens (plusmn standard error of mean) registered during one complete reproductive cycle in ewes andtheir offspring (a) shows the peak in FEC at late pregnancy in C ewes (PPER) and the significant (b) and sustained FECR induced by 119879

1

and1198792

peripartum strategic treatment with moxidectin (two-factor ANOVA 119901 lt 005) preventing the PPER (PPERPre) (b) shows the significantincrease in FEC at preweaning (b) in ewesrsquo offspring (two-factor ANOVA 119901 lt 005) Adult ewes 119899 = 43 (14 C 15 119879

1

and 14 1198792

) Sucklinglambs 119899 = 58 lambs (18 born from C ewes 20 from 119879

1

ewes and 20 from 1198792

ewes)

values) A ratio change for each clinical and zootechnicalvariable was calculated by dividing the median values beforetreatment (dry mating midpregnancy and late pregnancy)over the median after treatment (early intermediate lateand preweaning period) Group effect on ratio changes wasassessed by one-factor ANOVA and Tukey tests 119901 values lessthan 005 (119901 lt 005) were considered significant Statisticalanalysis was performed using the software SPSS Statistics210

3 Results

An effect of treatment and sampling time on FEC wasestablished (119901 lt 005) Mean FEC from ewes before andduring mating period were significantly lower than thoseregistered during pregnancy and lactation in C ewes PPERoccurred in C ewes at late postpartumperiod 4ndash6weeks afterlambing and induced a significant increase in FEC (119901 lt 005)(Figure 2(a))

PeripartumMox treatment in1198791

and1198792

ewes significantlyreduced FEC 15 days after treatment and efficiently preventedPPER (119901 lt 005) No differences between 119879

1

and 1198792

mean forFEC after treatment were observed FEC remained low untilpreweaning period in both groups

Significant differences by treatment and sampling timewere recorded for clinical parameters (119901 lt 005) Mox treat-ment applied to group 119879

1

prevented increase in FAMACHAvalues after lambing as observed in C and119879

2

groups (Table 2)No major changes were found for body weight and bodycondition scores

A significant increase in FEC occurred to lambs atpreweaning period (Figure 2(b)) twoweeks after FECpeak incontrol ewes (119901 lt 005) Although no significant differencesamong preweaning FEC were observed between lambs bornto C 119879

1

or 1198792

ewes (119901 lt 005) untreated control ewesoffspring showed a sharper increase in FEC (Figure 2(b))and required treatment Lambsrsquo clinical parameters did notshow significant differences over time or in function of ewesrsquotreatment group (data not shown)

4 Discussion

The present study evaluated under field conditions the mag-nitude of PPER of gastrointestinal nematodes in Colombianwool sheep and tested the efficacy of Mox and its impact ontwo periparturient treatment schemes in ewes at lambing atthe period of the highest birth rate in Andean flocks PPERand treatment efficiency and persistency were evaluated in


Table 1 FECR induced by moxidectin strategic treatment of periparturient ewes during the same reproductive cycle

Time of treatment Evaluated period

Mean FEC plusmn SEM Efficacy of treatmentUntreated

control ewes119899 = 11

lowast

Treated ewes1198991198791= 15 and1198991198792= 14

FECR 95 CI

Before lambing (1198791

)

Before treatment 1705 plusmn 537 1060 plusmn 314 mdash mdash15 days after treatment (PEMox)

lowastlowast 745 plusmn 351 3 plusmn 3 993 97ndash100Late postpartum (PPERPre)

lowastlowast 4168 plusmn 1417 217 plusmn 172 948 662ndash996Preweaning (PWPer)

lowastlowast 2582 plusmn 1205 123 plusmn 59 952 794ndash989

48 h after lambing (1198792

)


lowastlowast 1205 plusmn 316 27 plusmn 18 961 891ndash100Late postpartum (PPRPre)



1

late pregnancy treated group 1198792

48 hours postlambing treated group PEMox posttreatment efficacy induced by moxidectin PPERPre PPER preventioninduced by moxidectin PWPer preweaning moxidectin persistency FEC fecal egg count SEM standard error of mean FECR fecal egg count reduction95 CI 95 confidence intervals lowastThree C ewes with high FEC and associated clinical signs were excluded after intermediate postpartum period due to Moxtreatment by ethical considerations and their data were not included in the analysis lowastlowastSignificant effect of treatments (one-way ANOVA and Tukey tests119901 lt 005) in FEC by evaluated period

Table 2 Treatment-induced differences in the median of ratio change of clinical (FAMACHAcopy and Dag score) and zootechnical (bodyweight and body condition) parameters

Measured parameters

Median (minndashmax)

Untreatedcontrol group119899 = 11

lowast

Late pregnancyMox injection119899 = 15

48 hourspostlambingMox injection119899 = 14

Change ratioFAMACHAlowastlowast 073 (05ndash1)a 1 (067ndash125)b 067 (067ndash1)a

Dag scorelowastlowast 175 (05ndash2)a 1 (067ndash3)b 116 (067ndash2)ab

Body weight 119 (106ndash128) 116 (102ndash14) 119 (105ndash142)Body condition 104 (082ndash103) 1 (07ndash12) 1 (067ndash13)

Data were calculated by dividing the median of the parameter values before treatment (dry mating midpregnancy and late pregnancy) over its median aftertreatment (early intermediate late and preweaning period) Min minimum value max maximum value FAMACHAcopy values (1ndash5) Dag score values (0ndash5) body condition values (1ndash5) lowastThree C ewes with high FEC and associated clinical signs were excluded after intermediate postpartum period due to Moxtreatment lowastlowastSignificant differences between treatments (one-wayANOVA119901 gt 005) Treatment differences (Tukey test119901 gt 005) are denoted by superscripts

terms of FEC as well as in terms of clinical (anemia anddiarrhea score) and zootechnical (weight body condition)performances

The study was conducted under field conditions withnaturally infected ewes As the animals belonged to theSheep Research Center of National University in Bogota theyhad been selected among a larger group in order to allowan optimal standardization of the study conditions and theinvestigation of a reduced number of animals (14-15 ewesper group) Local (Creole) or well adapted breeds (RomneyMarsh Hampshire and Corriedale) were kept on typicalColombian altitude pastures If keeping all animal groups(1198791

1198792

and C) on the same pasture allowed an optimalstandardization of the infectious third larvae pressure it alsodiminished the effect of the treatments that were testedIndeed in spite of the high efficacy and persistence of Moxstrategic treatment it is likely that FECR observed in eweswould have been even better if separated pastures would havebeen used after treatment It might also be assumed that the

lack of zootechnical impact (body weight and body conditionscore) of the treatments was at least partially due to stan-dardization of the infectious pressure Keeping the animals onseparated pastureswould have increased group-related differ-ences among ewes and particularly among lambs Howeverour study aimed to simulate local breeding conditions that isextensive grazing and no separation of treated fromuntreatedanimals Untreated animals favor the ldquorefugiardquo populationof parasites by inducing a dilution effect on eggs shed bytreated animals although most treatment practices still relyon systematic treatment of animal groups [44]

The fluctuation in FEC observed throughout ewersquos repro-ductive cycle might have been linked to ewersquos productivitystage and the endocrine immunological and metabolicchanges [6 13 16] Low mean FEC in mature ewes at dry andmating periods could be related to minimum maintenancenutritional requirements and to the active immunologicalresponse described against gastrointestinal nematodes inempty adult ewes that limit the establishment of consumed


infective larvae and the development and reproduction ofparasitic stages [13 18]

In contrast nutritional requirements are increased duringpregnancy and late pregnancy hence it is possible thatthe increased mean FEC recorded during pregnancy butespecially at late pregnancy could be related to higher nutri-tional demands leading to augmented intake of contaminatedherbage with infective larval stages but also to the onset ofimmunity breakdown towards gastrointestinal nematodesIn this study the highest percentage of ewes with bodycondition values ge3 was recorded at late pregnancy period(884) Macarthur et al [14] have described that ewersquosbody condition values ge3 at late pregnancy improve theproductive performance of lactating ewes and suckling lambsand reduce the risk of immune relaxation to gastrointestinalnematodes during peripartum period This suggests that anadequate nutrient supply by pasturing and supplementationin the flock could reduce the impact on the severity ofgastrointestinal infections during lactation It has been alsoestablished that immunological deficiencies against gastroin-testinal nematodes start at late pregnancy and they wererelated to low levels of both circulating eosinophils andtotal antibodies directed against nematodes 23 days beforelambing [45] The FEC values observed in this study at latepregnancy (Table 1) suggest the need to establish strategictreatment protocols at this critical period reducing pasturecontamination and offspring infection after lambing

At immediate peripartum period there was a slightreduction in FEC in control ewes followed by a significantincrease during lactation (Figure 2(a)) On the contrary ewesof groups 119879

1

and 1198792

displayed a significant and sustaineddecrease in FEC after periparturient treatment Although 119879

1

ewes maintained a slightly lower gastrointestinal nematodeburden during all lactation no differences in terms of FECor zootechnical parameters were observed between groups119879

1

and 1198792

At intermediate and late postpartum period a continuous

and drastic increase in mean FEC was observed in controlewes At this time ewes should increase their catabolism of fattissue in order to ensure the production of milk to supporttheir lambs [21] Late postpartum FEC peak reached incontrol ewes coincides with the systemic and local relaxationof the immunological response against nematodes reportedby Beasley et al [45] six weeks after lambing It has beendescribed that during these periods the rate of establish-ment of adult parasites is increased and the ewes lost theirability to suppress nematodes fecundity allowing a furthersignificant increase in FEC [21 45] The stress caused bybirth process nursing andmaternal behavior could favor thealready depressed systemic immunity and promote the PPER[14] Indeed relaxation of immunity against gastrointestinalnematodes was observed in control ewes in which 357(119899 = 5) had FEC higher than 4000 eggs per gram at late post-partum period and 214 (119899 = 3) registered FAMACHAcopyvalues ge4 Only one anemic ewe was recorded in 119879

2

groupThe significance of PPER observed at late postpartum

period in this trial contributes to high larvae pasture contam-ination especially when susceptible lambs are grazing along-side the ewes thereby increasing their chances of becoming

heavily infected Our results showed that after the latepostpartum peak in C ewes there was a significant increasein lambsrsquo FEC at preweaning period due to the ingestionof pasture contaminated with nematode infective larvae Aneffective acquired immunological response in lambs is onlygradually developed during the first year of life [6] Strategictreatment of ewes seemed to somewhat protect their lambsdelaying nematode infection (Figure 2(b)) It is possible thatdelayed egg excretion in lambs born from treated ewes wasdue to prolonged Mox secretion by milk suckling Imperialeet al [46] showed that residual concentrations of Mox wererecovered in milk up to 35 days after treatment (between178 and 1835 ngmLminus1 daily) Considering that daily milkintake ranges from 1000 to 2000mL in lambs milk secretionof 100 ngmLminus1 Mox per day would lead to ingestion of100ndash200120583g Mox per lamb per day Although this temporalexcretion of Mox could reduce FEC it also exposes lambsrsquonematodes to subtherapeutic doses reducing ldquorefugiardquo pop-ulation of parasites and predisposing to resistance processes[47] Recently Dever and Kahn [48] have demonstratedthat anthelmintics extremely lipophilic as Mox administeredat the rate of 1mg kgminus1 of body weight to lactating ewescould reduce significantly FEC in suckling offspring andexpose lambs to subtherapeutic doses of the drug a riskfactor for the development of anthelmintic resistance Ourstudy employed only 200mgmLminus1 and due to differences intreatment period application (late pregnancy or immediateperipartum) 119879

1

offspring received lower Mox by milk than1198792

In order to reduce the risk of milk Mox residues latepregnancy treatment 35 days before lambing could be recom-mended

As mentioned earlier all animals enrolled in this studywere kept together in order to standardize infectious larvaepressure and to favor ldquorefugiardquo gastrointestinal nematodepopulation Despite the high estimated PEMox and PWPer itwould however be interesting to assess the protective effectof ewesrsquo peripartum treatment in animals housed on separatepastures in order to evaluate the impact of treatment on FECand clinical parameters in ewes and lambs whose infectiouslarvae pressure would be lower than in the present studywhere untreated control ewes continued to contaminate theenvironment of treated ewes and their untreated offspring

5 Conclusions

This study describes the FEC changes throughout ewesrsquoreproductive stages and confirmed that PPER exists undertropical Andes high altitude conditions in Colombia Moxtreatment applied prior to or shortly after lambing efficientlyprevented PPER and reduced changes of FAMACHA andDag scores over time FEC increase occurring in suck-ling lambs at preweaning period tended to be delayed bytreating ewes at peripartum period Although larger animalgroups are needed to characterize the impact of PPER onzootechnical parameters this study suggests that ewes raisedunder tropical Andes high altitude conditions are prone toundergo changes of pathophysiological indicators in responseto increased gastrointestinal nematode burdens that could beuseful in targeted treatment strategies


Disclosure

Preliminary results were presented as an abstract at the2nd Benelux Congress on Physiology and PharmacologyMaastricht 4th-5th April 2014

Conflict of Interests

None of the authors of this paper has a financial or personalrelationship with other people or organizations that couldinappropriately influence or bias the content of the paper

Acknowledgment

The authors thank ldquoCooperation Universitaire Belgerdquo ARESBelgium for financial support

References

[1] S Gaba J Cabaret C Chylinski C Sauve J Cortet and ASilvestre ldquoCan efficient management of sheep gastro-intestinalnematodes be based on random treatmentrdquo Veterinary Para-sitology vol 190 no 1-2 pp 178ndash184 2012

[2] MRKnox R B Besier L F Le Jambre et al ldquoNovel approachesfor the control of helminth parasites of livestockVI summary ofdiscussions and conclusionsrdquo Veterinary Parasitology vol 186no 1-2 pp 143ndash149 2012

[3] D M Leathwick and R B Besier ldquoThe management of anthel-mintic resistance in grazing ruminants in Australasiamdashstra-tegies and experiencesrdquo Veterinary Parasitology vol 204 no 1-2 pp 44ndash54 2014

[4] J B da Silva C P Rangel B de Azevedo Baeta and A Hda Fonseca ldquoRisk factors relating to helminth infections incows during the peripartumrdquo Revista Brasileira de ParasitologiaVeterinaria vol 21 no 2 pp 92ndash96 2012

[5] V Goldberg G Ciappesoni and I Aguilar ldquoModelling thefaecal worm egg count curve during the periparturient periodin uruguayan merino sheeprdquo Spanish Journal of AgriculturalResearch vol 10 no 4 pp 986ndash992 2012

[6] I G Colditz D L Watson G D Gray and S J Eady ldquoSomerelationships between age immune responsiveness and resist-ance to parasites in ruminantsrdquo International Journal for Para-sitology vol 26 no 8-9 pp 869ndash877 1996

[7] S Tembely A Lahlou-Kassi J E O Rege et al ldquoBreed andseason effects on the peri-parturient rise in nematode eggoutput in indigenous ewes in a cool tropical environmentrdquoVeterinary Parasitology vol 77 no 2-3 pp 123ndash132 1998

[8] N D Sargison ldquoPharmaceutical treatments of gastrointestinalnematode infections of sheepmdashfuture of anthelmintic drugsrdquoVeterinary Parasitology vol 189 no 1 pp 79ndash84 2012

[9] L P Kahn M R Knox and G D Gray ldquoEnhancing immunityto nematode parasites in pregnant and lactating sheep throughnutrition and genetic selectionrdquo in Recent Advances in AnimalNutrition in Australia J L Corbett Ed vol 12 pp 15ndash22University of New England Armidale Australia 1999

[10] P Sakkas J G M Houdijk S Athanasiadou and I KyriazakisldquoSensitivity of periparturient breakdown of immunity to para-sites to dietary protein sourcerdquo Journal of Animal Science vol90 no 11 pp 3954ndash3962 2012

[11] A M Beasley L P Kahn and R G Windon ldquoThe periparturi-ent relaxation of immunity in Merino ewes infected with Tri-chostrongylus colubriformis endocrine and body compositionalresponsesrdquo Veterinary Parasitology vol 168 no 1-2 pp 51ndash592010

[12] A C Kotze B M Hines and A P Ruffell ldquoA reappraisal of therelative sensitivity of nematode pharyngeal and somatic mus-culature to macrocyclic lactone drugsrdquo International Journal forParasitology Drugs and Drug Resistance vol 2 pp 29ndash35 2012

[13] A R Sykes ldquoEnvironmental effects on animal production thenutritional demands of nematode parasite exposure in sheeprdquoAsian-Australasian Journal of Animal Sciences vol 13 pp 343ndash350 2000

[14] F A Macarthur L P Kahn and R G Windon ldquoImmune res-ponse of twin-bearing Merino ewes when infected with Hae-monchus contortus effects of fat score and prepartum supple-mentationrdquo Livestock Science vol 157 no 2-3 pp 568ndash576 2013

[15] A R Williams J C Greeff P E Vercoe R J Dobson and L JE Karlsson ldquoMerino ewes bred for parasite resistance reducelarval contamination onto pasture during the peri-parturientperiodrdquo Animal vol 4 no 1 pp 122ndash127 2010

[16] N D Sargison D J Bartram and D J Wilson ldquoUse of along acting injectable formulation of moxidectin to controlthe periparturient rise in faecal Teladorsagia circumcincta eggoutput of ewesrdquo Veterinary Parasitology vol 189 no 2ndash4 pp274ndash283 2012

[17] L P KahnMRKnoxGDGray JM Lea and SWWalkden-Brown ldquoEnhancing immunity to nematode parasites in single-bearing Merino ewes through nutrition and genetic selectionrdquoVeterinary Parasitology vol 112 no 3 pp 211ndash225 2003

[18] A M Beasley L P Kahn and R G Windon ldquoThe influenceof reproductive physiology and nutrient supply on the peripar-turient relaxation of immunity to the gastrointestinal nematodeTrichostrongylus colubriformis in Merino ewesrdquo Veterinary Par-asitology vol 188 no 3-4 pp 306ndash324 2012

[19] L A Jones P Sakkas J G M Houdijk D P Knox andI Kyriazakis ldquoAmelioration of the periparturient relaxationof immunity to parasites through a reduction in mammalianreproductive effortrdquo International Journal for Parasitology vol42 no 13-14 pp 1127ndash1134 2012

[20] F J McPherson S Shini A W Gibbon and M J DrsquoOcchioldquoProtein supplementation in the first 100 days of gestationfails to enhance resistance of weaned Merino lambs againstHaemonchus contortusrdquo Livestock Science vol 150 no 1ndash3 pp11ndash21 2012

[21] F A Macarthur L P Kahn and R G Windon ldquoRegulatingmaternal production of twin-bearing Merino ewes throughfat score and prepartum supplementation when infected withHaemonchus contortusrdquo Livestock Science vol 157 no 2-3 pp442ndash451 2013

[22] V H Suarez ldquoHelminthic control on grazing ruminants andenvironmental risks in South Americardquo Veterinary Researchvol 33 no 5 pp 563ndash573 2002

[23] M B Molento F S Fortes D A S Pondelek et al ldquoChallengesof nematode control in ruminants focus on Latin AmericardquoVeterinary Parasitology vol 180 no 1-2 pp 126ndash132 2011

[24] A N Henrioud ldquoTowards sustainable parasite control practicesin livestock production with emphasis in Latin AmericardquoVeterinary Parasitology vol 180 no 1-2 pp 2ndash11 2011

[25] J F Torres-acosta R I Rodrıguez-Vivas and R Camara-Sarmiento ldquoEfecto del parto sobre la eliminacion de huevecillos


de nematodos y ooquistes de Eimeria en cabras criollasrdquoRevistaBiomedica vol 6 no 4 pp 208ndash215 1995

[26] E Romjali A Batubara V S Pandey and R M GatenbyldquoShort communication Peri-parturient rise in faecal strongyleegg counts of different genotypes of sheep in North SumatraIndonesiardquoVeterinary Parasitology vol 68 no 1997 pp 191ndash1962000

[27] N Mandonnet M Bachand M Mahieu et al ldquoImpact onproductivity of peri-parturient rise in fecal egg counts in Creolegoats in the humid tropicsrdquoVeterinary Parasitology vol 134 no3-4 pp 249ndash259 2005

[28] M Mahieu and G Aumont ldquoPeriparturient rise in MartinikHair Sheep and perspectives for gastrointestinal nematodecontrolrdquo Tropical Animal Health and Production vol 39 no 6pp 387ndash390 2007

[29] D C Moreno-Vargas and H A Grajales-Lombana ldquoCaracteri-zacion del proceso administrativo y de mercado en los sistemasovinos del tropico alto colombianordquo Revista Cienci Animal no7 pp 85ndash98 2014

[30] M Knox and J Steel ldquoNutritional enhancement of parasitecontrol in small ruminant production systems in developingcountries of south-east Asia and the Pacificrdquo InternationalJournal for Parasitology vol 26 no 8-9 pp 963ndash970 1996

[31] R A Rocha A F T Amarante and P A Bricarello ldquoCompari-son of the susceptibility of Santa Ines and Ile de France ewes tonematode parasitism around parturition and during lactationrdquoSmall Ruminant Research vol 55 no 1ndash3 pp 65ndash75 2004

[32] GMorales E Sandoval L A Pino andZ Rondon ldquoEvaluacionde dos criterios de utilidad en un programa de control de lainfeccion por nematodos gastrointestinales en ovinos mediantetratamiento antihelmıntico selectivordquo Zootecnia Tropical vol26 no 2 pp 141ndash150 2008

[33] M Tibbo K Aragaw J Philipsson et al ldquoA field trial of pro-duction and financial consequences of helminthosis control insheep production in Ethiopiardquo Preventive Veterinary Medicinevol 84 no 1-2 pp 152ndash160 2008

[34] G Cringoli L Rinaldi V Veneziano L Mezzino J Vercruysseand F Jackson ldquoEvaluation of targeted selective treatmentsin sheep in Italy effects on faecal worm egg count and milkproduction in four case studiesrdquo Veterinary Parasitology vol164 no 1 pp 36ndash43 2009

[35] P Godoy J Lian R N Beech andR K Prichard ldquoHaemonchuscontortus P-glycoprotein-2 in situ localisation and characteri-sation of macrocyclic lactone transportrdquo International Journalfor Parasitology vol 45 no 1 pp 85ndash93 2015

[36] M Lloberas L Alvarez C Entrocasso et al ldquoComparativetissue pharmacokinetics and efficacy of moxidectin abamectinand ivermectin in lambs infected with resistant nematodesimpact of drug treatments on parasite P-glycoprotein expres-sionrdquo International Journal for Parasitology Drugs and DrugResistance vol 3 pp 20ndash27 2013

[37] DMarquezG Jimenez FGarcıa andCGarzon ldquoResistencia alos antihelmınticos en nematodos gastrointestinales de bovinosen municipios de Cundinamarca y Boyacardquo Corpoica Ciencia yTecnologıa Agropecuaria vol 9 no 1 pp 113ndash123 2008

[38] J M Broughan and RWall ldquoFaecal soiling and gastrointestinalhelminth infection in lambsrdquo International Journal for Parasitol-ogy vol 37 no 11 pp 1255ndash1268 2007

[39] A Di Loria V Veneziano D Piantedosi et al ldquoEvaluation ofthe FAMACHA system for detecting the severity of anaemia insheep from southern Italyrdquo Veterinary Parasitology vol 161 no1-2 pp 53ndash59 2009

[40] S A Henriksen and J P Christensen ldquoDemonstration of Iso-spora suis oocysts in faecal samplesrdquoVeterinary Record vol 131no 19 pp 443ndash444 1992

[41] R J Dobson B C Hosking C L Jacobson et al ldquoPreservingnew anthelmintics a simple method for estimating faecal eggcount reduction test (FECRT) confidence limits when efficacyandor nematode aggregation is highrdquo Veterinary Parasitologyvol 186 no 1-2 pp 79ndash92 2012

[42] G C Coles C Bauer F H M Borgsteede et al ldquoWorldAssociation for the Advancement of Veterinary Parasitology(WAAVP) methods for the detection of anthelmintic resis-tance in nematodes of veterinary importancerdquo Veterinary Para-sitology vol 44 no 1-2 pp 35ndash44 1992

[43] P R Torgerson M Paul and R Furrer ldquoEvaluating faecalegg count reduction using a specifically designed packagelsquoeggCountsrsquo in R and a user friendlyweb interfacerdquo InternationalJournal for Parasitology vol 44 no 5 pp 299ndash303 2014

[44] F Kenyon A W Greer G C Coles et al ldquoThe role oftargeted selective treatments in the development of refugia-based approaches to the control of gastrointestinal nematodesof small ruminantsrdquo Veterinary Parasitology vol 164 no 1 pp3ndash11 2009

[45] A M Beasley L P Kahn and R G Windon ldquoThe peripar-turient relaxation of immunity in Merino ewes infected withTrichostrongylus colubriformis parasitological and immuno-logical responsesrdquo Veterinary Parasitology vol 168 no 1-2 pp60ndash70 2010

[46] F A Imperiale M R Busetti V H Suarez and C E LanusseldquoMilk excretion of ivermectin and moxidectin in dairy sheepassessment of drug residues during cheese elaboration andripening periodrdquo Journal of Agricultural and Food Chemistryvol 52 no 20 pp 6205ndash6211 2004

[47] J A vanWyk ldquoRefugiamdashoverlooked as perhaps themost potentfactor concerning the development of anthelmintic resistancerdquoOnderstepoort Journal of Veterinary Research vol 68 no 1 pp55ndash67 2001

[48] M Dever and L Kahn ldquoDecline in faecal worm egg countsin lambs suckling ewes treated with lipophilic anthelminticsImplications for hastening development of anthelmintic resis-tancerdquo Veterinary Parasitology vol 209 no 3-4 pp 229ndash2342015

Submit your manuscripts athttpwwwhindawicom

Veterinary MedicineJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Veterinary Medicine International



International Journal of

Microbiology


AnimalsJournal of

EcologyInternational Journal of


PsycheHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Evolutionary BiologyInternational Journal of


Hindawi Publishing Corporationhttpwwwhindawicom

Applied ampEnvironmentalSoil Science

Volume 2014

Biotechnology Research International


Agronomy




Journal of Parasitology Research

Hindawi Publishing Corporation httpwwwhindawicom


Volume 2014

Zoology

GenomicsInternational Journal of


InsectsJournal of


The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014


VirusesJournal of

ScientificaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Cell BiologyInternational Journal of



Case Reports in Veterinary Medicine


continues for several weeks after parturition This impairedresistance is associated with an increase in strongylid fecalegg count (FEC) commonly referred to as the periparturientnematode egg rise (PPER) [5 9ndash14] PPER has been des-cribedmainly in sheep breeds exploited in temperate regionsIndeed the flocksrsquo seasonal management allows the springcontamination of pasture with nematode eggs shed by lac-tating ewes and the concomitant infection of lambs with theinfective larvae hatched from those eggs [15 16] Althoughwell known the exact cause of PPER remains poorly under-stood Increased FEC has been also associated with variationsin hormonal profiles at peripartum (prolactin and cortisollevels) and low levels of metabolisable protein intake duringlate pregnancy and lactation [13 17ndash21]

In tropical regions of South America sheep productionis based on extensive grazing with limited managementand sanitary practices which leads to increased mortalityrates and reduced productivity due to gastrointestinal ne-matodes [22ndash24] Under these conditions the importanceof a PPER and its epidemiological consequences in smallruminants remain to be established [7 25ndash28] On the onehand infective larvae may be continuously available in thetropics and reproductive cycles and lambing are not strictlyseasonal events as in temperate countries Indeed in Colom-bian flocks lambing might occur during the entire yearbut two main annual periods of births during AprilndashJuneand November-December at the end of rainy periods aredescribed [29] On the other hand physiopathological con-sequences of PPER in lactating ewes and their offspringare believed to be important in the tropics because theinfectious pressure persists at a high level and because nutri-tional management is often heterogeneous [24 26 30 31]Consequently environmental parameters reproductive cyclefeatures and feeding management practices are fundamentaltools for rational anthelmintic treatment [3 4 32] In order tominimize nematode egg outputs and to regulate pasture con-tamination with infective third larval stages in tropical sheepproduction systems strategic treatment of highly infectedanimal groups as periparturient ewes is recommended [28 33 34]

Among the available chemical groups used to control gas-trointestinal nematodes in sheep macrocyclic lactones rep-resent the cornerstone of current anthelmintic drug control[35] Moxidectin (Mox) a macrocyclic lactone of the chemi-cal family of milbemycins has been widely used during thelast 30 years [36] However the intensive use of this broad-spectrum antiparasitic compound could lead to the emer-gence of resistance in gastrointestinal nematodes [35 36]This situation has encouraged the search for treatment strate-gies to optimize Mox potential avoiding unnecessary treat-ments particularly in geographic areas where Mox use isnot a frequent practice and resistance is not yet fully present[36 37]

The present study hypothesized (1) that PPER occursin Colombian sheep raised under Andean high altitudetropical conditions during the period of the highest lamb-ing rate (AprilndashJune) (2) that Mox is still an effectiveanthelmintic molecule at tropical Andes and (3) thatMox strategic treatment of ewes administered either at

late pregnancy or early peripartum period would preventPPER

2 Materials and Methods

The study was conducted at the Center for Sheep ResearchTechnological Development and Extension of the NationalUniversity of Colombia located inMosquera-Cundinamarca(4∘4010158405710158401015840N 74∘1210158405010158401015840W)at 2510m above sea levelThemeantemperature during the study period was 135∘C and themonthly average rainfall 86mm The protocols employedfollowed the national guidelines for care and use of animals(Colombian Law 891989) and were approved by the EthicalCommittee of the Faculty of VeterinaryMedicine andAnimalScience of National University of Colombia (CB-035-2013)

21 Animals This study enrolled 43 healthy wool ewes offour breeds (Colombian creole Romney Marsh Hampshireand Corriedale) Ewes were grazing together in Loliumperenne and Pennisetum clandestinum pastures and weresupplemented with concentrate feed hay and mineralizedsalt according to physiological requirements Fresh drinkingwater was available ad libitum Ewesrsquo clinical and para-sitological follow-up was performed during one completereproductive cycle (dry period mating period pregnancyperiod and postpartum period) Since birth lambs (119899 = 58)were keptwith their dams andunderwent the same follow-up

22 Experimental Design A longitudinal study was con-ducted during 40 weeks and included nine sampling periodswhere parasitological and clinical evaluations were per-formed in relation to ewersquos reproductive state (Figure 1)The last anthelmintic treatment was applied more than fourweeks before the beginning of the follow-up (fenbendazole10mgsdotkgminus1 once daily during three days) Ewes were investi-gated before breeding around mating (natural reproductionwith a mating period of 34 days) at midpregnancy (sim80 daysof pregnancy) at late pregnancy (7ndash29 days before lambing)at immediate peripartum (6 days before until 2 days afterlambing) at early postpartum (2ndash15 days after lambing) atintermediate postpartum (15ndash30 days after lambing) at latepostpartum (30ndash45 days after lambing) and at prewean-ing (46ndash60 days after lambing) Lambs were investigatedsince birth at the same time points as their dams At latepregnancy ewes were ranked on the basis of body weightbody score and parasite infection burden and allocated intothree groups Ewes of group 119879

1

(119899 = 15) received a singleMox (Cydectin Fort Dodge Animal Health) subcutaneousinjection of 200 120583g kgminus1 of body weight at late pregnancy(sim135 days of gestation) Ewes of group 119879

2

(119899 = 14) receiveda single Mox subcutaneous injection of 200 120583g kgminus1 bodyweight 2 days after lambing Control ewes (C group 119899 = 14)remained untreated throughout the whole study Five furtherfortnightly samplings were performed after lambing

23 Clinical and Zootechnical Parameters The animals weremonitored daily during the entire course of the exper-iment Development of clinical signs related to parasite


D M MP

TT1

TT2

Lambing





PPERPre PWPer

T1 ewesn = 14

n = 14

n = 14

C ewes

T2 ewes

Lambsn = 58

PEMoxT1

PEMoxT2








1198791198940

) times (1198620

11986215

)] where 1198791198940

and 11987911989415

are the arithmetic


1

or 1198792

) and 1198620

and 11986215



1

and 1198792



1

and 1198792





0100020003000400050006000700080009000

10000

Dry

Mat

ing

Preg

nanc

y

Late

pr

egna

ncy

Imm

edia

te

perip

artu

m

Early

po

stpar

tum

Inte

rmed

iate

postp

artu

m

Late

po

stpar

tum

Prew

eani

ng

C ewes

a a

b b

PPER

b b

Mea

n va

lues

of Stro

ngylid

eggs

per g

ram

of f

eces

(epg

)

T2 ewesT1 ewes


0

1000

2000

3000

4000

5000

6000

7000

8000

9000

10000

Part

uriti

on

Early

postp

artu

m

Inte

rmed

iate

postp

artu

m

Late

postp

artu

m

Prew

eani

ng

C lambs

a

b

Mea

n va

lues

of Stro

ngylid

eggs

per g

ram

of f

eces

(epg

)

T2 lambsT1 lambs



1

and1198792


1

and 14 1198792


1


ewes)


3 Results



and1198792


1

and 1198792



1


2



1

or 1198792


4 Discussion







lowast

Treated ewes1198991198791= 15 and1198991198792= 14

FECR 95 CI


)






)





1




Measured parameters



lowast









1198792








1

and 1198792


1


1

and 1198792



2




1




5 Conclusions



Disclosure




Acknowledgment


References


























































Microbiology


AnimalsJournal of








Volume 2014



Agronomy







Volume 2014

Zoology



InsectsJournal of




VirusesJournal of







D M MP

TT1

TT2

Lambing





PPERPre PWPer

T1 ewesn = 14

n = 14

n = 14

C ewes

T2 ewes

Lambsn = 58

PEMoxT1

PEMoxT2








1198791198940

) times (1198620

11986215

)] where 1198791198940

and 11987911989415

are the arithmetic


1

or 1198792

) and 1198620

and 11986215



1

and 1198792



1

and 1198792





0100020003000400050006000700080009000

10000

Dry

Mat

ing

Preg

nanc

y

Late

pr

egna

ncy

Imm

edia

te

perip

artu

m

Early

po

stpar

tum

Inte

rmed

iate

postp

artu

m

Late

po

stpar

tum

Prew

eani

ng

C ewes

a a

b b

PPER

b b

Mea

n va

lues

of Stro

ngylid

eggs

per g

ram

of f

eces

(epg

)

T2 ewesT1 ewes


0

1000

2000

3000

4000

5000

6000

7000

8000

9000

10000

Part

uriti

on

Early

postp

artu

m

Inte

rmed

iate

postp

artu

m

Late

postp

artu

m

Prew

eani

ng

C lambs

a

b

Mea

n va

lues

of Stro

ngylid

eggs

per g

ram

of f

eces

(epg

)

T2 lambsT1 lambs



1

and1198792


1

and 14 1198792


1


ewes)


3 Results



and1198792


1

and 1198792



1


2



1

or 1198792


4 Discussion







lowast

Treated ewes1198991198791= 15 and1198991198792= 14

FECR 95 CI


)






)





1




Measured parameters



lowast









1198792








1

and 1198792


1


1

and 1198792



2




1




5 Conclusions



Disclosure




Acknowledgment


References


























































Microbiology


AnimalsJournal of








Volume 2014



Agronomy







Volume 2014

Zoology



InsectsJournal of




VirusesJournal of







0100020003000400050006000700080009000

10000

Dry

Mat

ing

Preg

nanc

y

Late

pr

egna

ncy

Imm

edia

te

perip

artu

m

Early

po

stpar

tum

Inte

rmed

iate

postp

artu

m

Late

po

stpar

tum

Prew

eani

ng

C ewes

a a

b b

PPER

b b

Mea

n va

lues

of Stro

ngylid

eggs

per g

ram

of f

eces

(epg

)

T2 ewesT1 ewes


0

1000

2000

3000

4000

5000

6000

7000

8000

9000

10000

Part

uriti

on

Early

postp

artu

m

Inte

rmed

iate

postp

artu

m

Late

postp

artu

m

Prew

eani

ng

C lambs

a

b

Mea

n va

lues

of Stro

ngylid

eggs

per g

ram

of f

eces

(epg

)

T2 lambsT1 lambs



1

and1198792


1

and 14 1198792


1


ewes)


3 Results



and1198792


1

and 1198792



1


2



1

or 1198792


4 Discussion







lowast

Treated ewes1198991198791= 15 and1198991198792= 14

FECR 95 CI


)






)





1




Measured parameters



lowast









1198792








1

and 1198792


1


1

and 1198792



2




1




5 Conclusions



Disclosure




Acknowledgment


References


























































Microbiology


AnimalsJournal of








Volume 2014



Agronomy







Volume 2014

Zoology



InsectsJournal of




VirusesJournal of











lowast

Treated ewes1198991198791= 15 and1198991198792= 14

FECR 95 CI


)






)





1




Measured parameters



lowast









1198792








1

and 1198792


1


1

and 1198792



2




1




5 Conclusions



Disclosure




Acknowledgment


References


























































Microbiology


AnimalsJournal of








Volume 2014



Agronomy







Volume 2014

Zoology



InsectsJournal of




VirusesJournal of










1

and 1198792


1


1

and 1198792



2




1




5 Conclusions



Disclosure




Acknowledgment


References


























































Microbiology


AnimalsJournal of








Volume 2014



Agronomy







Volume 2014

Zoology



InsectsJournal of




VirusesJournal of







Disclosure




Acknowledgment


References


























































Microbiology


AnimalsJournal of








Volume 2014



Agronomy







Volume 2014

Zoology



InsectsJournal of




VirusesJournal of






































Microbiology


AnimalsJournal of








Volume 2014



Agronomy







Volume 2014

Zoology



InsectsJournal of




VirusesJournal of






research article effect of moxidectin treatment at...

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