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Roczniki Naukowe Polskiego Towarzystwa Zootechnicznego, t. 6 (2010), nr 1 Milk yield and quality in sheep with maedi-visna virus* Czesława Lipecka 1 , Anna Szymanowska 1 , Marek Szymanowski 1 , Andrzej Junkuszew", Tomasz M. Gruszecki", Jacek Kuźmak 2 , Monika Olech 2 lUniversity of Life Sciences, Department of Sheep and Goat Breeding, ul. Akademicka l3, 20-950 Lublin, Poland 2National Veterinary Research Institute, Department of Biochemistry, al. Partyzantów 57, 24-100 Puławy, Poland Milk yie!d eontroi strategy involved 65 ewes of synthetic meat-prolific lines BCP and SCP of a different serologie response developed to the presenee of antibodies against maedi-visna virus (MVV). Atotal number of ewes eomprised 36 seropositive animals (MVV+) and 29 seronegative ones (MVV-). The ewes of the both groups were similar as regards genotype, suceessive lactation (1-4) and the number of lambs reared. Dams and offspring were managed under the same environmental conditions and feeding systems in two groups, with no eontaet between them (from November through April). Milk yield controi carried out for two months (every 14 day) was implemented by a eonventional method, i.e. oxytocin administration. The milk sampies were examined for fat, protein and laetose eontent, whereas TOK test (equiva- lent of CMT) and the milk SCC study were used to assess the mammary gland health status. The obtained researeh findings have indicated that the ewes ehallenged with MV vi- rus(MVV+) during the 2-month lactation period produced less milk by average 7.09 kg but of a higher protein level (by 0.18 %) and fat (by 0.21 %) while lower lactose eoncentration (by 0.21 %) as compared to the ewes free from virus (MVV-). Variability of these traits was lactation - stage dependent. There was found a lower percentagę of ewe udder infections in the MVV- ewes than in the MVV+ ones. The mammary gland condition was shown to be affeeted not only by maedi-visna infection but a genotype and lactation stage as well. KEY WORDS: sheep / maedi-visna / milk The sheep farming focused on slaughter lamb production is large1y dependent on ewe milk efficiency. It determines the appropriate development and growth rate of lambs at the first stage of their life when milk remains the sole nutritional source providing passive immunity to the neonatal lambs. Amongst many factors affecting *The present work has been performed within the frames of research projeet 2 P06Z 009 29. 51

Milk yield and quality in sheep with maedi-visna virus*ptz.icm.edu.pl/download/2010/tom_6_1/6_Lipecka.pdfRoczniki Naukowe Polskiego Towarzystwa Zootechnicznego, t. 6 (2010), nr 1 Milk

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  • Roczniki Naukowe Polskiego Towarzystwa Zootechnicznego, t. 6 (2010), nr 1

    Milk yield and quality in sheepwith maedi-visna virus*

    Czesława Lipecka 1, Anna Szymanowska 1,Marek Szymanowski 1,Andrzej Junkuszew", Tomasz M. Gruszecki", Jacek Kuźmak2,Monika Olech2

    lUniversity of Life Sciences, Department of Sheep and Goat Breeding,ul. Akademicka l3, 20-950 Lublin, Poland2NationalVeterinary Research Institute, Department of Biochemistry,al. Partyzantów 57, 24-100 Puławy, Poland

    Milk yie!d eontroi strategy involved 65 ewes of synthetic meat-prolific lines BCP and SCP ofa different serologie response developed to the presenee of antibodies against maedi-visnavirus (MVV). Atotal number of ewes eomprised 36 seropositive animals (MVV+) and 29seronegative ones (MVV-). The ewes of the both groups were similar as regards genotype,suceessive lactation (1-4) and the number of lambs reared. Dams and offspring were managedunder the same environmental conditions and feeding systems in two groups, with no eontaetbetween them (from November through April). Milk yield controi carried out for two months(every 14 day) was implemented by a eonventional method, i.e. oxytocin administration. Themilk sampies were examined for fat, protein and laetose eontent, whereas TOK test (equiva-lent of CMT) and the milk SCC study were used to assess the mammary gland health status.The obtained researeh findings have indicated that the ewes ehallenged with MV vi-rus(MVV+) during the 2-month lactation period produced less milk by average 7.09 kg butof a higher protein level (by 0.18%) and fat (by 0.21%) while lower lactose eoncentration (by0.21%) as compared to the ewes free from virus (MVV-). Variability of these traits waslactation - stage dependent. There was found a lower percentagę of ewe udder infections inthe MVV- ewes than in the MVV+ ones. The mammary gland condition was shown to beaffeeted not only by maedi-visna infection but a genotype and lactation stage as well.

    KEY WORDS: sheep / maedi-visna / milk

    The sheep farming focused on slaughter lamb production is large1y dependent onewe milk efficiency. It determines the appropriate development and growth rate oflambs at the first stage of their life when milk remains the sole nutritional sourceproviding passive immunity to the neonatal lambs. Amongst many factors affecting

    *The present work has been performed within the frames of research projeet 2 P06Z 009 29.

    51

  • ovine milk yield, the ani mai health status is of primary importance. One of the com monchronic infections reported in sheep flocks remains maedi-visna disease, caused by MVvirus from the genus Lentlvirus of the family Retroviridae. The incidence of the virusis globally differentiated [2, 5, 6, 10]. In Europe, there are sheep flocks with even90-95% animals seropositive to MV virus [l, 3, 22, 24] whereas in Poland, it isestimated that approximately 60% of sheep flocks is MVV-infected [12].

    A number of studies [5, 8, 25] has provided strong evidence that the major infec-tious agent is dam' s milk, especially colostrum.

    Although the c\inical manifestations of maedi-visna disease are predominantlyobserved in older sheep [11, 13], the sheep flocks with a recognized seropositivereaction are frequently characterized by lower birth-weight lambs, declined body gainsand increased mortality rate in both, mothers and offspring [6, 8, 22]. Arsenault et al.[2] and Dungu et al. [6] found markedly higher body weight after birth (from 0.15 upto 0.50 kg) in the lamb groups from seronegative mothers as compared to the infectedones. While Keen et al. [9, 10] noted that lambs obtained from the MVV challengedmothers showed average body weight lower by 0.59 kg on 56 day of age and 3-4 kg on80 day as compared to the lambs from seronegative animals. This fact may be attributedto, among others, progressing deterioration of production and quality of milk obtainedfrom sheep mothers with rnaedi-visna MV virus and as a consequence, a declinedgrowth rate of offspring. Besides, Peterhans et al. [21] and Ploumi et al. [22] indicatethat MVV-seropositive sheep flocks are commonly associated with mastitis incidencethat results in economical losses caused by the decreased milk production. In France,the estimates assume that in highly infected flocks (over 50%), milk yield depressed by10% that accounts for approximately 4% income from the sale of milk and lamb meat.

    The present research objective was to assess ovine milk yield and quality as wellas to evaluate the mamrnary gland of sheep with a seropositive reaction to maedi-visnavirus.

    Materiał and methods

    In 2006-2007, the milk yield control inc\uded atotal of 65 ewes of syntheticprolific-rneat lines Bep and sep, in that 36 seropositive animals (MVV+) and 29seronegative ones (MVV-).The ew es were allocated to the aforementioned groups onthe basis of commercial ELISA MVV assay (Institute Pourquier, France) used formonitoring the basie herd of mothers. Determinations were performed three times foreach ewe (every 6 month) in compliance with the producer's instructions and the ELISAreadings, using 450 nm wavelength range.

    The ewes of both groups were uniform as regards a genotype, successive lactation(1-4) and the number of reared lambs. The ewes and lambs were managed under thesame environmental conditions, maintained in twa separate groups (MVV+ and MVV-)with no direct contact from November through April. A feeding level of each groupwas in compliance with the recommended nutritional standards [23]. The lambs wereraised in the conventional production system (up to 70 day) and from 10 day of age

    52

  • they were fed hay and concentrate ad libitum. The 2-month milk yield control (every14 day) was performed by the traditional method, i.e. oxytocin administration [16] thatlaunched after the colostrum period. The collected milk sampies were evaluated fora eontent of protein, fat and lactose with Milko-scan apparatus application. At the endof the first and second lactation month, the mammary gland health status was assessedwith the TOK test (CMT) whereas milk somatic celI counts by Fossomatic apparatus.

    The research findings illustrating milk yield and chemical composition were analy-zed statistically using the method of least squares (SAS 9.1.3). The multifactor analysisof variance considered the effect of a group, season, genotype, successive lactation andthe num ber of reared lambs. The somatic celI counts (SCC) were presented as thou-sand/cm.' and the 10gSCC; this trait was statistically studied with the application oftwo-factor analysis of variance (genotype, group). Differences between the trait meanvalues were verified with the Tukey's test.

    Results and discussion

    During the 2-month lactation, average daily milk yield of the seropositive sheepstudied in relation to the MVV antibodies occurrence was equal to 1.87 kg and 104.5kg for the whole control period (Tab. 1). It appeared to be lower by 0.12 and 7.09 kg,respectively, compared to the seronegative mothers.

    Table 1 - Tabela 1Milk yield (kg) of seropositive (MYY+) and seronegative (MYY-) mothers at each lactation stageWydajność mleka (kg) matek serododatnich (MYY+) i seroujemnych (MYY-) w poszczególnych okresachlaktacji

    II

    MVV+ (n=36) MVV- (n=29)

    daily milk yield for daily milk yield for

    yield period yield period

    dobowa za okres dobowa za okres

    LSM SE LSM SE LSM SE LSM SE

    2.30 0.12 32.27 1.73 2,53 0.14 35042 2.02

    2.24 0.12 31.42 1.63 2.20 0.11 30.80 1.55

    1.64 0.12 22.91 1.73 1.84 0.09 25.74 1.29

    l.31 0.06 18.35 0.89 lAI 0.08 19.70 l.13

    l.87 0.09 104.57 4.97 1.99 0.07 11l.66 4.15

    Effect

    Wpływ

    Interactions

    Interakcje

    Period

    Okres

    R G L O

    * *

    li! RxM*

    IV RxM*

    LactationLaktacja

    RxM*

    R - research year - rok badań; G - genotype - genotyp; L - consecutive lactation - kolejna laktacja; 0-number of reared lambs - liczba odchowywanych jagniąt; M - maedi-visna

    *P$O.05

    53

  • The highest difference in milk production between the groups was established atthe first fourteen days as it reached 3.15 kg in favor of the MVV- mothers. The nextlactation period was marked with a slight decrease of daily yield by 0.06 kg in the groupof mothers with MVV+ and by 0.10 kg in the gro up MVV-free, yet their total milk yieldin two investigated period (I+II) proved to be higher by 2.53 kg in the sheep withoutantibodies to MVV. As the lactation prcgressed, further depression of milk productionwas observed in both groups of mothers, but the difference between MVV+ and MVV-mothers milk yields persisted, still in favor of the seronegative mothers. It is consistentwith the research results of other authars [14, 16, 17] who found that the lactation peakoccurs between 2 and 4 week which, subject to a sheep breed and lactation length isfollowed by the dec1ine of sheep milk production. The studies of Lipecka et al. [14]showed that milk production efficiency achieved between the first and fourth lactationweek constituted a reliable index of total milk production by sheep milked after wea-ning.

    According to Mroczkowski [16] milk yield of sheep proves to be a very intricateproblem affected by a number of factors with different interactions between thern. Thefact that in the present studies, none of the investigated factors had influence on milkyield during control period I (Tab. 1) implies that depressed milk production in thegroups of mothers infected by virus (MVV +) was likely to result from their poorer bodycondition and lower body weight which is confirrned, among others) in the researchesof Dungu et al. [6].

    As the lactation advanced, the influence of the research year and number of raisedlambs was shown to be more notable, while the interaction observed (year x maedi)suggests possible contribution of other factors as we1l.

    Nutritive value of ovine milk is largely determined by a eontent of such constituentslike, fat, protein ar lactose. Qualitative analysis of milk perforrned during the ongoinglactation (Tab. 2) demonstrated some variation dependent on the occurrence of maedi-visna infection and control period.

    During control period I, there was noted a significantly higher protein eontent(4.71 %) and lactose (5.60%), whereas a depressed fat level (6.18%) in milk from theMVV + mothers as compared to those free from MVV. Differences between the meanvalues of the traits studied in the milk from the MVV+ dams and MVV- ones werestatistically significant (pśO.05; PśO.Ol). In the fo1lowing lactation periods, solelyprotein eontent persisted at a higher level in the seropositive dams, while other compo-nents concentration was simiJar between the groups. At the late lactation (period IV),fat eontent in the milk from the MVV+ mothers increased (up to 7.32%) to reach alevelsignificantly higher (by 1.33%) as against the milk obtained from the MVV- mothers.Throughout the 2-month control time, average eontent of protein and fat appeared to behigher by 0.18% (pśO.Ol) and 0.21 %, respectively whereas lactose declined by 0.25%in milk from the mothers with maedi-visna disease diagnosed. Differences in the qualityof milk obtained from this group and from the mothers MVV- (except for protein) werefound within the limits of statistical errar. The features under investigation were affected

    54

  • Traits MVV+ MVV- Effect Interactions

    Cechy (n=36) (n=29) Wpływ Interakcje

    LSM SE LSM SE R G L O

    Period [ - I okres

    Protein (0/0) 4.71* 0.07 4.48* 0.Q7 **Białko (0/0)Fat(%) 6.18** 0.24 7.07** 0.22 ** ** GxM**, RxM*Tłuszcz (0/0)Lactose (0/0) 5.60** 0.03 5.40** 0.04Laktoza (0/0)

    Period II - II okres

    Protein (0/0) 4.65* 0.Q7 4.37* 0.08 LxM**Białko (0/0)Fat (0/0) 6.68 0.31 6.31 0.22 **Tłuszcz (0/0)Lactose (0/0) 5.44 0.08 6.51 1.38Laktoza (0/0)

    Period III - III okres

    Protein (0/0) 5.25 0.07 5.00 0.10Białko (0/0)Fat(%) 5.74 0.19 5.71 0.28Tluszcz (0/0)Lactose (0/0) 5.42 0.Q3 5.42 0.05 **Laktoza (0/0)

    Period IV - IV okres

    Protein (0/0) 5.41 0.08 5.47 0.19 GxM*, LxM*Białko (0/0)Fat (0/0) 7.32** 0.18 5.99** 0.19Tłuszcz (0/0)Lactose (0/0) 5.23 0.03 5.35 0.06Laktoza (0/0)

    Average for lactation - Średnio za laktację

    Protein (0/0) 5.01* 0.05 4,83* 0.08 GxM*, LxM**Białko (0/0)Fat (0/0) 6.48 0.17 6.27 0.17 ** GxM*Tłuszcz (0/0)Lactose (0/0) 5.42 0.03 5.67 0.34Laktoza (0/0)

    R - research year - rok badań; G - genotype - genotyp; L - consecutive lactation - kolejna laktacja; 0-number of reared lambs - liczba odchowywanych jagniąt; M - maedi-visna**p.::;O.Q1;*P~O.05

    55

    Table 2 - Tabela 2Milk quality of seropositive (MVV +) and seronegative (MVV-) mothers at each lactation stageJakość mleka matek serododatnich (MVV+) i seroujemnych (MVV-) w poszczególnych okresach laktacji

  • not only by the infection status but the research year along with the interaction genotypex maedi-visna and the number of reared lambs.

    The obtained research findings concerning milk yield and qualitative changes ofmilk produced imply the influence of some other factors that, among others, may berelated with the health status of the mammary gland. As many authors have proven [19,20,21,27], in the case of seropositive animals, mastitis is a concurrent disorder indu-cing milk production losses as high as 10%. The TOK test for mammary gland healthassessment revealed a substantively higher infection rate in the ewe group with MVV+than in the MVV- one. In the former group, TOK test gave positive results for one arboth halves of the udder at the lactation peak in 37% mothers and 19.6% ones in thesecond rnonth; while for healthy sheep (MVV-), there was recorded 10.3% in bothperiods (Fig. 1). Taking into account ani maI genotype, it was found that in the first

    % 40.--------------------------------------------------------,35+---

    30+---

    25+---

    20+---

    15+---

    10+---

    5+---

    I monthI miesiąc

    II monthII miesiąc

    IIIBryy+ Sll\lvv-I

    Fig. l. TOK-positive sheep from MYY+ and MYY- groupsRys. l. Dodatni wynik TOK u owiec MYY+ i MYY-

    month in the MVV+ sheep of meat-prolific line BCP, the positive test result wasrecorded in 35% of ewes and in SCP - 38.5%. In the following month, the percentagewas lower in sheep of both seropositive genotypes to reach 25% in BCP and 15.4% inSCP. A markedly lower infection rate in both months was determined in the seronega-tive sheep, that for the BCP line ewes was approximately 5.6% and for the SCP ones -18.2 and 27.3% (Fig. 2).

    McDougall et al. [15] report that the prediction of mastitis occurrence based onTOK test results is rather challenging and point to somatic celi counts (SCC) determinedin milk sampIes as a more accurate indicator of intramammary infection (IMI) rate.Olechnowicz et al. [18] state that physiological limit of SCC in ovine milk is associatedwith a breed and may range between 200 up to 400 000 SCC/ml. A notably lower celi

    56

  • %45r---------------------·------------------40+------------------------------------------------------------4

    15

    351~30~

    25 -

    20

    10

    5

    oImonthImiesiąc

    IImonthIImiesiąc

    II§lBCP MYY+ .SCPMVY+ [[JBCPMVY- I:'lSCP!\IYv-1

    Fig. 2. TOK positive result in relation to genotypeRys. 2. Dodatni wynik TOK w zależności od genotypu

    level was established in milk obtained from dairy breed ewes than in meat-type ones[7]. Some authors [4, 18,26] are of the opinion that ovine milk in which the SCC exceed500000 cells/ml is not acceptable as such milk sampies appeared to be four times morefrequently infected by pathogens as compared to milk with lower SCC.

    On the basis of the present researches (Tab. 3) it has been demonstrated that theSCC eontent in the first and second lactation period was on average 5.8 and 2.4 timehigher in milk from the MVV+ mothers and oscillated between 40 up to 25 703thousand/crn ' and 35 to 6625 thousand/cm ', respectively, as compared to milk obtainedfrom the MVV- mothers with the values between 33 to 2376 and 32 to 2342 thou-sand/cm '. The differences concerning the absolute number of somatic cells convertedinto natural logarithm SCC in the first research period were confirmed statistically.

    Taking into account sheep genotype, significantly higher somatic celI count eon-verted into logSCC in both periods was stated in milk of the seropositive ewes BCP(5.61 and 5.55) as against SCP (5.51 and 5.02). As for milk from the seronegative ewes,SCC logarithm was higher than in the SCP ewes (5.05 and 5.42) compared to the BCPones (4.70 and 4.39). The analysis shows that in both lactation periods, milk from theSCP ew es in the MVV- mothers contained more somatic cells than milk from theseronegative BCP and even outnumbered the values obtained for the seropositive BCPin II research period (Tab. 3). Occurring of significant interaction between genotypeand maedi implies that sheep of SCP line with genotype containing 25% Suffolk breedshow higher susceptibility to MVV infection and thus, are more prone to subclinicalmastitis as compared to sheep BCP. This fact is consistent with the studies of Kędziora

    57

  • Table 3 - Tabela 3Somatic cell count in milk of seropositive (MYY+) and seronegative (MYY-) ewes in relation to genotypeZawartość komórek somatycznych w mleku maciorek serododatnich (MYY+) i seroujemnych (MYY-) zuwzględnieniem genotypu

    MYY+ MYY-

    GenotypeGenotyp

    somatie cellskomórki somatyczne

    somatic cellskomórki somatyczne

    thousand/crrr' logSCCtys.zcrrr' logLKS

    thousand/crrr'tys.rcrrr'

    logSCClogLKS

    min - max s min - max

    First month of lactation - J miesiąc laktacji

    BCP 1888 40 - 25703 5.61 1.74 133 33 - 376 4.70 0.64

    SCP 1037 55 - 17087 5.51 1.29 456 38 - 2376 5.05 1.42

    Total 1415 40 - 25 703 5.56' 1.49 244 33 - 2376 4.82' 0.97Razem

    Second month of lactation - II miesiąc laktacji

    BCP 858 35 - 6625 5.55** 1.48 96 32 - 276 4.39** 0.60

    SCP 307 49 - 3514 5.02 0.95 488 56 - 2342 5.42 1.26

    Total 552 35 - 6625 5.26 1.23 231 32 - 2342 4.74 0.99Razem

    **P$O.OI; *P:O;O.05

    et al. [11] and Tietze et al. [27] who, having investigated many breeds and lines, provedhigher susceptibility of the Suffolk breed and populations developed with distributionof Suffolk genotype to any kind of infections.

    Summing up the present research findings, it has been found that the ew es infectedby maedi-visna virus produced slightly less milk of higher fat and protein eontent butlower lactose concentration compared to the milk from ewes free from MV virus.Variation of qualitative and quantitative traits was dependent on the lactation period.The ew es from MVV + gro up showed elevated susceptibility to subclinical mastitisincidence. That was confirmed by the TOK test results as well as a high level, frequentlyexceeding the physiological norm of 500 000 SCC/cm3 of somatic cell counts in milkas against the milk from seronegative mothers. The present authors believe that theresearch results presented are attributable to numerous factors, in that the health statusof animals. However, it seems impossible to prove correct the hypothesis of the directinfluence of MV virus on alevel of features associated with milk yield and the mam-mary gland health. Far more justified seems to be the hypothesis about the indirect effectof the MVV infection on the features connected with ovine milk yield as it is alsoconsistent with the results presented by Peterhans et al. [21] and Dungu et al. [6].

    58

    s

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