Effect of somatic cell count level on functional longevity in Valle del Belice dairy sheep assessed using survival analysis
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1 J. Dairy Sci. 9 : doi: /jd American Dairy Science Aociation, 009. Effect of omatic cell count level on functional longevity in Valle del Belice dairy heep aeed uing urvival analyi V. Riggio,* 1 D. O. Maizon,* B. Portolano,* H. Bovenhui, and J. A. M. van Arendonk * Dipartimento S.En.Fi.Mi.Zo. Sezione Produzioni Animali, Univerità degli Studi di Palermo, Viale delle Scienze Parco d Orlean, 9018 Palermo, Italy Animal Breeding and Genomic Centre, Wageningen Univerity, PO Box 338, 6700 AH Wageningen, the Netherland Intituto Nacional de Tecnología Agropecuaria, EEA Anguil, CC 11, 636 La Pampa, Argentina ABSTRACT The objective of thi tudy were to evaluate the effect of omatic cell count (SCC) on functional longevity and to etimate the heritability of functional longevity uing urvival analyi in Valle del Belice dairy heep. A total of 4,880 lactation of,190 ewe from 11 flock were ued. In thi tudy, SCC wa conidered a an indication of ubclinical matiti. In cae of clinical cae, identified by the technician at milking time, tet-day weight and milk ample of thoe ewe were not conidered. Somatic cell were analyzed a count, without any tranformation, and were grouped in 3 clae baed on the oberved SCC maximum (mxscc). The mxscc clae, expreed a 10 3 cell/ml, were claified a 1 if mxscc 500, if 500 < mxscc < 1,000, and 3 if mx- SCC 1,000. An increae in SCC wa aociated with an increaed hazard of being culled. Ewe in the highet cla of SCC on a tet-day had a 0% higher hazard of being culled than thoe in the lowet cla. Therefore, SCC played a role in culling deciion of Valle del Belice dairy heep farmer. The heritability etimate for functional longevity wa 7% on the logarithmic cale and 11% on the real cale, indicating that election for thi trait i poible in heep. The flock-year-eaon effect explained 19% of the variation on the logarithmic cale and 7% of the variation on the real cale. Key word: omatic cell count, longevity, urvival analyi, dairy heep INTRODUCTION Intramammary infection are the primary caue of matiti in dairy ewe and cow. Matiti lead to economic loe, mainly ariing from dicarded milk, reduced milk production and quality, and increaed health care cot both in dairy ewe (Leitner et al., 004) and cow (e.g., Wellenger et al., 00). Albenzio Received April 30, 008. Accepted September 8, Correponding author: vriggio@unipa.it et al. (00) reported a reduction in fat and caein content in ewe infected by matiti. Almot all heep milk i proceed into cheee; thu, any change in caein content would have a ubtantial effect on the indutrial value of the milk. Legarra et al. (007) reported that increaed uceptibility to matiti i one of the reaon for culling in heep. However, little information i available about the relationhip between longevity and both clinical and ubclinical matiti in heep. Bergonier and Berthelot (003) reported that annual incidence of clinical matiti in heep i generally le than 5%, wherea the prevalence of ubclinical matiti range from le than 10 to more than 50%. Barillet et al. (001) reported a 5% frequency of culling for clinical matiti and a 9.7% frequency for ubclinical matiti a predicted by SCC. In cattle, the incidence of matiti ha an important effect on culling deciion (e.g., Neerhof et al., 000), particularly matiti that occur before the time of peak milk yield (Beaudeau et al., 1994). Antagonitic genetic correlation for longevity with matiti reitance, ranging from 0. to 0.53, were found in dairy cow (Nielen and Pederen, 1995; Mrode et al., 000; Roxtröm and Strandberg, 00). Matiti caue an increae in SCC in mall ruminant (Zeng et al., 1997; Leitner et al., 004) and cattle (e.g., Heringtad et al., 006). Moreover, matiti data are difficult and expenive to collect, wherea SCC i currently recorded in everal milk recording cheme in both dairy heep (Atruc et al., 004) and cattle (Boettcher, 005). Therefore, SCC i promoted a an indirect method of predicting mammary infection and a a election criterion to improve matiti reitance (Heringtad et al., 000; Barillet, 007). However, Legarra et al. (007) conidered the meaure of SCC a an indicator of ubclinical matiti. Wherea clinical matiti i generally identified by evident ign, ubclinical matiti i uually inferred from SCC (Bergonier and Berthelot, 003). In dairy cattle, the effect of SCC on culling at the phenotypic level wa firt aeed by Beaudeau et al. (1995). Previou tudie, uing urvival analyi, 6160
2 SOMATIC CELL COUNT AND LONGEVITY IN SHEEP 6161 reported that higher concentration of SCC were aociated with higher rate of culling (Samoré et al., 003; Caraviello et al., 005). Antagonitic genetic correlation between SCC and longevity, ranging from 0.16 to 0.36, have been reported for dairy cow (Nielen and Pederen, 1995; Mrode et al., 000; Roxtröm and Strandberg, 00), indicating that elevated SCC i aociated with reduced longevity. However, information regarding the relationhip between SCC and functional longevity i lacking in heep. Legarra et al. (007) uggeted that a much more detailed tudy on culling policie and relationhip between SCS, SCC, matiti, and urvival in dairy heep i needed. Longevity corrected for milk production level, functional longevity, i an approximate meaure for involuntary culling (Dekker, 1993). At preent, only a few etimate of heritability for longevity are available in dairy heep (Conington et al., 001; El-Saied et al., 005). The objective of thi tudy were to evaluate the effect of SCC a an indirect meaure of ubclinical matiti on functional longevity, and to etimate the heritability of functional longevity in Valle del Belice dairy ewe. longevity for a given ewe wa partitioned into lactation period; conequently, all record began with a lambing. In cae where ewe were not culled during a pecific lactation period, record were treated a right cenored. Ewe were conidered culled, and therefore record were conidered uncenored, if the lat tet-day reported wa at leat 6 mo before the end of the obervation period for each flock. The 6-mo period wa choen by conidering the interval between lambing and the poibility that a ewe wa in a dry period. Statitical Analyi The analyi wa performed with a urvival analyi (Ducrocq and Caella, 1996) uing the Survival Kit 3.0 et of program (Ducrocq and Sölkner, 1998a). A Weibull model, le computationally demanding compared with the Cox model, wa ued. The Weibull ditribution aumption wa checked by plotting ln[ lns(t)] againt ln(t), where S(t) wa the Kaplan-Meier etimate of the urvivor function, ln wa natural logarithm, and t wa the number of day from lambing within lactation. The following Weibull model wa ued: Data MATERIALS AND METHODS h ijlmnop (t) = h 0 (t) exp [l i (t) + op j + age l + mk m (t) + cc n (t) + fy o + p ], The original data et conited of 6,530 lactation of 3,19 ewe. Data for SCC were collected at approximately 1-mo interval by the Univerity of Palermo (Italy) in 17 Valle del Belice flock between 1998 and 006; SCC wa meaured only when ewe were free of clinical matiti. The Valle del Belice breed i the mot productive autochthonou breed reared in Sicily. At milking time, cae of clinical matiti were identified by the technician and tet-day weight and milk ample of thoe ewe were not conidered. Clinical matiti wa reported for the evident ign of udder inflammation, or abnormal milk, or both. Mot cae of matiti were confirmed by a veterinarian. Record were excluded when SCC information wa miing, ewe had miing ire identification, or ewe were ired by ram with fewer than 4 female offpring. Moreover, record were left out when the age at firt lambing wa not in the range of 10 to 30 mo and when they were from flock with obervation for a period of le than yr. After editing, the data et conited of 4,880 lactation record from,190 ewe reared in 11 flock. The average number of SCC tet-day wa 3.5 per lactation. The repone variable wa the productive life defined on a lactation bai, either from one lambing to the next or to culling, whichever came firt, in accordance with Roxtröm et al. (003). In thi analyi, the overall where h ijlmnop (t) wa the hazard of culling for a given ewe at time t, being t day from lambing within a lactation; h 0 (t) wa the Weibull baeline hazard function, with cale parameter λ and hape parameter ρ; l i (t) wa the time-dependent fixed effect of the ith tage of lactation. Five clae were defined a 1 when 0 < DIM 60, when 60 < DIM 10, 3 when 10 < DIM 180, 4 when 180 < DIM 50, and 5 when DIM > 50. The tage of lactation effect wa included to account for change in the culling hazard within lactation. op j wa the time-independent fixed effect of the jth parity, with j = 1,,5. age l wa the time-independent fixed effect of the lth age at firt lambing cla, where l = 1 when firt lambing occurred at 10 to 18 mo of age, at 19 to 3 mo of age, and 3 at 4 to 30 mo of age. When the information about the age at firt lambing wa mied, uch a when ewe were recorded from a econd or later lactation, the age at firt lambing wa approximated by conidering a fixed interval between paritie equal to 365 d. mk m (t) wa the time-dependent fixed effect of the mth cla for average daily milk production, expreed a milk deviation (milk_dev) from the mean and tandardized by the correponding tandard deviation within tage of lactation and flock. The milk deviation were aumed to be piecewie contant from the beginning to the end of a given tage of lacta-
3 616 RIGGIO ET AL. tion. Three clae were conidered: m = 1 if milk_dev < 1, m = if 1 < milk_dev 1, and m = 3 if milk_dev > 1. cc n (t) wa the time-dependent fixed effect of the nth cla, baed on the oberved SCC maximum (mxscc) within a tage of lactation; it wa aumed to be piecewie contant from the beginning to the end of a given tage of lactation. The mxscc clae, expreed a 10 3 cell/ml, were claified a 1 if mxscc 500 (with 3,690 record), if 500 < mxscc <1000 (with 1,409 record), and 3 if mxscc 1000 (with,867 record). Threhold for SCC clae were choen according to Bergonier et al. (1994) and baed on the evidence provided by other author that healthy heep normally have higher SCC than cow (e.g., Fthenaki et al., 1991). fy o wa the time-independent random effect of the oth flock-year-eaon of the lambing ubcla, with o = 1,,166 from up to 11 flock in 9 yr of lambing, conidering 3 lambing eaon. The lambing eaon wa equal to 1 when lambing occurred from Augut to November, equal to from December to March, and equal to 3 from April to July (Portolano et al., 007). A fy cla wa included in the analyi if there were at leat 4 record within it. The fy effect were aumed to follow a log-gamma ditribution with parameter γ. p wa the time-independent random effect of ire (p = 1,,168), aumed to be ditributed a a multivariate normal with mean vector 0 and covariance matrix Aσ, where A wa the additive relationhip matrix among ire. A ire model wa ued. Heritability wa etimated a (Ducrocq and Caella, 1996) hˆlog 4σ = ψ( γ)+ σ +, π where ψ(γ) i the trigamma function evaluated at the etimated marginal poterior mode of the variance of the flock-year-eaon effect and π i the pi contant. The effective heritability wa etimated a (Yazdi et al., 00) ĥ eff 4σ σ 6 = ( ) + +1 ψ γ Standard error for the effective heritability wa approximated (equation.8 in Roff, 1997). By replacing the numerator 4σ with ψ(γ), we etimated the proportion of the total variation, explained by the flock-yeareaon effect, on both logarithmic and real cale.. Table 1. Chi-quared (χ ) 1 tet baed on likelihood ratio tet for all effect in the model Effect in the model df χ P-value Stage of lactation < Parity < Age at firt lambing Daily milk production 11.5 < Maximum SCC Flock-year-eaon < Sire < Chi-quared i a likelihood ratio tet; that i, the difference between the log(likelihood) for the reduced model (without the effect teted) and the log(likelihood) for the full model. RESULTS Longevity for a given ewe wa partitioned into lactation and, by conequence, about 76.4% of the record were right cenored. The average lactation length, conidering the entire data et (culled and not culled animal), wa 171 ± 7 d wherea the lactation length of animal that were not culled wa 50 ± 35 d. The daily average of milk yield wa 1,310 g wherea the average tet-day SCC wa 1, cell/ml. The fitted model explained approximately 50% of the total variation in the repone variable. The hape parameter ρ wa equal to 1.33, indicating that a time increaed within lactation, o did the hazard of culling. The plot ued to check the Weibull ditribution aumption, ln[ lns(t)] veru ln(t), howed a traight line (reult not hown), an indication that thi aumption wa valid. Chi-quare tet approximation baed on likelihood ratio tet were calculated for all the effect in the model (Table 1). The ignificance of each effect reulted from the correponding P-value. Etimate of time-independent fixed effect indicated that ewe at econd lambing were at a lower hazard of being culled than ewe at firt lambing (Table ). Relatively more culling in firt parturition might be explained by culling for low production or culling for lambing difficultie, epecially for ewe having the firt lambing at an early age. Moreover, ewe at the fourth or greater lambing were at a higher hazard than ewe at the firt lambing. The effect of age at firt lambing reulted, in general, in an increae in culling rate with age. Table 3 how the etimate of time-dependent fixed effect. The etimate for the firt to fourth clae of tage of lactation were ignificantly different from 1, indicating that ewe in thee clae were at a higher hazard of being culled than thoe in the fifth cla, the reference level. Ewe in the firt and econd clae of milk production were at a higher hazard of being culled than thoe in the third (reference) cla with greatet
4 SOMATIC CELL COUNT AND LONGEVITY IN SHEEP 6163 Table. Mode () ˆb and tandard deviation ( σˆˆ b ) of the marginal poterior ditribution, hazard ratio ( ĥ ) baed on poterior mode, and 95% confidence interval (CI) for ĥ with lower and upper bound for the timeindependent fixed effect, etimated with the model including SCC Effect 1 Cla ˆb σˆˆ b ĥ 95% CI for ĥ Lower Upper Parity Age at firt lambing Parity = 1 and age at firt lambing = 1 were ued a reference level. milk yield. Regarding SCC, ewe in the econd and third clae were at a higher hazard of being culled than thoe in the firt cla with the leat SCC. Table 4 how the etimate for the time-independent random effect, heritabilitie for productive life, and proportion of variation explained by the flock-yeareaon effect obtained with the Weibull model. The heritability of productive life wa 0.07 on the logarithmic cale and 0.11 on the real cale. The proportion of variation in productive life explained by the flock-yeareaon effect wa 0.19 on the logarithmic cale and 0.7 on the real cale. DISCUSSION Prognotic factor particularly SCC, which erve a an indirect meaure of ubclinical matiti affected productive life in Valle del Belice ewe. To our knowledge, thi i the firt uch finding in heep, uing urvival analyi. Therefore, reult were motly compared with thoe reported for dairy cattle. A lactation bai approach wa choen becaue it better uited our data, which were collected on farm during different period. Roxtröm et al. (003) did not report major difference between longevity analyzed on a lactation bai and longevity baed on the entire length of life. The effect of age at firt lambing reulted, overall, in an increae in culling rate with age. It i not convenient for a farmer to keep animal that are going to lamb for the firt time at an advanced age. Thi reult wa in agreement with the reult reported by Samoré et al. (003) in dairy cattle. However, Chirino et al. (007) reported that age at firt calving did not affect the hazard of culling in the Spanih Holtein-Frieian cattle population. The effect of tage of lactation wa included in the model becaue it allowed for better modeling of the baeline hazard and ha an important factor affecting Table 3. Mode () ˆb and tandard deviation ( σˆˆ b ) of the marginal poterior ditribution, hazard ratio ( ĥ ) baed on poterior mode, and 95% confidence interval (CI) for ĥ with lower and upper bound for the timedependent fixed effect, etimated with the model including SCC Effect 1 Cla ˆb σˆˆ b ĥ 95% CI for ĥ Lower Upper Stage of lactation Daily milk production Maximum SCC Stage of lactation = 5, daily milk production = 3, and maximum SCC = 1 were ued a reference level.
5 6164 RIGGIO ET AL. Table 4. Mean (±SD) and mode of the random effect in the model, heritabilitie for the productive life on logarithmic h ˆlog ( ) and real ( ĥ eff ) cale, tandard error of ĥeff, and proportion of variation ( ) and real explained by flock-year-eaon effect on logarithmic Pfy log ( Pfy eff ) cale Item Mean (±SD) σ ire Mean (±SD) σ fy Mode σ ire Mode σ fy Value (±0.06) (±0.67) hˆlog 0.07 ĥ eff 0.11 SE ( ĥeff ) 0.05 Pfy log 0.19 Pfy eff 0.7 culling. Ewe in middle lactation (i.e., d) had a higher hazard of being culled compared with thoe in late lactation. When referring only to culling becaue of matiti, a review by Bergonier et al. (003) howed that in heep, the majority of cae of matiti occur during the firt third of lactation. In dairy cattle, Beaudeau et al. (1995) and Roxtröm et al. (003) reported an increaed hazard of culling in early lactation. The etimate for the clae of daily milk production howed that ewe with a level of production below the flock average had a higher hazard of being culled, in agreement with reearch reult in cattle (e.g., Vukainovic et al., 001; Chirino et al., 007). Ewe with a maximum SCC between 500 and 1,000 or 1, cell/ml in a tage of lactation had a lightly higher hazard of being culled than ewe with leer maximum. Thee etimate were in the ame direction a thoe reported by Beaudeau et al. (1995) in dairy cow, with a range of 1.7 from the highet to lowet cla for SCC, wherea they were much lower than thoe reported by Samoré et al. (003). Samoré et al. (003) conidered SCS intead of SCC, reporting a 3-fold higher rate of culling for cow with tet-day in the highet clae of SCS. However, uing SCC or SCS i equivalent when clae are ued. The tranformation of SCC into SCS, therefore, would not have changed thee clae becaue the particular tranformation that i ued to go from SCC to SCS i a one-to-one function. The rik aociated with SCC level etimated in thi tudy wa le and might be explained by the fact that mot Valle del Belice farmer do not directly ue SCC information to make culling deciion for animal. In heep, the current milk payment ytem of mot countrie i baed only on milk yield and not on SCC level, which i different from the cattle indutry. However, Valle del Belice heep milk i mainly ued for producing raw-milk traditional cheee (Pecorino and Vatedda del Belice cheee) either by farm, mall local dairie, or cheee indutrie working at the regional level. Therefore, an indirect effect of SCC on culling can be conidered becaue SCC ha a remarkable influence on the bulk milk compoition and lactodynamographic parameter of Valle del Belice heep (Giaccone et al., 005). Moreover, the genetic correlation between milk production trait (milk yield and fat and protein yield and content) and SCS level in Valle del Belice heep are poitive, ranging from 0.16 to 0.31 (Riggio et al., 007). However, Bufano et al. (1994) howed that high SCC (>1 million/ml) do occur in normal heep milk, epecially toward the end of lactation, wherea Bergonier et al. (003) howed that nonpathological factor are reponible for variation of SCC in ewe milk between and cell/ml. Conidering SCC a an indicator of ubclinical matiti, thee reult may be compared with tudie analyzing the rate of culling directly aociated with matiti incidence. Beaudeau et al. (1995) found that udder health diorder were alway highly related to an increae in culling rate in dairy cow. Legarra et al. (007), in a tudy to derive the economic value of SCS in dairy heep, reported that SCS had an effect on culling deciion. In the preent tudy, the economic weight of culling wa conidered indirectly baed on the genetic correlation between SCS level and the culling becaue of ubclinical matiti. A genetic increae of 1 unit of SCS increae the trait culled by matiti in 0.1 time the genetic correlation. The flock-year-eaon effect wa an important factor explaining the oberved variation in productive life. Thi reult wa in agreement with the reult from other tudie on Valle del Belice heep (Portolano et al., 007; Riggio et al., 007), confirming the importance of thi factor. Milking practice might be an important factor in influencing udder health. In Sicily, only a few farmer ue a milking machine; mot farmer milk ewe by hand. It i not common for farmer to wah ewe udder or their hand before milking. Moreover, antibiotic dry therapy i not implemented on all farm. Thi variability i reflected in different hygiene condition among farm, which can influence milk quality. Literature concerning heep report heritability etimate for functional longevity omewhat lower than thoe preented in thi tudy. El-Saied et al. (005)
6 SOMATIC CELL COUNT AND LONGEVITY IN SHEEP 6165 reported a heritability of 0.05 for functional longevity in the Churra breed. Similar etimate of heritability for longevity, meaured a day or year in the flock, were reported in the literature for meat breed [0.06 for Autralian Doret heep (Brah et al., 1994) and 0.08 for Scottih Blackface (Conington et al., 001)]. The heritability etimated for functional longevity in thi tudy wa higher than etimate reported by Chirino et al. (007) in cattle, ranging between 0.05 and 0.07, wherea Neerhof et al. (000) and Ducrocq and Sölkner (1998b) reported heritabilitie around 0.05 for the logarithmic cale and 0. for the real cale. CONCLUSIONS An increae in SCC a an indicator of ubclinical matiti wa aociated with an increae in rate of culling. Therefore, elevated SCC ariing from ubclinical matiti played an indirect role in the culling deciion of Valle del Belice dairy heep farmer although, at preent, they do not elect directly to reduce SCC. The proportion of additive genetic variation etimated for functional longevity in Valle del Belice ewe indicate that it may be poible to improve productive life by genetic election. The conitent flock-year-eaon effect etimated confirm the high variability in management of the Valle del Belice breed. ACKNOWLEDGMENTS The author acknowledge the Minitero delle Politiche Agricole Alimentari e Foretali (MiPAAF) (D.M. 30/7303/05), Aeorato Indutria della Regione Siciliana Serv. 3 (DRS 359/005), and Aeorato Agricoltura e Forete della Regione Siciliana (DDG n. 158/006) for financial upport for thi reearch. The project funded by Minitero dell Itruzione, dell Univerità e della Ricerca, project #007898KYN (PRIN 007) i alo acknowledged. The econd author had an experienced reearcher poition within a Marie Curie European Tranfer of Knowledge Development project with contract number MTKD/I- CT REFERENCES Albenzio, M., L. Taibi, A. Mucio, and A. Sevi. 00. 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