Management practices associated with udder health of first-parity dairy cows in early lactation

Preventive Veterinary Medicine 88 (2009) 138–149

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Management practices associated with udder health of first-parity dairy cows in early lactation A.-K. Nyman a,b,*, U. Emanuelson c, A.H. Gustafsson b, K. Persson Waller a,c a

Department of Animal Health and Antimicrobial Strategies, National Veterinary Institute, SE-751 89 Uppsala, Sweden Swedish Dairy Association, P.O. Box 7019, SE-750 07 Uppsala, Sweden c Department of Clinical Sciences, Swedish University of Agricultural Sciences, P.O. Box 7054, SE-750 07 Uppsala, Sweden b

A R T I C L E I N F O

A B S T R A C T

Article history: Received 17 July 2007 Received in revised form 22 August 2008 Accepted 28 August 2008

This study aimed at investigating associations between management routines including feeding, housing, and milking around calving, and udder health of first-parity cows in early lactation in Swedish large, high producing, low bulk-milk somatic cell count (SCC) dairy herds housed in free stalls. Seventy-two dairy herds participated and data concerning 1189 first-parity cows calving during the study period (October 2005–January 2006) was collected. Multivariable regression analysis were performed with three different outcomes; within-herd number of first-parity cows veterinary treated for clinical mastitis at days 10 to 60 after calving, within-herd number of first-parity cows with a SCC  200,000 cells/mL at first test-day, and SCC of first-parity cows at first test-day. Cow factors significantly associated with good udder health of first-parity cows (few cases of clinical mastitis and or low SCC) were being of the Swedish Red breed, having a high milk yield at first test-day, and a milk-urea 5 mmol/L at first test-day. Herd factors significantly associated with good udder health were having mattresses as flooring in the cubicles in the lactating cow housing, and to house the first-parity cows in tie stalls 1 month before calving. Cow factors significantly associated with poor udder health of firstparity cows were having a milk-urea <4 mmol/L at first test-day. Herd factors significantly associated with poor udder health of first-parity cows were feeding first-parity cows sugar-beet pulp or corn silage, and to give silage from a different batch to pregnant heifers than to lactating cows. Moreover, to have sawdust or shavings in the calving pen, to be moved from the calving pen 2 days after calving, to milk first-parity cows at the calving site instead of in the parlor, and to rinse, clean or disinfect milking units before a firstparity cow was milked were also significantly associated with poor udder health of firstparity cows. The results indicate that different control measures must be taken depending on the nature of the udder health problem. ß 2008 Elsevier B.V. All rights reserved.

Keywords: First-parity dairy cow Early lactation Clinical mastitis SCC Management factors

1. Introduction Udder health of cows can be measured in different ways, e.g. by measuring the somatic cell count (SCC) as an

* Corresponding author at: Department of Animal Health and Antimicrobial Strategies, National Veterinary Institute, SE-751 89 Uppsala, Sweden. Tel.: +46 18 67 40 98; fax: +46 18 30 91 62. E-mail address: [email protected] (A.-K. Nyman). 0167-5877/$ – see front matter ß 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.prevetmed.2008.08.005

indicator of inflammatory response, by calculating the prevalence or incidence of minor and major pathogens as an indicator of intra-mammary infection (IMI), or by calculating the incidence of clinical mastitis (CM). These measurements represent different aspects of udder health, and factors, both at herd and animal level, associated with elevated SCC differ from those associated with increased incidence of CM (Bakken, 1982; Barkema et al., 1998a,b; Svensson et al., 2006). Thus, herds with low bulk-milk SCC (BMSCC) can still have a high incidence of CM (Schukken

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et al., 1990; Peeler et al., 2002; Nyman et al., 2007). There are also reasons to believe that different factors are associated with udder health at different stages of lactation, and in first-parity cows compared to older cows, but information on this is scarce. The udder health in the first month after calving has a major impact on the udder health during the rest of lactation. Most cases of CM occur in the first month of lactation (Barkema et al., 1998b; Svensson et al., 2006) and first-parity cows have been shown to have a higher incidence of CM in early lactation than older cows (Barkema et al., 1998b; Valde et al., 2004; Nyman et al., 2007). Occurrence of CM in early lactation increases the risk of mastitis later in lactation (Edinger et al., 1999; van Dorp et al., 1999), and elevated SCC in early lactation often results in elevated SCC throughout the whole lactation (De Vliegher et al., 2004a). In the period around calving, the first-parity cow experiences a number of physiological changes related to calving and the onset of lactation. In addition, the firstparity cow must adapt to changes in housing, feeding, management, and to milking. As an example, pregnant heifers are often housed in a different building and housing system than the lactating cow. The animal is in extreme cases moved multiple times in the period around calving, e.g. from one housing system in late pregnancy to a precalving system, followed by the calving area, a post-calving pen or group, and finally the lactating cow housing. Such changes can be stressful for the animal, and may negatively influence their immune defense and thereby increasing the risk of udder infections (Mallard et al., 1998). Effects of management, including housing and feeding, of first-parity cows before, at and after calving, on udder health in early lactation have, however, not been studied in great detail. Only a few management factors associated with the udder health of first-parity cows have been identified. Myllys and Rautala (1995) and Svensson et al. (2006) identified associations between concentrate feeding and udder health of first-parity cows, while Waage et al. (1998) identified an association with roughage feeding, heifers being on pasture or not, and udder health. Moving heifers from pasture to confined housing the day of calving and use of restraint measures at milking have also been shown to be associated with udder health of firstparity cows (Svensson et al., 2006). That feeding seems important for the udder health of first-parity cows is also shown by Compton et al. (2007) and Nyman et al. (2008), which both found associations between blood serum concentration of different metabolites and udder health of first-parity cows. Several other individual animal risk factors have been identified, e.g. difficult calving, udder injuries, udder edema, milk production, SCC, and breed (Oltenacu and Ekesbo, 1994; Slettbakk et al., 1995; Myllys and Rautala, 1995; Waage et al., 2001; Barnouin and Chassagne, 2001; Svensson et al., 2006; Compton et al., 2007). Thus, the knowledge of individual animal risk factors associated with udder health of first-parity cows is plentiful, while more research is needed to identify important management factors associated with udder health in this period. The aim of this study was therefore to investigate associations between management routines

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including feeding, housing, and milking around calving, and udder health of first parity-cows in early lactation in high producing, low BMSCC Swedish dairy herds with 80 cows housed in free stalls. This type of herd was selected as it represents the future trend in Swedish dairy farming. 2. Materials and methods 2.1. Herds Herds were selected using data obtained from the official Swedish milk-recording scheme (SOMRS) and the animal disease-recording scheme (SADRS). Through the SOMRS and the SADRS, information is available on milk production and cow health for approximately 79% of the Swedish dairy herds and 86% of the Swedish dairy cows. Herds were selected in February 2005 based on data from September 2002 to August 2004. To minimize the effect of random fluctuations and to improve reproducibility of the data the selection of herds was based on the arithmetic means of the selection criteria for two consecutive 12month periods. The selection criteria were: to have lactating cows in free stall (3 years before the years of selection), to have a herd size of 80 cows, to be a herd with a BMSCC below the Swedish average (<192,000 cells/ mL (geometric mean)), and to be a herd with a milk production above the Swedish average (>8894 kg of milk/ year) during the selection period (Swedish Dairy Association, 2006a,b). The average herd size in Sweden during the time of selection was 46 cows, and approximately 12% of the 7285 dairy herds enrolled in the SOMRS during this period had a herd size 80 cows. Approximately 16% of the 7285 dairy herds enrolled in the SOMRS housed their lactating cows in free stalls (Swedish Dairy Association, 2006b). Of the selection parameters milk production was calculated as an average of the sum of kg of milk per year divided by the average number of cows. The BMSCC was calculated as an average of the geometric mean BMSCC of the two-selection year’s consecutive monthly test-days, and the herd size was calculated as average number of cows in the herd during the selection years. Herds fitting the selection criteria but owned by a university, school or commercial company were excluded from further selection (n = 7). All farmers of the remaining herds fitting the selection criteria (n = 105) received a letter describing the study. Herds were contacted by phone according to a random order (using a random-number generator) 2 weeks after the initial letter was sent. At this time information was retrieved from the farmer on the number of heifers estimated to calve during October 2005– January 2006. If the herd had at least 5 such heifers the farmer was asked to participate in the study. When 80 farmers had accepted no more were contacted (18 of the contacted farmers could not or did not want to participate). The sample size was set to 80 herds for practical and economic reasons, but due to dropouts only 78 herds participated in the study. Each participating herd was visited once by personnel from the local livestock organization between 15 October 2005 and 15 February 2006. The two main investigators (A.-K. Nyman and K.

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Persson Waller) personally informed and trained the feedadvisors about the study and procedures to be performed on farm. 2.2. Collection of data The observation period was from 1 October 2005 to 31 March 2006, but animal data was collected only for heifers calving between 15 October 2005 and 15 January 2006. For these animals information about calving date, difficulties at calving, age at calving, veterinary-treated diseases (clinical mastitis, retained placenta, etc.), breed, and production (milk, fat, protein, milk-urea and cow composite SCC at monthly test-days) for the observation period were collected from the SOMRS and SADRS. The observation period per animal was from 10 days before to 2 months after calving. In Sweden, only veterinarians are allowed to start an antibiotic treatment of a disease and every treatment should be reported to the SADRS, which is administered by the Swedish Board of Agriculture and linked to the SOMRS. Herd values of average milk production, incidence of animals with a consecutive low (<131,000 cells/mL at three consecutive test-days) or high SCC (>300,000 cells/mL at three consecutive test-days) in the herds, breed composition, percentage of first-parity cows, and herd size was also collected from the SOMRS for the year 1 September 2005–31 August 2006. There are two main dairy breeds in Sweden, the Swedish Red breed (SR) and the Swedish Holstein breed (SH). A herd comprising of 80% of one breed was considered a SR-herd or SH-herd. If the herd comprised of <80% of each breed, it was considered a SH/SR herd. On the individual level, cross-bred cows (SH/SR-breed) were categorized as to be of SR-breed due to the small number of cross-bred animals and that there were fewer animals of the SR-breed than of the SH-breed. 2.3. Questionnaire Personnel from the local livestock organization interviewed the farmer about management routines, including housing, milking, and feeding of first-parity cows 1 month before calving, at calving (3 days) and 1 month after calving (a total of 166 questions). The farmer freely answered the questions, which mostly were semi-closed with space available for the interviewer to make notes if alternatives to the options were given. Efforts were taken to not give too much aid if the farmer had difficulties in answering the questions in order to not influence the response. Each interview took approximately 1.5 h to complete. The questionnaire was based on questionnaires used in previous field studies (Svensson et al., 2006; Nyman et al., 2007). 2.4. Feed samples At their visit to the farm, the person from the local livestock organization took grass-silage and grain samples from the feed given to first parity-cows at 3 days around calving. Samples were taken by collecting material from at least 10 different areas of each of the silage (only opened silage storages) and grain storage areas. The composite

samples were immediately sent by mail to the Department of Feed, National Veterinary Institute, Uppsala, Sweden, for analysis within 36 h. The silage was analyzed for pH, DM, and mould, bacteria and yeast contents, while the grain was analyzed for water activity, and mould, bacteria and yeast contents according to accredited methods. 2.5. Statistical analysis Three different outcomes were used to assess the udder health: the within-herd number of first-parity cows that were veterinary treated for clinical mastitis (VTCM) in the period 10 to 60 days after calving, the within-herd number of first-parity cows with a SCC  200,000 cells/mL at first test-day, and the SCC at first test-day (transformed using the natural logarithm to LnSCC). Poisson-regression analyses was used to study variables at herd level for the two first outcomes, while hierarchical linear-regression analysis, with herd as random factor, was used to study variables both at herd level and at the individual cow level for the third outcome. In the Poisson-regression analysis of the first outcome the natural log of the sum of numbers of days at risk (number of days each first-parity cows participated in the study until end of study, culling or to first case of clinical mastitis) for all first-parity cows included in the study per herd was used as offset. For the second outcome the natural log of the total numbers of first-parity cows at the first testday in each herd was used as offset. Associations between the dependent variable and each of the variables were first screened in univariable Poisson or linear regression analysis. Variables with a P-value  0.20, provided that there was no collinearity (r < 0.70) between variables, were then considered for further analysis. Collinearity between variables was assessed pair-wise by calculation of Spearman rank correlations. Continuous variables not linearly related to the outcome, were categorized using the quartiles as cut-points, or by using biologically important, or recommended cutpoints. Variables with many missing values (>20% missing observations) were not used in the multivariable analysis. Categories of categorical variables with too few observations were amalgamated when biological, or logical, new categories were possible to make. In other cases such categorical variables were not used in the analysis. Due to their large number, the variables were arranged in four groups of variables: feed and feeding, herd and cow data, housing, and milking. A general overview of the variables in the four groups is presented in Table 1. A full list of all variables is available from the corresponding author upon request. Multivariable models, one for each group of variables, were constructed using manual stepwise forward regression analysis, where variables not significant in the model were re-entered whenever a new variable became significant, or a variable was removed. Potential confounders were considered in every model. A variable was considered as a confounder if the point estimates of the coefficients in a model changed >20% with the potential confounder present. To remain in the sub-models variables had to have a P-value  0.10 in the likelihood ratio x2-test. A final model was then constructed where variables

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Table 1 Overview of variables, divided into four subject-oriented groups, used to find associations with udder health of first parity-cows in 72 dairy herds with average herd size of 149 cows, milk production of 10,090 kg of milk, and BMSCC of 191,000 cells/mL, housed in free stalls (Sweden, 2005–2006) Examples of variables

Total number of variables

Feed and feeding Feeding plans, amounts of concentrates and roughages given, type of feed given, silage hygiene, mineral and vitamin administration, cleaning routines of feed alleys, feed blenders, and concentrate feeding stations

99

Herd and cow data Milk production, herd size, proportion first-parity cows, breed, age at calving, health disorders during the study period, milk composition at first test-day

22

Housing Stall type, floor characteristics, type of bedding, cleaning routines, number of changes of stall/flooring, grouping

26

Milking Adaptation to milking, teat dipping, restraining, milking order

16

Total

significant in the final sub-models were included by stepwise forward selection. A variable with a Pvalue  0.05 was considered statistically significant and retained in the model. Biologically plausible interactions between the main effects were tested in all final models. To adjust for differences in SCC due to the effect of calving and onset of lactation the linear and quadratic terms of DIM was used as adjusting factor in the hierarchical linear-regression models. Intra class correlation (ICC; r) was calculated from the variance components obtained from the final hierarchical linear regression model. The ICC was calculated as r ¼ s 2h =ðs 2h þ s 2 Þ, where s 2h is the variance component containing the variance between herds and s2 is the variance component containing the variance within the herds. Model validation was performed according to Dohoo et al. (2003). The fit of the Poisson-regression models was evaluated using deviance statistics (sum of squared deviance divided by the degrees of freedom). To assess normality of residuals, normal probability plots of deviance and Anscombe residual (Q–Q plot) were performed and visually examined. Influential points and outliers were identified by looking at Cook’s distance values, deviance and Pearson residuals. The linear regression model was evaluated by assessing the normality of residuals at herd level by plotting the BLUP against the linear prediction of the fixed part of the model, and a normal probability plot of the BLUP (Q–Q plot). The normality of residuals at cow level was assessed by looking at normal probability plots of the residuals and standardized residuals (Q–Q plot) as well as looking at the plot of standardized residuals against the fitted values. Data editing and all the statistical analyses were done using Stata Software (StataCorp., 2003; Stata Statistical Software: Release 8.0; College Station, TX, USA: StataCorp LP). 3. Results

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analyses. Two more herds were excluded from the analysis on VTCM since they did not have reliable records of VTCM (no possibility to confirm the present or lack of cases with the veterinarian). Thus, information from 70 herds was used in the analysis of factors associated with number of first-parity cows VTCM in the period 10 to 60 days after calving, while information from 72 herds was used in the analysis of factors associated with number of first-parity cows with a SCC of 200,000 cells/mL at first test-day. These herds, including a total of 1189 first-parity cows during the study period, were also used in the analysis on LnSCC at first test-day. 3.2. Descriptive data The arithmetic mean annual herd size, milk production, geometric mean BMSCC, and 95% confidence interval (CI) for the 72 herds were 149 cows (95% CI: 133–166 cows), 10,090 kg milk/cow-year (95% CI: 9890–10,290 kg milk/ cow-year), and 190,400 cells/mL (95% CI: 179,700– 201,500 cells/mL), respectively. Thirty-two herds were classified as SH-herds, 11 as SR-herds and 29 as SH/SRherd. On the individual level 718, 424 and 47 first-parity cows were of the SH-breed, SR-breed and SH/SR-breed, respectively. In total, 79 first-parity cows (6.9% of the 1150 first-parity cows (6–47 first-parity cows per herd) in the 70 herds contributing with VTCM data; range 0–5 cases/herd) from 41 herds had VTCM in the period 10 to 60 days after calving. This corresponds to an overall incidence rate of 0.10 cases per 100 cow-days (range 0–0.50 per herd). The highest incidence rate occurred during the first weeks after calving (Fig. 1). The geometric mean SCC at first test-day (occurring on average 20 days postpartum) was 64,300 cells/mL (95% CI: 60,100–68,600 cells/mL), and 175 first-parity cows (14.7% of the 1189 first-parity cows in the 72 herd contributing with SCC data; range 0–14 first-parity cows/ herd) from 58 herds had a SCC  200,000 cells/mL at first test-day.

3.1. Questionnaire 3.3. Feed samples All 78 participating farmers answered the on-farm interview, but 6 herds had fewer than 5 heifers calving during the study period and were excluded from all

Grass silage was used at all farms. The mean dry matter content of the grass silage samples was 31% (95% CI: 29–

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Fig. 1. Incidence rate of cases of veterinary-treated clinical mastitis per 5 day period from 10 to 60 days after calving in 1150 first parity-cows from 70 Swedish dairy herds (79 cases in 79 first-parity cows).

33%) and the mean pH was 4.2 (95% CI: 4.1–4.2). Growth of yeast and mould was observed in 69% and 72% of the grass silage samples, respectively. In 40% of all the grass silage samples Penicillium (P.) roqueforti was found. Grain was stored at 74% of the farms, and the mean dry matter content of the grain samples was 72% (95% CI: 70–74%). Growth of yeast and mould were observed in 94% and 92% of the grain samples, respectively. In 18% and 82% of all the grain samples Aspergillus spp. and Fusarium spp. was found, respectively. 3.4. Multivariable analyses A total of 152 herd-level and 11 cow-level variables were screened in the initial univariable analyses for associations with the three outcomes. In the analyses of factors associated with VTCM 32 variables had a P-value of 0.20, and a total of 9 remained in the sub-models (P < 0.10; Table 2). In the analyses of factors associated with SCC  200,000 cells/mL at first test-days 23 variables had a P-value of 0.20, and a total of 7 remained in the sub-models (P < 0.10; Table 3). In the analyses of factors associated with LnSCC at first test-day 27 variables had a P-value of 0.20, and a total of 11 remained in the sub-models (P < 0.10; Table 4). Due to the large number of variables no results from the univariable analysis are presented. Collinearity was found between some of the variables, and in those cases the variable which gave the best log likelihood in the univariable analysis was used. The variables remaining in the sub-models (Tables 2–4) were offered to the final Poisson or linear regression models. In the final multivariable analysis of factors associated with VTCM, five variables remained with a P  0.05 (Table 5). Thus, to feed first-parity cows sugarbeet pulp at calving and onwards, to give silage from a different batch to pregnant heifers than to lactating cows,

to have sawdust or shavings in the calving pen, and to milk first-parity cows at the calving site instead of in the parlor were associated with an increased number of VTCM. To house first-parity cows in tie stalls 1 month before calving was associated with a decreased number of VTCM. Three variables remained (P  0.05) in the final multivariable model of variables associated with SCC  200,000 cells/mL at first test-day (Table 6). To feed firstparity cows corn silage at calving and onwards, to milk first-parity cows at the calving site instead of in the parlor, and to rinse, clean or disinfect the milking units before a first-parity cow was milked were associated with an increased number of first-parity cows with SCC  200,000 cells/mL at first test-day. In the final multivariable analysis of variables associated with LnSCC at first test-day 6 main variables and one interaction term remained with a P  0.05 (Table 7). To give sugar-beet pulp at calving and onwards, to have a milk-urea <4 mmol/L at first test-day, and to be moved from the calving pen 2 days after calving were associated with increased LnSCC. To be of the SR-breed, to have a high milk yield at first test-day, to have a milk-urea 5 mmol/L at first test-day, and to have mattresses as flooring in the cubicles in the lactating cow housing were associated with decreased LnSCC of first parity-cows at first test-day. One interaction was significant; percentage of milk-fat at first test-day interacted with being VTCM before first test-day. First-parity cows VTCM had higher LnSCC at first test-day than those not VTCM independently of percentage of milkfat, but cows with a high percentage of milk-fat that had been VTCM had a higher LnSCC than cows with a low percentage of milk-fat that had been VTCM. 3.5. Model fit Overdispersion was not observed in the two Poisson models. The estimated overdispersion parameter from the

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Table 2 Variables considereda in the final multivariable Poisson-regression analysis of their association with number of first-parity cows veterinary treated for clinical mastitis (VTCM) in the period 10 to 60 from calving in 70 Swedish dairy-herds Variable

No. of herds

Within-herd proportion of first-parity cows VTCM (median)

Feed and feeding Amount of concentrates given at 1 month after calving 13.7 kg 23 12.1–13.7 kg 24 >12.1 kg 23

P-value

0.0 8.0 8.3

0.01

4.8 8.7

0.02

2.7 10.0

0.02

Herd data Months with most first-parity cows calving in the study period October–November 33 December–January 37

8.3 5.3

0.08

Housing Housing system 1 month before calving Free stall Tie stall

7.1 0.0

0.05

Flooring in stalls at 1 month before compared to 1 month after calving Same 46 Different 24

6.5 7.1

0.08

Type of bedding in calving area Straw Sawdust or shavings

58 12

6.2 8.8

0.03

53 17

6.3 10.5

0.02

6.3 10.6

0.03

Sugar-beet pulp given at calving and onwards No 40 Yes 30 Silage from a different batch given to pregnant heifers than to lactating cows No 35 Yes 35

Milking Milking site during the colostrum period In parlor At calving site

52 18

Use of post-milking teat disinfection in the colostrum period Yes 55 No 15 a

Exhibiting a significant association (P < 0.10) in the sub-models.

sample mean and variance were <0.001 for both the VTCM model and the 200,000 SCC model. The variance components of the final multivariable hierarchical regression model gave an ICC of 0.04. Thus, most of the variation was seen within the herds (between individuals in a herd), and not between herds. All final multivariable models showed reasonably good fit to the data, and no obvious patterns were seen in the residual plots. A few outliers were observed, but removing them did not improve the models. 4. Discussion In the present study we found several factors associated with early lactation udder-health of first-parity cows, and that those factors differed between various aspects of udder health. Only two variables; use of sugar-beet pulp at calving and onwards, and to be milked at the calving site, were associated with more than one of the outcomes (VTCM and LnSCC). This may be explained by the fact that the three outcomes, even though all representing aspects of udder health, were quite dissimilar. VTCM is dependent on the ability of the farmer/staff to detect CM and the

willingness to call for a veterinarian for treatment, which is varying (Nyman et al., 2007). Hence, this outcome differs markedly from the other two outcomes, which were based on SCC. The cut-off at 200,000 cells/mL, used as one of the outcomes, has been reported to have a sensitivity of 74–83 and a specificity of 59–89 in detecting prevalence of infection (Dohoo and Leslie, 1991; Schepers et al., 1997). A different cut-off used in the present study would probably have given other results, but in order to find the most optimal cut-off more studies of IMI and SCC are needed. The fact that none of the variables found significant in the final models of the two SCC outcomes were the same was somewhat unexpected. This implies that there can be a marked difference between SCC as a dichotomous variable and as a continuous variable, although, the choice of cut-off may make the dichotomous variable more or less dissimilar to the continuous variable. 4.1. Feed and feeding One of our hypotheses was that the feeding regime was more intense, e.g. higher levels of concentrates, and that they had a less well-balanced diet in herds with high

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Table 3 Variables considereda in the final multivariable Poisson-regression analysis of their association with number of first-parity cows with a SCC  200,000 cells/ mL at first test-day after calving in 72 Swedish dairy-herds Variable

No. of herds

Feed and feeding Sugar-beet pulp given at 1 month before calving No 59 Yes 13 Corn silage given at calving and onwards No Yes

56 16

Within-herd proportion of first-parity cows with SCC  200,000 cells/mL at first test-day (median)

P-value

12.5 18.8

0.03

11.1 18.6

0.03

Herd data Proportion of cows with consecutive high SCC (>300,000 cells/mL on three consecutive test-days) 22% 18 19.4 13–21.9% 35 11.5 <13% 19 11.1

0.02

Housing Alone or in group at calving Alone In group Moved from the calving area 1 day after calving 2 days after calving Milking Milking site during the colostrum period In parlor At calving site

55 17

11.5 16.7

0.02

39 33

11.5 15.6

0.03

55 17

11.5 20.0

0.05

Milking units are rinsed, cleaned or disinfected before a first-parity cow is milked No 49 10.5 Yes 23 16.7 a

<0.001

Exhibiting a significant association (P < 0.10) in the sub-models.

proportion of first-parity cows with mastitis compared to those with a low proportion. Another hypothesis was that the hygienic quality of the feed was worse in herds with poor udder health in first-parity cows. The results from the present study gave some support for these hypotheses. In herds where more first-parity cows were VTCM, pregnant heifers got silage from a different batch than the lactating cows. Silage batches can differ markedly in nutrient content (e.g. energy, protein, and fiber) and a sudden change in diet is not beneficial for the rumen function and could negatively influence the health of the cow (Dirksen et al., 1985; Dawson and Allison, 1988). There was also some evidence of a less well-balanced feeding ration on the individual level. Low milk-urea concentration (<4 mmol/L) at first test-day was associated with increased SCC at first test-day. This is in accordance with earlier studies, which showed an association between decreasing milk-urea concentrations and increased SCC (Godden et al., 2001; Johnson and Young, 2003). As low milk-urea indicates a lack of protein in the feed (Ipharraguerre et al., 2005; Schei et al., 2005) it is plausible that the feed ration given at calving and early lactation to first-parity cows having increased SCC at first test-day in the present study, was not properly balanced regarding protein. The relationship between feeding of first-parity cows in early lactation and udder health needs to be investigated further. The reasons behind the associations between the use of sugar-beet pulp and an increased risk of CM, and increased

individual SCC, and between use of corn silage and increased number of first-parity cows with a SCC  200,000, are not clear. Similar associations have been found in other studies, but none have been able to explain the nature of the association (Schukken et al., 1990; Barkema et al., 1999; Bareille et al., 2000). One possible explanation could be that the hygienic quality of corn silage can be poor due to growth of, e.g. mycotoxin producing moulds. In the present study we did not analyze the hygienic quality of sugar-beet pulp and corn silage, but found growth of the mycotoxin producing mould P. roqueforti in grass silage samples. Auerbach et al. (1998) detected P. roqueforti in more than 80% of sampled silages (both corn and grass silage) taken from different dairy farms. They also found higher concentrations of the mycotoxin roquefortin C in corn silages than in grass silages. Even low levels of mycotoxins are believed to cause immune suppression and increase the risk of infectious diseases (Osweiler, 2007). Another theory possibly explaining the associations between corn silage, sugarbeet pulp and udder health is based on the fact that both corn silage and sugar-beet pulp have low contents of protein. This theory is supported by observations made in the present study, that cows with low milk-urea (<4 mmol/L) at first test-day more often were given a diet containing sugar-beet pulp at calving and onwards than cows with higher milk-urea at first test-day (data not shown). However, a similar association between milk-urea

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145

Table 4 Variables considereda in the final multivariable linear-regression analysis of their association with LnSCC of 1189 first-parity cow at first test-day after calving in 72 Swedish dairy-herds Variable

No. of animals

Geometric mean SCC at first test-day (1000/mL)

P-value

Feed and feeding Sugar-beet pulp given at 1 month before calving and onwards No 935 Yes 254

60.1 82.3

0.007

Herd and first-parity cow data Breed of first-parity cow Swedish Holstein Swedish Red

718 471

67.6 59.7

0.001

Milk-urea <4 mmol/L 4 mmol/L 5 mmol/L >5 mmol/L

235 396 330 220

98.2 65.3 52.5 50.5

<0.001

Milk yield at first test-day <28.5 kg 28.5 kg

591 598

83.7 49.6

0.004

Percentage milk-fat at first test-day <4.2% 4.2%

644 545

52.7 81.4

<0.001

Proportion of cows with consecutive high SCC (>300,000 cells/mL on three consecutive test-days) 22% 329 74.9 13–21.9% 589 64.8 <13% 271 52.6 Veterinary treated for clinical mastitis before first test-day No 1134 Yes 55 Housing Moved from the calving-area 1 day after calving 2 days after calving

561 628

Type of flooring in the cubicles in the lactating cow housing Rubber mat 857 Mattress 243 Only concrete 89 Milking Milking site during the colostrum period In parlor At calving site

918 271

Milking units are rinsed, cleaned or disinfected before a first-parity cow is milked No 752 Yes 437

0.02

63.4 87.8

0.04

57.6 71.0

0.001

66.3 55.8 70.7

0.03

61.6 74.4

0.05

57.8 77.4

<0.001

Herd was included as random factor. a Exhibiting a significant association (P < 0.10) in the sub-models.

concentration and diets containing corn silage was not observed. It has been shown that first-parity cows fed diets supplemented with protein feed were in less negative energy balance in early lactation compared to first-parity cows fed unsupplemented diets (Tesfa et al., 2001). A more positive energy balance is beneficial for the immune system (Ingvartsen et al., 2003) and the udder health (Suriyasathaporn et al., 2000). 4.2. Herd and individual data None of the herd-level variables remained in the final models, probably due to the selection of herds. The herds in

the present study were selected by specific criteria regarding milk production, BMSCC, and herd size, which may have made them too similar and hence not significantly different in herd-level variables tested and factors associated with them. Other studies of factors associated with CM or SCC on herd level have shown significant associations with herd milk production (De Vliegher et al., 2004b; Barnouin et al., 2005), BMSCC (Elbers et al., 1998; Barkema et al., 1999), breed (Schukken et al., 1990; Barkema et al., 1999) and herd size (Waage et al., 1998; Barkema et al., 1998a). At the individual cowlevel, however, breed and milk yield at first test-day had significant effects on SCC in the present study. First-parity

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146

Table 5 Final multivariable Poisson-regression analysis of variables significantly (P  0.05) associated with number of first-parity cows veterinary treated for clinical mastitis in the period 10 to 60 days after calving in 70 Swedish dairy herds (deviance = 58.7 on 64 d.f.) S.E. (b)

IRRa

95% CI (IRRa)

P-value

0.61

–

–

–

– 0.23

– 1.82

– 1.15, 2.88

– 0.01

– 2.02

– 1.24, 3.30

– 0.005

– 0.32

– 0.37

– 0.19, 0.68

– 0.002

Ref.b 0.62

– 0.27

– 1.87

– 1.09, 3.18

– 0.02

Milking Milking site during the colostrum period In parlor Ref.b At calving site 0.64

– 0.24

– 1.90

– 1.18, 3.06

– 0.008

b

Variable

Intercept 8.78 Feed and feeding Sugar-beet pulp given at calving and onwards No Ref.b Yes 0.60

Silage from a different batch given to pregnant heifers than to lactating cows No Ref.b – Yes 0.70 0.25 Housing Housing system 1 month before calving Free stall Ref.b Tie stall 1.01 Type of bedding in calving area Straw Sawdust or shavings

a b

IRR = incidence rate ratio. Reference category.

cows of the SR-breed had lower LnSCC at first test-day than cows of the SH-breed. This difference has been shown repeatedly during the last decade (Swedish Dairy Association, 2003), and might be an effect of differences in breeding strategies. A significant association between breed and SCC on the individual cow level was also observed by Compton et al. (2006). Our finding that a higher milk yield at first test-day was associated with a lower LnSCC at the same time was probably due to a dilution effect (Green et al., 2006). The factor influencing the individual LnSCC the most was the interaction term between being VTCM before first test-day and milk-fat at first test-day. An association between increased SCC and CM has been shown by others (Dohoo et al., 1984; Edinger et al., 1999). However, that the risk of increased LnSCC could be different between cows VTCM depending on percentage of milk-fat at first test-day is somewhat unexpected. In a review by Hortet and

Seegers (1998), both high and low milk-fat percentages were reported to be associated with CM. 4.3. Housing One of our hypotheses was that multiple changes of housing in the period around calving are stressful for firstparity cows and could have a negative influence on udder health, but we could not confirm this in the present study. Instead, we found that housing pregnant heifers in tie stalls 1 month before calving compared to house them in free stalls was associated with a reduced number of first-parity cows VTCM. It is likely that many first-parity cows with VTCM in the first weeks of lactation were infected already before calving. Cow to cow, and cow to heifer, contact is more common in free stalls than in tie stalls, which may increase the risk of transmission of infectious agents between animals. In the present study, the majority of the

Table 6 Final multivariable Poisson-regression analysis of variables significantly (P  0.05) associated with number of first-parity cows with a SCC  200,000 cells/ mL at first test-day after calving in 72 Swedish dairy herds (deviance = 71.8 on 68 d.f.) Variable

B

S.E. (b)

IRRa

95% CI (IRRa)

P-value

Intercept 2.75 Feed and feeding Corn silage given at calving and onwards No Ref.b Yes 0.39

0.26

–

–

–

– 0.16

– 1.47

– 1.08, 2.02

– 0.01

Milking Milking site during the colostrum period In parlor Ref.b At calving site 0.37

– 0.17

– 1.45

– 1.04, 2.03

– 0.001

– 1.68

– 1.24, 2.29

– 0.001

Milking units are rinsed, cleaned or disinfected before a first-parity cow is milked – No Ref.b Yes 0.52 0.16 a b

IRR = incidence rate ratio. Reference category.

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147

Table 7 Final hierarchical multivariable linear-regression analysis of variables significantly (P < 0.05) associated with LnSCC of 1189 first-parity cows at first testday in 72 Swedish dairy herds Variable

b

S.E. (b)

LSMa

Intercept DIM (DIM)2

4.03 0.03 0.0009

0.10 0.004 0.0002

– – –

Feed and feeding Sugar-beet pulp given at calving and onwards No Ref.c Yes 0.28

95% CI (LSMa)

P-value

– – –

– n.a.b <0.001

– 0.10

59.0 79.7

– 67.0, 94.8

– 0.006

Ref.c 0.20

– 0.07

65.9 58.6

– 52.4, 65.5

– 0.006

0.33 Ref.c 0.19 0.18

0.09 – 0.08 0.09

98.2 65.1 51.4 50.1

84.9, 113.6 – 45.5, 58.2 43.0, 58.3

<0.001 – 0.01 0.06

Milk yield at first test-day <28.5 kg 28.5 kg

Ref.c 0.23

– 0.07

81.8 48.6

– 44.0, 53.6

– 0.001

Housing Moved from the calving-area 1 day after calving 2 days after calving

Ref.c 0.27

– 0.08

55.2 70.8

– 63.5, 79.0

– 0.001

– 0.10 0.15

65.4 53.4 67.6

– 45.0, 63.3 51.9, 87.9

– 0.001 0.40

– 43.3, 85.1 70.5, 86.6 89.5, 253.4

– 0.68 0.002 <0.001

Herd and first-parity cow data Breed of first-parity cow Swedish Holstein Swedish Red Milk-urea <4 mmol/L 4 mmol/L 5 mmol/L >5 mmol/L

Type of flooring in the cubicles in the lactating cow housing Rubber mat Ref.c Mattress 0.33 Only concrete 0.12

Interaction Percentage of milk-fat at first test-day * veterinary treated for clinical mastitis (VTCM) before first test-day <4.2% and not VTCM Ref.c – 51.0 4.2% and not VTCM 0.07 0.18 60.7 <4.2% and VTCM 0.21 0.07 78.1 4.2% and VTCM 1.01 0.27 150.6 a b c

LSM on LnSCC scale back-transformed to original scale (1000/mL). n.a. = not applicable. Reference category.

farms that housed their pregnant heifers in free stalls had them together with dry cows. It has been shown that the rate of CM increases when dry cows and pregnant heifers are housed together (Barkema et al., 1999). Use of sawdust or wood shavings, compared to use of straw, in the calving area was associated with an increased number of first-parity cows VTCM. This was in agreement with Bartlett et al. (1992), but in contrast to findings by O’Reilly et al. (2006). As udder pathogens can grow in large numbers both in straw and sawdust, the frequency of cleaning, and distribution of fresh bedding, may be more important in improving udder health than type of bedding. In the present study, however, no significant association was found between the frequency of cleaning, distribution of fresh bedding, and udder health. Using mattresses, compared to rubber mats, in the cubicles of the lactating cow housing was associated with decreasing LnSCC. The reasons behind this finding are not known, and in a study by Chaplin et al. (2000), no such association was found. To move first-parity cows from the calving area 2 days compared to 1 day after calving was associated with an

increased LnSCC, which was in line with De Vliegher et al. (2004b). If not cleaned properly after calving, the calving area provides a good environment for environmental udder pathogens. Associations between poor hygiene of the calving area and udder health have been shown in several studies (Barkema et al., 1999; Bareille et al., 2000; De Vliegher et al., 2004a). 4.4. Milking To milk first-parity cows at the calving site instead of in the parlor was associated with an increase in both number of first-parity cows VTCM and number of first-parity cows with SCC 200,000 cells/mL at first test-day. This was most likely due to poorer milking routines and milking equipment at the calving site than in the parlor. To rinse, wash or disinfect the milking unit before a first-parity-cow was milked was also associated with an increased number of first-parity cows with SCC  200,000 cells/mL at first test-day. A similar association was found by Barnouin et al. (2005), where herds with a high incidence rate of CM more frequently rinsed

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the clusters after a cow with high SCC. As the variables found significant in our study might not be causative, it is possible that the findings was due to that herds with first parity-cows with high LnSCC try to reduce the transmission of contagious bacteria between cows in this way. Studies have shown, however, that cluster rinsing results only in a marginal reduction of bacterial counts in the clusters (Shearn et al., 1994), with no influence on the incidence of IMI (Smith et al., 1985). 4.5. Final remark The differences in nature of the udder health measures chosen in this study can explain the differences in risk factors found in the three final multivariable models. The udder health measure VTCM depends on the actual observation of a case of mastitis. Thus, both the nature of the case (e.g. severity) and the awareness of the farmer/ worker can influence the number of cases being observed, but also the willingness/need to contact a veterinarian for treatment, and the reliability of the veterinarian to record the treatment influences the number of cases reported. The SCC is a different and entirety objective measure of the udder health compared to the VTCM, as is also the udder health measure of number of sub-clinical cases of mastitis (SCC  200,000 cells/mL). Moreover, it is important to bear in mind that the associations found in this study between the investigated variables and outcomes may not necessarily indicate causal relationships, and there is also a possibility of finding associations ‘‘due to chance alone’’ when many factors are studied in large datasets (Dohoo et al., 1997). The results found in the present study should therefore be confirmed in independent studies to be certain that the associations found between the factors and udder health are true. 5. Conclusions Our study identified several factors that were related to udder health of first-parity cows. Some factors related to feeding (using corn silage and sugar-beet pulp, low milkurea), housing (not using straw in the calving area or mattresses in the cubicles), general management (moving cows from the calving site after 2 day after calving, milking at the calving site during colostrum period), and herd characteristics (SH-breed rather than SR-breed) increased the risk for udder disorders. However, our study also identified that the factors may vary depending on the type of udder health problem. More studies are needed to confirm some of these results. Acknowledgements The authors gratefully acknowledge the financial support from the Swedish Farmer’s Foundation for Agricultural Research (Stockholm, Sweden) and the Swedish Dairy Association (Stockholm/Eskilstuna, Sweden). We would especially like to thank all participating farmers for their hospitality and cooperation, and the technicians for invaluable assistance.

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