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Effects of behaviour on the development of claw lesions in early lactation dairy cows
Applied Animal Behaviour Science 134 (2011) 16–22
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Effects of behaviour on the development of claw lesions in early lactation dairy cows Sabine Dippel a,∗ , Cassandra B. Tucker b , Christoph Winckler a , Daniel M. Weary c a BOKU – University of Natural Resources and Life Sciences, Vienna, Department of Sustainable Agricultural Systems, Division of Livestock Sciences, Gregor-Mendel-Strasse 33, 1180 Vienna, Austria b University of California, Animal Science Department, 1 Shields Ave, Davis, CA 95616, USA c Animal Welfare Program, University of British Columbia, 2357 Main Mall, Vancouver, BC V6T 1Z4, Canada
a r t i c l e
i n f o
Article history: Accepted 6 June 2011 Available online 2 July 2011 Keywords: Lameness Cow comfort Sole haemorrhage White line separation Standing time
a b s t r a c t Claw lesions such as haemorrhages (HAEM) or white line separation (WLS) are caused by a variety of factors. The aim of this study was to assess the relationship between behaviour and the development of claw lesions. Holstein cows (n = 33) were housed in four pens with sand-bedded cubicles and solid concrete flooring, and stocked at two different densities in order to increase variation in cubicle use. Lying, feeding and standing behaviour were recorded for 48 consecutive hours per week during the first 3 weeks after calving using 10 min scan sampling from video. Claw health was scored at approximately 11, 40, 69, and 95 days after calving. For each time point and cow, we calculated four hoof health scores by summing the respective lesion severity scores for all four feet: total HAEM (HAEMT), HAEM sole only (HAEM-S), HAEM white line only (HAEM-W), and total WLS (WLS-T). Analysis consisted of linear mixed models with repeated observations and HAEM-T, HAEMS, HAEM-W and WLS-T, respectively, as dependent variables. The lesion scores at first claw scoring were included as covariates in each model. Cows that spent more time standing with their front feet in the cubicle had significantly higher haemorrhage scores in all feet (HAEM-T). Lying time was not associated with any of the lesion scores, perhaps because cubicle design and management encouraged reasonable lying times (11.0 h/d on average). In conclusion, standing partially in the cubicle increased the risk of claw haemorrhages in dairy cows after calving. Barns should be designed and managed to minimize this behaviour. © 2011 Elsevier B.V. All rights reserved.
1. Introduction Lameness is one of the most important health and welfare problems in dairy cows. On average one quarter of cows are lame at a given time (Espejo et al., 2006), while on single farms more than 80% of the herd can be affected
∗ Corresponding author. Current address: Institute of Animal Welfare and Animal Husbandry, Friedrich-Loeffler-Institut, Doernbergstr. 25/27, 29223 Celle, Germany. Tel.: +49 5141 3846200; fax: +49 5141 3846117. E-mail addresses: [email protected], sabine.dippel@fli.bund.de (S. Dippel). 0168-1591/$ – see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.applanim.2011.06.006
(Dippel et al., 2009b). Lesions in the claws, such as sole ulcers, are known to be an important source of lameness (Murray et al., 1996). The causation of lameness and claw lesions is complex and includes risk factors such as nutrition (Manson and Leaver, 1988), housing (Somers et al., 2003) and genetics (Boelling and Pollott, 1998). Dairy cows in the northern hemisphere are commonly kept in cubicle barns with solid or slatted concrete flooring in the walking area, and stalls (“cubicles”) with rubber mats, cow mattresses or deep bedding as a lying surface. In these barns standing behaviour is thought to be associated with claw health for several reasons. Firstly, while cows are standing on concrete flooring, which is typically provided
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outside of the stall, their claws are exposed to mechanical forces which can cause damage through trauma or excessive weight bearing (Lischer and Ossent, 1994). Secondly, claws may be in contact with manure slurry while standing which can soften the horn and thus possibly increase risk of injury (Borderas et al., 2004). Cows with longer daily standing times have been found to have more claw lesions and lameness (Leonard et al., 1996; Galindo and Broom, 2000). Similarly, longer standing times before calving are associated with the development of haemorrhages after calving; after calving, animals with haemorrhages have shorter standing times (Chapinal et al., 2009b). In addition, parameters associated with lying comfort such as type of cubicle surface and abnormal lying behaviour have been associated with lameness in on-farm surveys (Dippel et al., 2009a). Another potential risk behaviour is time spent standing with only the front feet in the cubicle (“perching”), a behaviour related to cubicle comfort (Tucker et al., 2004). Cows who spend more time perching in a cubicle have been found to be more likely to become lame (Galindo et al., 2000; Proudfoot et al., 2010). However, the causal nature of this relationship is not clear, as the weight distribution of cows standing with front feet raised is not different from cows standing level (Chapinal et al., 2009a). Finally, as with standing in the alley, partially standing in the cubicle increases exposure of the hind feet to slurry, and moisture. In addition to behaviour performed in the cubicle, feeding behaviour may also be related to claw health. Cows spend a considerable amount of time eating and reductions in feeding time or intake around partition are related to other disorders, such as metritis and ketosis (Urton et al., 2005; Goldhawk et al., 2009). Furthermore, changes in diet, specifically increases in concentrate intake, are associated with an increase in claw lesions around the time of calving (Livesey et al., 1998). The combination of changes in feeding behaviour and an increase in concentrates in the diet during the transition period indicates that time spent feeding may be an important factor influencing claw health. In general, the period of highest risk for claw lesion development is the time around calving because of the major physiological and environmental changes taking place. Most claw lesions are related to disruption of the horn producing tissue (corium) inside the claws. Causes of disruption include a decline in rumen-pH (acidosis) due to a high carbohydrate:fibre ratio in the diet, endotoxinemitting infections like metritis, or mechanical overload due, for example, to prolonged standing on a hard surface (Lischer and Ossent, 1994; Livesey et al., 1998; Mülling et al., 2006). Damage to the corium causes blood infiltration into the horn and diminishes horn quality. The modified horn grows outwards and becomes visible as discolorations and low quality horn on the surface of the claw approximately 6–16 weeks later (Bergsten and Frank, 1996; Mülling et al., 2006). Our aim was to investigate the effects of time spent standing with the front feet in a cubicle, feeding and lying during the first 3 weeks after calving on the development of claw lesions up to 13 weeks after calving. As lying
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time of cows housed in cubicles decreases with increasing stocking density (Fregonesi et al., 2007), we manipulated stocking density in order to increase variation in cubicle use. 2. Materials and methods 2.1. Animals and housing conditions The experiment was conducted at the UBC Dairy Education & Research Centre, Agassiz (BC), Canada. We housed 48 Holstein cows, in four groups of 12, in 3-row pens with sand-bedded cubicles and solid concrete flooring, with automatic scrapers on a 6-h-schedule. All cows entered the experiment within one day from calving. In order to keep group size constant, experimental pens had been stocked with non-experimental cows at the start of the experiment, which were replaced one by one by experimental cows. Cows were randomly assigned to pens and blocked by lactation number and 305-day yield of the previous lactation. Median lactation number was two (range one to eight) and mean previous 305-day yield was 11,623 ± 2080 kg (mean ± SD). As not all cows calved on the same day it took 19, 26, 29 and 32 days for groups to become established. Cows spent 91–102 days on the experiment (mean: 95 days). Two groups were housed at a 1:1 cow-to-cubicle ratio (“100%”; two primiparous and three multiparous (pen 1), and three primiparous and nine multiparous cows (pen 3); Fig. 1) and two groups were overstocked at 1.3 cows per cubicle (“133%”; one primiparous and three multiparous (pen 2), and three primiparous and nine multiparous cows (pen 4)). Stocking densities in excess of 100% are common on commercial farms, for example a recent US survey found that 30.4% of cubicle farms housed cows at ≥110% (USDA, 2010). In the 133% condition walking area allowance was reduced from 5.33 m2 /cow to 4.71 m2 /cow and feeding space decreased from 0.61 m/cow to 0.54 m/cow. This was achieved by blocking off the dead-end side of the pen perpendicular to the feed face (Fig. 1). Each pen contained head-to-head and head-to-wall cubicles. Cubicle width was 120 cm and cubicle lengths 240 cm (head-to-head) and 270 cm (head-to-wall). The neckrail was located 160 cm from the curb and the neckrailcurb diagonal was 206 cm. Cubicles were bedded every 10–14 days with washed river sand (max. grain size 2 mm). The entire herd was milked at 05:00 h and 15:00 h in a double-twelve side-by-side parlour in the same building, and cows were out of the pen for approximately 1 h per milking. Cows were fed fresh total mixed ration (roughage mixed with concentrates) ad libitum after every milking (feed bunk with open rails). The ration contained 45.6% dry matter (DM) and was composed of 15.7% maize silage, 37.2% protein/mineral/energy supplement, 11.6% grass silage, 17.2% flattened maize/barley mix, 9.9% grass hay, and 8.4% alfalfa hay. Crude protein was 17.8%, net energy for lactation 0.76%, acid detergent fibre 18.0%, neutral detergent fibre 33.2%, calcium 0.73%, phosphorus 0.41%, and sodium 0.2% (all DM %). Before calving, cows and heifers had been housed in the same barn. Every cow had been hoof-trimmed by a professional hoof trimmer at dry
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Fig. 1. Layout of experimental pens. Grey areas = cubicles, hatched areas = blocked off for overstocking.
off. All animals were cared for according to the guidelines of the Canadian Council on Animal Care (1993). 2.2. Behavioural observations Behaviour was recorded for 48 consecutive hours per week (starting after afternoon milking) for 3 weeks after calving using time-lapse video with two cameras per pen (Panasonic WV-BP330 cameras with Pelco Varifocal Lenses in combination with Panasonic Time Lapse Video Cassette Recorder AG-6540 and Panasonic Video Multiplexer WJ-FS216). Lying, feeding, and standing behaviour were recorded using 10 min scan sampling with the following definitions: lying = ventral part of body touches ground completely (none of the cows lay down in the walking area), feeding = standing at feed bunk with head above bunk, standing with front feet in cubicle = standing with both front feet in cubicle and rear feet in alley. Time budgets were expressed as percent of positive scans per total scans of one 48 h observation period (= weekly value). Weekly values were summarized by calculating the mean and extreme values across weeks. The latter refers to the smallest value for lying and feeding and the largest value for standing with front feet in the cubicle (based on their predicted effect on claw lesions) from weeks 1, 2 and 3, respectively. For nine of the cows included in analysis, there were only data from two weeks of observation available due to technical problems. 2.3. Claw lesion recording The claws of all animals were scored four times at 4week intervals (T1 to T4). At T1, cows were on average 11 days post partum (days in milk (DIM); range 7–18), at T2 40 DIM (35–46), at T3 69 DIM (65–77), and at T4 95 DIM (91–102). A professional hoof-trimmer (Giroux Hoof Trimming, Agassiz, Canada) cleaned and pared approximately 1 mm off the surface of the claws before lesions were scored by a single trained observer. Lesions were recorded separately in five zones (following the 6th Symposium on Diseases of the Ruminant Digit, Liverpool, 1990). For analysis we merged values from zones
1 to 3 as “white line” and 4 and 5 as “sole”. Haemorrhages (HAEM) were scored on the entire distal surface based on the arithmetic system of Leach et al. (1998), which distinguishes lesions based on their colouration and changes in horn structure (Table 1). White line separation (WLS) was scored using a five point scale ranging from striation to separations wider than 2 mm (modified after Smilie et al., 1999; Table 1). We defined striation as more than five regularly spaced black stripes perpendicular to the white line, and a solid black line as completely black discoloration of the white line at least as long as five striation lines. We used the number of striation lines as length parameter instead of measurements because striation lines are equally spaced independently of the curve of the white line and can still be distinguished even if the white line is black (solid black line). Visibly distinct lesions were scored separately. During the experiment all cows were treated twice for digital dermatitis (topical treatment with 9.91 g/L LincoSpectinTM 100 solution in the milking parlour once a day on 3 consecutive days). Digital dermatitis occurred only rarely after treatments and therefore was not analysed. There were no cases of interdigital skin hyperplasia. The respective HAEM and WLS severity scores given to all single lesions found were summed up for T1, T2, T3 and T4, respectively (’sum of arithmetic severity scores’;
Table 1 Scoring keys for haemorrhages (Leach et al., 1998) and white line separation (modified after Smilie et al., 1999). Severity score
Haemorrhage
0
No alterations visible on distal surface Diffuse red or yellow Stronger red Deep dense red Port coloration
1 2 3 4 5 6 7 8
Red, raw, possibly fresh blood Corium exposed Severe ulcer–major loss of horn Infected ulcer
White line separation
Striation (>5 lines), dirt Solid black line Parting <2 mm Parting >2 mm, wall completely split off
S. Dippel et al. / Applied Animal Behaviour Science 134 (2011) 16–22
following Leach et al., 1998). This approach allows us to distinguish cows with several severe injuries from those with multiple, less severe injuries. This was important because in this study the sample size was insufficient to categorize animals as healthy or injured. We calculated four summary scores for each cow: total sum of haemorrhages (HAEM-T), sum of haemorrhages in the sole (HAEM-S), sum of haemorrhages in the white line (HAEM-W), and total sum of WLS (WLS-T). 2.4. Statistical analysis The data of 15 cows had to be dropped because of completely missing behaviour observations. This left 33 cows for analysis, nine primiparous and 24 multiparous. Data presented therefore refer to the 33 cows included in analysis only. Linear mixed models for HAEM-T, HAEMS, HAEM-W and WLS-T were calculated in SAS 9.1.3 (SAS Institute Inc., 2007) with the independent factors lying, feeding, and standing with only the front feet in cubicles. ‘Initial score’ was included as covariate and was kept in the models regardless of its significance in order to correct estimates for its influence. We calculated two models for each outcome: one with mean and one with extreme behaviour values. Mean lying time was correlated negatively with mean time standing with front feet in cubicles (rSpearman = −0.41, P = 0.017, n = 33 cows) so models were also calculated without mean lying. However, the estimates and p-values of models with and without mean lying were virtually identical to those from the models containing all behaviours. Therefore, only the models containing all behaviours are presented. Unlike the mean behaviour
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values, the extreme values for the three behaviours were not correlated (rSpearman = −0.16 to −0.30, P > 0.086, n = 33 cows). Models were calculated with PROC MIXED with period (T2 to T4) specified in the REPEATED statement and cow, nested by group, specified as repeated SUBJECT. The covariance-structure was defined as unstructured (selected via best fit based on Akaike information criterion and Schwarz Bayesian criterion). Residuals were evaluated visually (ODS GRAPHICS and RESIDUAL option). Finally, to investigate how injuries varied between front and hind claws, the HAEM-T scores in hind and front claws were compared at given claw scorings using Wilcoxon signed rank test in PROC UNIVARIATE. For all analyses, p-values less than 0.05 were regarded as indicating statistical significance. 3. Results 3.1. Dataset characteristics Cows spent on average 11.0 ± 2.2 h/d (mean ± SE) lying down, 4.5 ± 0.9 h/d feeding, and 2.3 ± 1.2 h/d standing with their front feet in cubicles. Averages of the minimum values were 9.8 ± 2.4 h/d for lying time and 3.9 ± 0.9 h/d feeding time. The average maximum time cows spent standing with their front feet in cubicles was 3.0 ± 1.6 h/d. The highest score for a single haemorrhage found on any one cow (Table 1) ranged from 1 to 5, and no cows had an ulcer. The maximum white line separation score/cow ranged from 1 to 4. The summary scores/cow were distributed as follows (means and ranges across T2, T3 and
Fig. 2. Total haemorrhage scores (HAEM-T), sum of haemorrhage scores in the sole (HAEM-S), sum of haemorrhage scores in the white line (HAEM-W) and total score sums of WLS (WLS-T) across claw scorings (T1 to T4; animal level scores).
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Fig. 3. Mean haemorrhage score sums/cow in front and hind claws across claw scorings (T2 to T4). n = 33 cows. *P < 0.001. Error bars represent the respective standard errors.
T4): HAEM-T 27.6 (7–70), HAEM-S 16.3 (4–50), HAEM-W 11.3 (0–28), WLS-T 38.6 (20–68). Lesion scores increased over time (Fig. 2). For HAEMT this increase was mainly due to increased lesions in the hind claws, which at T3 and T4 had higher scores than the front claws (P < 0.001; Fig. 3). 3.2. Relationship between behaviour and lesions Total haemorrhages (HAEM-T) were associated with time spent standing with front feet in cubicles and initial HAEM-T score (Table 2). Both mean and maximum time spent standing with front feet in the cubicles were associated with HAEM-T. HAEM-S was only associated with standing with front feet in cubicles (both mean and maximum) while HAEM-W were only associated with initial HAEM-W score. Only initial WLS-T score was associated with subsequent WLS-T. No measure of feeding or lying time was associated with lesion scores. 4. Discussion In general, the cows studied in this experiment had reasonably good claw health, as shown by the absence of ulcers. In contrast, sole ulcer prevalence was 14% in the study by Leonard et al. (1996) and 17% in Chapinal et al. (2009b). Of the behaviours studied, only time spent standing with the front feet in a cubicle was associated with claw lesions. Overall, cows that spent more time standing with front feet in cubicles had higher HAEM-T and higher HAEMS scores. This agrees with results from Proudfoot et al. (2010), who (two weeks before and 24 h after calving) found more standing with front feet in a cubicle in cows who developed sole lesions later in lactation. There are at least three potential explanations for this relationship: (1) standing with two feet in the cubicle increases weight bearing on the hind claws, (2) this behaviour corresponds with other possible risk factors such as social status, and (3) standing in this way increases exposure to slurry, thus increasing the risk for impaired hoof health. The first idea, that standing with the front feet in the cubicle increases
weight bearing by hind claws resulting in increased risk of injury, is unsupported. In a study where cows stood on load cells with the front feet raised, there was no difference in weight bearing by the hind feet compared to when the front and hind feet were level (Chapinal et al., 2009a). The second idea is based in part on the finding that subordinate cows spend more time standing partially in the cubicle compared to dominant animals (e.g. Galindo and Broom, 2000) and subordinates may be at greater risk for claw injuries for other reasons, such as sudden turns caused by displacements. Unfortunately, there is no empirical evidence to address this link. The third idea is well supported; standing with the front feet in the cubicle increases exposure of the hind feet to both manure and concrete. Exposure to moisture and manure decrease hoof hardness (Borderas et al., 2004) and cows kept in systems that limit exposure to both slurry and concrete have improved hoof health (Bergsten and Herlin, 1996; Livesey et al., 1998). Regardless of the mechanism, these results indicate that standing with the front two feet in the cubicle should be minimized. It is possible that development of the lesions caused the differences in behaviour, rather than vice versa. The findings described in this study show a relationship between standing partially in the cubicle and lesions, but cannot be used to definitively establish causation. However, we argue that it was the behaviour that led to changes in lesions development based on two lines of reasoning. The first is that cows differed in behaviour in the first few weeks after calving, well before the majority of lesions had developed. However, sole lesions only become visible weeks after damage to the corium occurs (Mülling et al., 2006) so the time course of the behavioural changes relative to injury is difficult to establish. More convincing are the results from Bernardi et al. (2009) who manipulated cubicle design (by making the neck rail less restrictive) reducing the time cows spent standing with their front feet in the cubicle. Lameness then declined in weeks that followed providing stronger evidence that lameness is varying as a result of the change in behaviour, rather than vice versa. Several aspects of housing design and management influence standing partially in the cubicle. A number of studies have shown that restrictive neck rail placement (closer to the cubicle surface or entrance) increases standing with only two feet in the cubicle (Tucker et al., 2005; Bernardi et al., 2009; Fregonesi et al., 2009). Cows also spend more time standing partially in narrower cubicles (Tucker et al., 2004), cubicles with less bedding (Tucker and Weary, 2004) and when the ratio of cows to cubicles is over 1:1 (Fregonesi et al., 2007). Together, these results illustrate changes in cubicle design and management that can reduce standing partially in the cubicle and thus likely reduce the risk of claw injuries. Lying time and feeding time after calving were not related to lesions later in lactation. One possible explanation for the lack of relationship with lying times is that these were relatively long in the current study. Lying time averaged 11.0 h/d and was thus close to what can be regarded the behavioural need (Jensen et al., 2005); even minimum lying time averaged 9.8 h/d. Cows in earlier work that has reported an association between shorter lying time and lameness. For example, Leonard et al. (1996)
S. Dippel et al. / Applied Animal Behaviour Science 134 (2011) 16–22
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Table 2 Results from mixed model analysis of the association between behaviour and claw lesions. Separate models were calculated for behaviour summarised as mean and extreme values recorded during 21 days after calving (unit = % of time). Extremes for feeding and lying are minimum values, extremes for standing with front feet in cubicles are maximum values. Claw lesions were analysed in the form of sums of single lesion severity scores/cow, repeatedly recorded three times within 14 weeks after calving. The respective sums of lesion severity scores directly after calving (initial score) was included as covariate. n = 33 cows, DF = 28. Dependent a
Behaviour summary
Factor
Estimate
Standard error
T
HAEM-T
Extreme
Intercept Initial HAEM-T score Feeding Lying Standing with front feet in cubicles Intercept Initial HAEM-T score Feeding Lying Standing with front feet in cubicles
21.14 0.45 −0.48 0.01 0.44 31.41 0.36 −0.70 −0.06 0.50
12.11 0.19 0.36 0.15 0.18 16.03 0.19 0.39 0.18 0.23
1.8 2.4 −1.3 0.1 2.4 2.0 1.9 −1.8 −0.4 2.2
0.092 0.022 0.192 0.948 0.025 0.060 0.066 0.088 0.729 0.039
Intercept Initial HAEM-S score Feeding Lying Standing with front feet in cubicles Intercept Initial HAEM-S score Feeding Lying Standing with front feet in cubicles
15.38 −0.04 −0.29 −0.02 0.52 19.31 −0.08 −0.34 −0.06 0.65
8.03 0.15 0.25 0.10 0.13 9.88 0.14 0.25 0.11 0.15
1.9 −0.2 −1.2 −0.2 4.1 2.0 −0.6 −1.4 −0.5 4.4
0.066 0.813 0.241 0.814 <0.001 0.061 0.567 0.181 0.596 <0.001
Intercept Initial HAEM-W score Feeding Lying Standing with front feet in cubicles Intercept Initial HAEM-W score Feeding Lying Standing with front feet in cubicles
10.95 0.86 0.18 −0.13 0.00 15.59 0.78 −0.03 −0.12 −0.06
7.92 0.30 0.25 0.10 0.12 10.92 0.32 0.28 0.12 0.16
1.4 2.9 0.7 −1.3 0.0 1.4 2.5 −0.1 −1.0 −0.4
0.178 0.007 0.466 0.213 0.996 0.165 0.020 0.912 0.344 0.731
Intercept Initial WLS-T score Feeding Lying Standing with front feet in cubicles Intercept Initial WLS-T score Feeding Lying Standing with front feet in cubicles
36.65 0.32 −0.26 −0.11 0.05 33.86 0.31 −0.09 −0.09 0.09
8.57 0.09 0.26 0.11 0.13 10.93 0.09 0.28 0.13 0.17
4.3 3.4 −1.0 −1.1 0.4 3.1 3.4 −0.3 −0.7 0.5
<0.001 0.002 0.332 0.302 0.696 0.004 0.002 0.751 0.473 0.611
Mean
HAEM-S
Extreme
Mean
HAEM-W
Extreme
Mean
WLS-T
Extreme
Mean
P
a HAEM-T = total haemorrhage (HAEM) sum per cow, HAEM-S = HAEM sum, sole only, HAEM-W = HAEM sum white line only, WLS-T = total white line separation sum per cow.
found an increase in lesions and lameness when lying time decreased from between 7 and 10 h/d to 5 h/d. In a more recent study, Chapinal et al. (2009b) reported lying times similar to those in the current study (approximately 9–12 h/d). They found that the relationship between lying behaviour and claw health was more complex than previously identified. Cows that developed sole ulcers had a steeper decline in lying times in the weeks before calving and a more marked increase in lying several weeks after calving compared to cows without ulcers (Chapinal et al., 2009b). The increase in lying time in cows with ulcers corresponds to higher gait scores, in agreement with others that have found that severely lame cows spend more time lying down (Ito et al., 2010; Gomez and Cook, 2010). These results suggest that pre-calving and/or changes in lying
behaviour might have more impact on the development of claw lesions than does lying behaviour after calving. However, pre-calving behaviour and daily changes in lying time were not assessed in the current study. Similarly, there was no relationship between time spent feeding and claw health. Cows showed little variation in feeding times, making it difficult to evaluate how variation in this parameter relates to claw lesions. In previous work linking health disorders after calving with feeding behaviour (Proudfoot et al., 2010), the period two weeks before and 24 h after calving seems particularly important, but this period was not investigated in the current work. Several studies have shown that keeping cows on pasture can also reduce the risk of lesions and lameness (Olmos et al., 2009). Cows housed indoors on bedded pack also have
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better hoof health (Webster, 2001). Indeed, the results from the current study suggest that one common feature reducing the risks is the lack of opportunity to stand partially in a cubicle. Together, our results and those of other studies indicate that, environments that allow cows to stand on clean, non-concrete standing surfaces are likely beneficial for hoof health. 5. Conclusions Standing with the front feet in the cubicle and the hind feet in the alley is associated with increased risk of claw haemorrhages later in lactation. These results indicate that dairy barns should be designed and managed to minimize time cows spend standing with their front feet in cubicles. Acknowledgements We thank Nelson Dinn and his team of the University of British Columbia’s Dairy Education and Research Centre, and Katie Lowe, Michelle Drissler, Kiyomi Ito, Frances Flower, Julie Huzzey, and Lorna Baird for their assistance. The project was funded by the Natural Sciences and Engineering Research Council of Canada through the Industrial Research Chair in Animal Welfare, and by contributions from the Dairy Farmers of Canada and many others listed at www.landfood.ubc.ca/animalwelfare/. Additional funding was provided to the first author through a “DAAD Doktorandenstipendium” from German Academic Exchange Service. References Bergsten, C., Frank, B., 1996. Sole haemorrhages in tied heifers in early gestation as an indicator of laminitis: effects of diet and flooring. Acta Vet. Scand. 37, 375–381. Bergsten, C., Herlin, A.H., 1996. Sole haemorrhages and heel horn erosion in dairy cows: The influence of housing system on their prevalence and severity. Acta Vet. Scand. 37, 395–408. Bernardi, F., Fregonesi, J., Winckler, C., Veira, D.M., von Keyserlingk, M.A.G., Weary, D.M., 2009. The stall-design paradox: neck rails increase lameness but improve udder and stall hygiene. J. Dairy Sci. 92, 3074–3080. Boelling, D., Pollott, G.E., 1998. Locomotion, lameness, hoof and leg traits in cattle II genetic relationships and breeding values. Livest. Prod. Sci. 54, 205–215. Borderas, T.F., Pawluczuk, B., de Passillé, A.M., Rushen, J., 2004. Claw hardness of dairy cows: relationship to water content and claw lesions. J. Dairy Sci. 87, 2085–2093. Chapinal, N., de Passillé, A.M., Rushen, J., 2009a. Weight distribution and gait in dairy cattle are affected by milking and late pregnancy. J. Dairy Sci. 92, 581–588. Chapinal, N., de Passillé, A.M., Weary, D.M., von Keyserlingk, M.A.G., Rushen, J., 2009b. Using gait score, walking speed, and lying behavior to detect hoof lesions in dairy cows. J. Dairy Sci. 92, 4365–4374. Dippel, S., Dolezal, M., Brenninkmeyer, C., Brinkmann, J., March, S., Knierim, U., Winckler, C., 2009a. Risk factors for lameness in cubicle housed Austrian Simmental dairy cows. Prev. Vet. Med. 90, 102–112. Dippel, S., Dolezal, M., Brenninkmeyer, C., Brinkmann, J., March, S., Knierim, U., Winckler, C., 2009b. Risk factors for lameness in freestallhoused dairy cows across two breeds, farming systems, and countries. J. Dairy Sci. 92, 5476–5486. Espejo, L.A., Endres, M.I., Salfer, J.A., 2006. Prevalence of lameness in highproducing Holstein cows housed in freestall barns in Minnesota. J. Dairy Sci. 89, 3052–3058. Fregonesi, J.A., Tucker, C.B., Weary, D.M., 2007. Overstocking reduces lying time in dairy cows. J. Dairy Sci. 90, 3349–3354. Fregonesi, J.A., von Keyserlingk, M.A.G., Weary, D.M., 2009. Cow prefer-
ence and usage of free stalls compared with an open pack area. J. Dairy Sci. 92, 5497–5502. Galindo, F., Broom, D.M., 2000. The relationships between social behaviour of dairy cows and the occurrence of lameness in three herds. Res. Vet. Sci. 69, 75–79. Galindo, F., Broom, D.M., Jackson, P.G.G., 2000. A note on possible link between behaviour and the occurrence of lameness in dairy cows. Appl. Anim. Behav. Sci. 67, 335–341. Goldhawk, C., Chapinal, N., Veira, D.M., Weary, D.M., von Keyserlingk, M.A.G., 2009. Prepartum feeding behavior is an early indicator of subclinical ketosis. J. Dairy Sci. 92, 4971–4977. Gomez, A., Cook, N.B., 2010. Time budgets of lactating dairy cattle in commercial freestall herds. J. Dairy Sci. 93, 5772–5781. Jensen, M.B., Pedersen, L.J., Munksgaard, L., 2005. The effect of reward duration on demand functions for rest in dairy heifers and lying requirements as measured by demand functions. Appl. Anim. Behav. Sci. 90, 207–217. Ito, K., von Keyserlingk, M.A.G., LeBlanc, S.J., Weary, D.M., 2010. Lying behavior as an indicator of lameness in dairy cows. J. Dairy Sci. 93, 3553–3560. Leach, K.A., Logue, D.N., Randall, J.M., Kempson, S.A., 1998. Claw lesions in dairy cattle: methods for assessment of sole and white line lesions. Vet. J. 155, 91–102. Leonard, F.C., O’Connell, J.M., O’Farrell, K.J., 1996. Effect of overcrowding on claw health in first-calved Friesian heifers. Brit. Vet. J. 152, 459–472. Lischer, C., Ossent, P., 1994. Klauenrehe beim Rind: eine Literaturübersicht (Laminitis in cattle: a literature review). Tierarztliche Praxis 22, 424–432. Livesey, C.T., Harrington, T., Johnston, A.M., May, S.A., Metcalf, J.A., 1998. The effect of diet and housing on the development of sole haemorrhages, white line haemorrhages and heel erosions in Holstein heifers. Anim. Sci. 67, 9–16. Manson, F.J., Leaver, J.D., 1988. The influence of concentrate amount on locomotion and clinical lameness in dairy cattle. Anim. Prod. 47, 185–190. Mülling, C., Green, L.E., Barker, Z.E., Scaife, J.R., Amory, J.R., Speijers, M., 2006. In: Navetat, H., Schelcher, F. (Eds.), Risk Factors associated with foot lameness in dairy cattle and a suggested approach for lameness reduction. Proc. 26th World Buiatrics Congress, Nice, 2006. , pp. 118–129. Murray, R.D., Downham, D.Y., Clarkson, M.J., Faull, W.B., Hughes, J.W., Manson, F.J., Merritt, J.B., Russell, W.B., Sutherst, J.E., Ward, W.R., 1996. Epidemiology of lameness in dairy cattle: description and analysis of foot lesions. Vet. Rec. 138, 586–591. Olmos, G., Boyle, L., Hanlon, A., Patton, J., Murphy, J.J., Mee, J.F., 2009. Hoof disorders, locomotion ability and lying times of cubicle-housed compared to pasture-based dairy cows. Livest. Sci. 125, 199–207. Proudfoot, K.L., Weary, D.M., von Keyserlingk, M.A.G., 2010. Behavior during transition differs for cows diagnosed with claw horn lesions in mid lactation. J. Dairy Sci. 93, 3970–3978. SAS Institute Inc., 2007. SAS OnlineDoc® 9.1.3. In: SAS Institute Inc., Cary, NC. Smilie, R.H., Hoblet, K.H., Eastridge, M.L., Weiss, W.P., Schnitkey, G.L., Moeschberger, M.L., 1999. Subclinical laminitis in dairy cows: use of severity of hoof lesions to rank and evaluate herds. Vet. Rec. 144, 17–21. Somers, J.G.C.J., Frankena, K., Noordhuizen-Stassen, E.N., Metz, J.H.M., 2003. Prevalence of claw disorders in Dutch dairy cows exposed to several floor systems. J. Dairy Sci. 86, 2082–2093. Tucker, C.B., Weary, D.M., 2004. Bedding on geotextile mattresses: how much is needed to improve cow comfort? J. Dairy Sci. 87, 2889–2895. Tucker, C.B., Weary, D.M., Fraser, D., 2004. Free-stall dimensions: effects on preference and stall usage. J. Dairy Sci. 87, 1208–1216. Tucker, C.B., Weary, D.M., Fraser, D., 2005. Influence of neck-rail placement on free-stall preference, use, and cleanliness. J. Dairy Sci. 88, 2730–2737. Urton, G., von Keyserlingk, M.A.G., Weary, D.M., 2005. Feeding behavior identifies dairy cows at risk for metritis. J. Dairy Sci. 88, 2843–2849. USDA (United States Department of Agriculture), 2010. Dairy 2007: Facility characteristics and cow comfort on U.S. dairy operations, 2007, p. 59. USDA–APHIS–VS, CEAH. Fort Collins, CO #524.1210. Webster, A.J.F., 2001. Effects of housing and two forage diets on the development of claw horn lesions in dairy cows at first calving and in first lactation. Vet. J. 162, 56–65.
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Applied Animal Behaviour Science journal homepage: www.elsevier.com/locate/applanim
Effects of behaviour on the development of claw lesions in early lactation dairy cows Sabine Dippel a,∗ , Cassandra B. Tucker b , Christoph Winckler a , Daniel M. Weary c a BOKU – University of Natural Resources and Life Sciences, Vienna, Department of Sustainable Agricultural Systems, Division of Livestock Sciences, Gregor-Mendel-Strasse 33, 1180 Vienna, Austria b University of California, Animal Science Department, 1 Shields Ave, Davis, CA 95616, USA c Animal Welfare Program, University of British Columbia, 2357 Main Mall, Vancouver, BC V6T 1Z4, Canada
a r t i c l e
i n f o
Article history: Accepted 6 June 2011 Available online 2 July 2011 Keywords: Lameness Cow comfort Sole haemorrhage White line separation Standing time
a b s t r a c t Claw lesions such as haemorrhages (HAEM) or white line separation (WLS) are caused by a variety of factors. The aim of this study was to assess the relationship between behaviour and the development of claw lesions. Holstein cows (n = 33) were housed in four pens with sand-bedded cubicles and solid concrete flooring, and stocked at two different densities in order to increase variation in cubicle use. Lying, feeding and standing behaviour were recorded for 48 consecutive hours per week during the first 3 weeks after calving using 10 min scan sampling from video. Claw health was scored at approximately 11, 40, 69, and 95 days after calving. For each time point and cow, we calculated four hoof health scores by summing the respective lesion severity scores for all four feet: total HAEM (HAEMT), HAEM sole only (HAEM-S), HAEM white line only (HAEM-W), and total WLS (WLS-T). Analysis consisted of linear mixed models with repeated observations and HAEM-T, HAEMS, HAEM-W and WLS-T, respectively, as dependent variables. The lesion scores at first claw scoring were included as covariates in each model. Cows that spent more time standing with their front feet in the cubicle had significantly higher haemorrhage scores in all feet (HAEM-T). Lying time was not associated with any of the lesion scores, perhaps because cubicle design and management encouraged reasonable lying times (11.0 h/d on average). In conclusion, standing partially in the cubicle increased the risk of claw haemorrhages in dairy cows after calving. Barns should be designed and managed to minimize this behaviour. © 2011 Elsevier B.V. All rights reserved.
1. Introduction Lameness is one of the most important health and welfare problems in dairy cows. On average one quarter of cows are lame at a given time (Espejo et al., 2006), while on single farms more than 80% of the herd can be affected
∗ Corresponding author. Current address: Institute of Animal Welfare and Animal Husbandry, Friedrich-Loeffler-Institut, Doernbergstr. 25/27, 29223 Celle, Germany. Tel.: +49 5141 3846200; fax: +49 5141 3846117. E-mail addresses: [email protected], sabine.dippel@fli.bund.de (S. Dippel). 0168-1591/$ – see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.applanim.2011.06.006
(Dippel et al., 2009b). Lesions in the claws, such as sole ulcers, are known to be an important source of lameness (Murray et al., 1996). The causation of lameness and claw lesions is complex and includes risk factors such as nutrition (Manson and Leaver, 1988), housing (Somers et al., 2003) and genetics (Boelling and Pollott, 1998). Dairy cows in the northern hemisphere are commonly kept in cubicle barns with solid or slatted concrete flooring in the walking area, and stalls (“cubicles”) with rubber mats, cow mattresses or deep bedding as a lying surface. In these barns standing behaviour is thought to be associated with claw health for several reasons. Firstly, while cows are standing on concrete flooring, which is typically provided
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outside of the stall, their claws are exposed to mechanical forces which can cause damage through trauma or excessive weight bearing (Lischer and Ossent, 1994). Secondly, claws may be in contact with manure slurry while standing which can soften the horn and thus possibly increase risk of injury (Borderas et al., 2004). Cows with longer daily standing times have been found to have more claw lesions and lameness (Leonard et al., 1996; Galindo and Broom, 2000). Similarly, longer standing times before calving are associated with the development of haemorrhages after calving; after calving, animals with haemorrhages have shorter standing times (Chapinal et al., 2009b). In addition, parameters associated with lying comfort such as type of cubicle surface and abnormal lying behaviour have been associated with lameness in on-farm surveys (Dippel et al., 2009a). Another potential risk behaviour is time spent standing with only the front feet in the cubicle (“perching”), a behaviour related to cubicle comfort (Tucker et al., 2004). Cows who spend more time perching in a cubicle have been found to be more likely to become lame (Galindo et al., 2000; Proudfoot et al., 2010). However, the causal nature of this relationship is not clear, as the weight distribution of cows standing with front feet raised is not different from cows standing level (Chapinal et al., 2009a). Finally, as with standing in the alley, partially standing in the cubicle increases exposure of the hind feet to slurry, and moisture. In addition to behaviour performed in the cubicle, feeding behaviour may also be related to claw health. Cows spend a considerable amount of time eating and reductions in feeding time or intake around partition are related to other disorders, such as metritis and ketosis (Urton et al., 2005; Goldhawk et al., 2009). Furthermore, changes in diet, specifically increases in concentrate intake, are associated with an increase in claw lesions around the time of calving (Livesey et al., 1998). The combination of changes in feeding behaviour and an increase in concentrates in the diet during the transition period indicates that time spent feeding may be an important factor influencing claw health. In general, the period of highest risk for claw lesion development is the time around calving because of the major physiological and environmental changes taking place. Most claw lesions are related to disruption of the horn producing tissue (corium) inside the claws. Causes of disruption include a decline in rumen-pH (acidosis) due to a high carbohydrate:fibre ratio in the diet, endotoxinemitting infections like metritis, or mechanical overload due, for example, to prolonged standing on a hard surface (Lischer and Ossent, 1994; Livesey et al., 1998; Mülling et al., 2006). Damage to the corium causes blood infiltration into the horn and diminishes horn quality. The modified horn grows outwards and becomes visible as discolorations and low quality horn on the surface of the claw approximately 6–16 weeks later (Bergsten and Frank, 1996; Mülling et al., 2006). Our aim was to investigate the effects of time spent standing with the front feet in a cubicle, feeding and lying during the first 3 weeks after calving on the development of claw lesions up to 13 weeks after calving. As lying
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time of cows housed in cubicles decreases with increasing stocking density (Fregonesi et al., 2007), we manipulated stocking density in order to increase variation in cubicle use. 2. Materials and methods 2.1. Animals and housing conditions The experiment was conducted at the UBC Dairy Education & Research Centre, Agassiz (BC), Canada. We housed 48 Holstein cows, in four groups of 12, in 3-row pens with sand-bedded cubicles and solid concrete flooring, with automatic scrapers on a 6-h-schedule. All cows entered the experiment within one day from calving. In order to keep group size constant, experimental pens had been stocked with non-experimental cows at the start of the experiment, which were replaced one by one by experimental cows. Cows were randomly assigned to pens and blocked by lactation number and 305-day yield of the previous lactation. Median lactation number was two (range one to eight) and mean previous 305-day yield was 11,623 ± 2080 kg (mean ± SD). As not all cows calved on the same day it took 19, 26, 29 and 32 days for groups to become established. Cows spent 91–102 days on the experiment (mean: 95 days). Two groups were housed at a 1:1 cow-to-cubicle ratio (“100%”; two primiparous and three multiparous (pen 1), and three primiparous and nine multiparous cows (pen 3); Fig. 1) and two groups were overstocked at 1.3 cows per cubicle (“133%”; one primiparous and three multiparous (pen 2), and three primiparous and nine multiparous cows (pen 4)). Stocking densities in excess of 100% are common on commercial farms, for example a recent US survey found that 30.4% of cubicle farms housed cows at ≥110% (USDA, 2010). In the 133% condition walking area allowance was reduced from 5.33 m2 /cow to 4.71 m2 /cow and feeding space decreased from 0.61 m/cow to 0.54 m/cow. This was achieved by blocking off the dead-end side of the pen perpendicular to the feed face (Fig. 1). Each pen contained head-to-head and head-to-wall cubicles. Cubicle width was 120 cm and cubicle lengths 240 cm (head-to-head) and 270 cm (head-to-wall). The neckrail was located 160 cm from the curb and the neckrailcurb diagonal was 206 cm. Cubicles were bedded every 10–14 days with washed river sand (max. grain size 2 mm). The entire herd was milked at 05:00 h and 15:00 h in a double-twelve side-by-side parlour in the same building, and cows were out of the pen for approximately 1 h per milking. Cows were fed fresh total mixed ration (roughage mixed with concentrates) ad libitum after every milking (feed bunk with open rails). The ration contained 45.6% dry matter (DM) and was composed of 15.7% maize silage, 37.2% protein/mineral/energy supplement, 11.6% grass silage, 17.2% flattened maize/barley mix, 9.9% grass hay, and 8.4% alfalfa hay. Crude protein was 17.8%, net energy for lactation 0.76%, acid detergent fibre 18.0%, neutral detergent fibre 33.2%, calcium 0.73%, phosphorus 0.41%, and sodium 0.2% (all DM %). Before calving, cows and heifers had been housed in the same barn. Every cow had been hoof-trimmed by a professional hoof trimmer at dry
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Fig. 1. Layout of experimental pens. Grey areas = cubicles, hatched areas = blocked off for overstocking.
off. All animals were cared for according to the guidelines of the Canadian Council on Animal Care (1993). 2.2. Behavioural observations Behaviour was recorded for 48 consecutive hours per week (starting after afternoon milking) for 3 weeks after calving using time-lapse video with two cameras per pen (Panasonic WV-BP330 cameras with Pelco Varifocal Lenses in combination with Panasonic Time Lapse Video Cassette Recorder AG-6540 and Panasonic Video Multiplexer WJ-FS216). Lying, feeding, and standing behaviour were recorded using 10 min scan sampling with the following definitions: lying = ventral part of body touches ground completely (none of the cows lay down in the walking area), feeding = standing at feed bunk with head above bunk, standing with front feet in cubicle = standing with both front feet in cubicle and rear feet in alley. Time budgets were expressed as percent of positive scans per total scans of one 48 h observation period (= weekly value). Weekly values were summarized by calculating the mean and extreme values across weeks. The latter refers to the smallest value for lying and feeding and the largest value for standing with front feet in the cubicle (based on their predicted effect on claw lesions) from weeks 1, 2 and 3, respectively. For nine of the cows included in analysis, there were only data from two weeks of observation available due to technical problems. 2.3. Claw lesion recording The claws of all animals were scored four times at 4week intervals (T1 to T4). At T1, cows were on average 11 days post partum (days in milk (DIM); range 7–18), at T2 40 DIM (35–46), at T3 69 DIM (65–77), and at T4 95 DIM (91–102). A professional hoof-trimmer (Giroux Hoof Trimming, Agassiz, Canada) cleaned and pared approximately 1 mm off the surface of the claws before lesions were scored by a single trained observer. Lesions were recorded separately in five zones (following the 6th Symposium on Diseases of the Ruminant Digit, Liverpool, 1990). For analysis we merged values from zones
1 to 3 as “white line” and 4 and 5 as “sole”. Haemorrhages (HAEM) were scored on the entire distal surface based on the arithmetic system of Leach et al. (1998), which distinguishes lesions based on their colouration and changes in horn structure (Table 1). White line separation (WLS) was scored using a five point scale ranging from striation to separations wider than 2 mm (modified after Smilie et al., 1999; Table 1). We defined striation as more than five regularly spaced black stripes perpendicular to the white line, and a solid black line as completely black discoloration of the white line at least as long as five striation lines. We used the number of striation lines as length parameter instead of measurements because striation lines are equally spaced independently of the curve of the white line and can still be distinguished even if the white line is black (solid black line). Visibly distinct lesions were scored separately. During the experiment all cows were treated twice for digital dermatitis (topical treatment with 9.91 g/L LincoSpectinTM 100 solution in the milking parlour once a day on 3 consecutive days). Digital dermatitis occurred only rarely after treatments and therefore was not analysed. There were no cases of interdigital skin hyperplasia. The respective HAEM and WLS severity scores given to all single lesions found were summed up for T1, T2, T3 and T4, respectively (’sum of arithmetic severity scores’;
Table 1 Scoring keys for haemorrhages (Leach et al., 1998) and white line separation (modified after Smilie et al., 1999). Severity score
Haemorrhage
0
No alterations visible on distal surface Diffuse red or yellow Stronger red Deep dense red Port coloration
1 2 3 4 5 6 7 8
Red, raw, possibly fresh blood Corium exposed Severe ulcer–major loss of horn Infected ulcer
White line separation
Striation (>5 lines), dirt Solid black line Parting <2 mm Parting >2 mm, wall completely split off
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following Leach et al., 1998). This approach allows us to distinguish cows with several severe injuries from those with multiple, less severe injuries. This was important because in this study the sample size was insufficient to categorize animals as healthy or injured. We calculated four summary scores for each cow: total sum of haemorrhages (HAEM-T), sum of haemorrhages in the sole (HAEM-S), sum of haemorrhages in the white line (HAEM-W), and total sum of WLS (WLS-T). 2.4. Statistical analysis The data of 15 cows had to be dropped because of completely missing behaviour observations. This left 33 cows for analysis, nine primiparous and 24 multiparous. Data presented therefore refer to the 33 cows included in analysis only. Linear mixed models for HAEM-T, HAEMS, HAEM-W and WLS-T were calculated in SAS 9.1.3 (SAS Institute Inc., 2007) with the independent factors lying, feeding, and standing with only the front feet in cubicles. ‘Initial score’ was included as covariate and was kept in the models regardless of its significance in order to correct estimates for its influence. We calculated two models for each outcome: one with mean and one with extreme behaviour values. Mean lying time was correlated negatively with mean time standing with front feet in cubicles (rSpearman = −0.41, P = 0.017, n = 33 cows) so models were also calculated without mean lying. However, the estimates and p-values of models with and without mean lying were virtually identical to those from the models containing all behaviours. Therefore, only the models containing all behaviours are presented. Unlike the mean behaviour
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values, the extreme values for the three behaviours were not correlated (rSpearman = −0.16 to −0.30, P > 0.086, n = 33 cows). Models were calculated with PROC MIXED with period (T2 to T4) specified in the REPEATED statement and cow, nested by group, specified as repeated SUBJECT. The covariance-structure was defined as unstructured (selected via best fit based on Akaike information criterion and Schwarz Bayesian criterion). Residuals were evaluated visually (ODS GRAPHICS and RESIDUAL option). Finally, to investigate how injuries varied between front and hind claws, the HAEM-T scores in hind and front claws were compared at given claw scorings using Wilcoxon signed rank test in PROC UNIVARIATE. For all analyses, p-values less than 0.05 were regarded as indicating statistical significance. 3. Results 3.1. Dataset characteristics Cows spent on average 11.0 ± 2.2 h/d (mean ± SE) lying down, 4.5 ± 0.9 h/d feeding, and 2.3 ± 1.2 h/d standing with their front feet in cubicles. Averages of the minimum values were 9.8 ± 2.4 h/d for lying time and 3.9 ± 0.9 h/d feeding time. The average maximum time cows spent standing with their front feet in cubicles was 3.0 ± 1.6 h/d. The highest score for a single haemorrhage found on any one cow (Table 1) ranged from 1 to 5, and no cows had an ulcer. The maximum white line separation score/cow ranged from 1 to 4. The summary scores/cow were distributed as follows (means and ranges across T2, T3 and
Fig. 2. Total haemorrhage scores (HAEM-T), sum of haemorrhage scores in the sole (HAEM-S), sum of haemorrhage scores in the white line (HAEM-W) and total score sums of WLS (WLS-T) across claw scorings (T1 to T4; animal level scores).
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Fig. 3. Mean haemorrhage score sums/cow in front and hind claws across claw scorings (T2 to T4). n = 33 cows. *P < 0.001. Error bars represent the respective standard errors.
T4): HAEM-T 27.6 (7–70), HAEM-S 16.3 (4–50), HAEM-W 11.3 (0–28), WLS-T 38.6 (20–68). Lesion scores increased over time (Fig. 2). For HAEMT this increase was mainly due to increased lesions in the hind claws, which at T3 and T4 had higher scores than the front claws (P < 0.001; Fig. 3). 3.2. Relationship between behaviour and lesions Total haemorrhages (HAEM-T) were associated with time spent standing with front feet in cubicles and initial HAEM-T score (Table 2). Both mean and maximum time spent standing with front feet in the cubicles were associated with HAEM-T. HAEM-S was only associated with standing with front feet in cubicles (both mean and maximum) while HAEM-W were only associated with initial HAEM-W score. Only initial WLS-T score was associated with subsequent WLS-T. No measure of feeding or lying time was associated with lesion scores. 4. Discussion In general, the cows studied in this experiment had reasonably good claw health, as shown by the absence of ulcers. In contrast, sole ulcer prevalence was 14% in the study by Leonard et al. (1996) and 17% in Chapinal et al. (2009b). Of the behaviours studied, only time spent standing with the front feet in a cubicle was associated with claw lesions. Overall, cows that spent more time standing with front feet in cubicles had higher HAEM-T and higher HAEMS scores. This agrees with results from Proudfoot et al. (2010), who (two weeks before and 24 h after calving) found more standing with front feet in a cubicle in cows who developed sole lesions later in lactation. There are at least three potential explanations for this relationship: (1) standing with two feet in the cubicle increases weight bearing on the hind claws, (2) this behaviour corresponds with other possible risk factors such as social status, and (3) standing in this way increases exposure to slurry, thus increasing the risk for impaired hoof health. The first idea, that standing with the front feet in the cubicle increases
weight bearing by hind claws resulting in increased risk of injury, is unsupported. In a study where cows stood on load cells with the front feet raised, there was no difference in weight bearing by the hind feet compared to when the front and hind feet were level (Chapinal et al., 2009a). The second idea is based in part on the finding that subordinate cows spend more time standing partially in the cubicle compared to dominant animals (e.g. Galindo and Broom, 2000) and subordinates may be at greater risk for claw injuries for other reasons, such as sudden turns caused by displacements. Unfortunately, there is no empirical evidence to address this link. The third idea is well supported; standing with the front feet in the cubicle increases exposure of the hind feet to both manure and concrete. Exposure to moisture and manure decrease hoof hardness (Borderas et al., 2004) and cows kept in systems that limit exposure to both slurry and concrete have improved hoof health (Bergsten and Herlin, 1996; Livesey et al., 1998). Regardless of the mechanism, these results indicate that standing with the front two feet in the cubicle should be minimized. It is possible that development of the lesions caused the differences in behaviour, rather than vice versa. The findings described in this study show a relationship between standing partially in the cubicle and lesions, but cannot be used to definitively establish causation. However, we argue that it was the behaviour that led to changes in lesions development based on two lines of reasoning. The first is that cows differed in behaviour in the first few weeks after calving, well before the majority of lesions had developed. However, sole lesions only become visible weeks after damage to the corium occurs (Mülling et al., 2006) so the time course of the behavioural changes relative to injury is difficult to establish. More convincing are the results from Bernardi et al. (2009) who manipulated cubicle design (by making the neck rail less restrictive) reducing the time cows spent standing with their front feet in the cubicle. Lameness then declined in weeks that followed providing stronger evidence that lameness is varying as a result of the change in behaviour, rather than vice versa. Several aspects of housing design and management influence standing partially in the cubicle. A number of studies have shown that restrictive neck rail placement (closer to the cubicle surface or entrance) increases standing with only two feet in the cubicle (Tucker et al., 2005; Bernardi et al., 2009; Fregonesi et al., 2009). Cows also spend more time standing partially in narrower cubicles (Tucker et al., 2004), cubicles with less bedding (Tucker and Weary, 2004) and when the ratio of cows to cubicles is over 1:1 (Fregonesi et al., 2007). Together, these results illustrate changes in cubicle design and management that can reduce standing partially in the cubicle and thus likely reduce the risk of claw injuries. Lying time and feeding time after calving were not related to lesions later in lactation. One possible explanation for the lack of relationship with lying times is that these were relatively long in the current study. Lying time averaged 11.0 h/d and was thus close to what can be regarded the behavioural need (Jensen et al., 2005); even minimum lying time averaged 9.8 h/d. Cows in earlier work that has reported an association between shorter lying time and lameness. For example, Leonard et al. (1996)
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Table 2 Results from mixed model analysis of the association between behaviour and claw lesions. Separate models were calculated for behaviour summarised as mean and extreme values recorded during 21 days after calving (unit = % of time). Extremes for feeding and lying are minimum values, extremes for standing with front feet in cubicles are maximum values. Claw lesions were analysed in the form of sums of single lesion severity scores/cow, repeatedly recorded three times within 14 weeks after calving. The respective sums of lesion severity scores directly after calving (initial score) was included as covariate. n = 33 cows, DF = 28. Dependent a
Behaviour summary
Factor
Estimate
Standard error
T
HAEM-T
Extreme
Intercept Initial HAEM-T score Feeding Lying Standing with front feet in cubicles Intercept Initial HAEM-T score Feeding Lying Standing with front feet in cubicles
21.14 0.45 −0.48 0.01 0.44 31.41 0.36 −0.70 −0.06 0.50
12.11 0.19 0.36 0.15 0.18 16.03 0.19 0.39 0.18 0.23
1.8 2.4 −1.3 0.1 2.4 2.0 1.9 −1.8 −0.4 2.2
0.092 0.022 0.192 0.948 0.025 0.060 0.066 0.088 0.729 0.039
Intercept Initial HAEM-S score Feeding Lying Standing with front feet in cubicles Intercept Initial HAEM-S score Feeding Lying Standing with front feet in cubicles
15.38 −0.04 −0.29 −0.02 0.52 19.31 −0.08 −0.34 −0.06 0.65
8.03 0.15 0.25 0.10 0.13 9.88 0.14 0.25 0.11 0.15
1.9 −0.2 −1.2 −0.2 4.1 2.0 −0.6 −1.4 −0.5 4.4
0.066 0.813 0.241 0.814 <0.001 0.061 0.567 0.181 0.596 <0.001
Intercept Initial HAEM-W score Feeding Lying Standing with front feet in cubicles Intercept Initial HAEM-W score Feeding Lying Standing with front feet in cubicles
10.95 0.86 0.18 −0.13 0.00 15.59 0.78 −0.03 −0.12 −0.06
7.92 0.30 0.25 0.10 0.12 10.92 0.32 0.28 0.12 0.16
1.4 2.9 0.7 −1.3 0.0 1.4 2.5 −0.1 −1.0 −0.4
0.178 0.007 0.466 0.213 0.996 0.165 0.020 0.912 0.344 0.731
Intercept Initial WLS-T score Feeding Lying Standing with front feet in cubicles Intercept Initial WLS-T score Feeding Lying Standing with front feet in cubicles
36.65 0.32 −0.26 −0.11 0.05 33.86 0.31 −0.09 −0.09 0.09
8.57 0.09 0.26 0.11 0.13 10.93 0.09 0.28 0.13 0.17
4.3 3.4 −1.0 −1.1 0.4 3.1 3.4 −0.3 −0.7 0.5
<0.001 0.002 0.332 0.302 0.696 0.004 0.002 0.751 0.473 0.611
Mean
HAEM-S
Extreme
Mean
HAEM-W
Extreme
Mean
WLS-T
Extreme
Mean
P
a HAEM-T = total haemorrhage (HAEM) sum per cow, HAEM-S = HAEM sum, sole only, HAEM-W = HAEM sum white line only, WLS-T = total white line separation sum per cow.
found an increase in lesions and lameness when lying time decreased from between 7 and 10 h/d to 5 h/d. In a more recent study, Chapinal et al. (2009b) reported lying times similar to those in the current study (approximately 9–12 h/d). They found that the relationship between lying behaviour and claw health was more complex than previously identified. Cows that developed sole ulcers had a steeper decline in lying times in the weeks before calving and a more marked increase in lying several weeks after calving compared to cows without ulcers (Chapinal et al., 2009b). The increase in lying time in cows with ulcers corresponds to higher gait scores, in agreement with others that have found that severely lame cows spend more time lying down (Ito et al., 2010; Gomez and Cook, 2010). These results suggest that pre-calving and/or changes in lying
behaviour might have more impact on the development of claw lesions than does lying behaviour after calving. However, pre-calving behaviour and daily changes in lying time were not assessed in the current study. Similarly, there was no relationship between time spent feeding and claw health. Cows showed little variation in feeding times, making it difficult to evaluate how variation in this parameter relates to claw lesions. In previous work linking health disorders after calving with feeding behaviour (Proudfoot et al., 2010), the period two weeks before and 24 h after calving seems particularly important, but this period was not investigated in the current work. Several studies have shown that keeping cows on pasture can also reduce the risk of lesions and lameness (Olmos et al., 2009). Cows housed indoors on bedded pack also have
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better hoof health (Webster, 2001). Indeed, the results from the current study suggest that one common feature reducing the risks is the lack of opportunity to stand partially in a cubicle. Together, our results and those of other studies indicate that, environments that allow cows to stand on clean, non-concrete standing surfaces are likely beneficial for hoof health. 5. Conclusions Standing with the front feet in the cubicle and the hind feet in the alley is associated with increased risk of claw haemorrhages later in lactation. These results indicate that dairy barns should be designed and managed to minimize time cows spend standing with their front feet in cubicles. Acknowledgements We thank Nelson Dinn and his team of the University of British Columbia’s Dairy Education and Research Centre, and Katie Lowe, Michelle Drissler, Kiyomi Ito, Frances Flower, Julie Huzzey, and Lorna Baird for their assistance. The project was funded by the Natural Sciences and Engineering Research Council of Canada through the Industrial Research Chair in Animal Welfare, and by contributions from the Dairy Farmers of Canada and many others listed at www.landfood.ubc.ca/animalwelfare/. Additional funding was provided to the first author through a “DAAD Doktorandenstipendium” from German Academic Exchange Service. References Bergsten, C., Frank, B., 1996. Sole haemorrhages in tied heifers in early gestation as an indicator of laminitis: effects of diet and flooring. Acta Vet. Scand. 37, 375–381. Bergsten, C., Herlin, A.H., 1996. Sole haemorrhages and heel horn erosion in dairy cows: The influence of housing system on their prevalence and severity. Acta Vet. Scand. 37, 395–408. Bernardi, F., Fregonesi, J., Winckler, C., Veira, D.M., von Keyserlingk, M.A.G., Weary, D.M., 2009. The stall-design paradox: neck rails increase lameness but improve udder and stall hygiene. J. Dairy Sci. 92, 3074–3080. Boelling, D., Pollott, G.E., 1998. Locomotion, lameness, hoof and leg traits in cattle II genetic relationships and breeding values. Livest. Prod. Sci. 54, 205–215. Borderas, T.F., Pawluczuk, B., de Passillé, A.M., Rushen, J., 2004. Claw hardness of dairy cows: relationship to water content and claw lesions. J. Dairy Sci. 87, 2085–2093. Chapinal, N., de Passillé, A.M., Rushen, J., 2009a. Weight distribution and gait in dairy cattle are affected by milking and late pregnancy. J. Dairy Sci. 92, 581–588. Chapinal, N., de Passillé, A.M., Weary, D.M., von Keyserlingk, M.A.G., Rushen, J., 2009b. Using gait score, walking speed, and lying behavior to detect hoof lesions in dairy cows. J. Dairy Sci. 92, 4365–4374. Dippel, S., Dolezal, M., Brenninkmeyer, C., Brinkmann, J., March, S., Knierim, U., Winckler, C., 2009a. Risk factors for lameness in cubicle housed Austrian Simmental dairy cows. Prev. Vet. Med. 90, 102–112. Dippel, S., Dolezal, M., Brenninkmeyer, C., Brinkmann, J., March, S., Knierim, U., Winckler, C., 2009b. Risk factors for lameness in freestallhoused dairy cows across two breeds, farming systems, and countries. J. Dairy Sci. 92, 5476–5486. Espejo, L.A., Endres, M.I., Salfer, J.A., 2006. Prevalence of lameness in highproducing Holstein cows housed in freestall barns in Minnesota. J. Dairy Sci. 89, 3052–3058. Fregonesi, J.A., Tucker, C.B., Weary, D.M., 2007. Overstocking reduces lying time in dairy cows. J. Dairy Sci. 90, 3349–3354. Fregonesi, J.A., von Keyserlingk, M.A.G., Weary, D.M., 2009. Cow prefer-
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