|
|
||||||||





* Department of Sustainable Agricultural Systems, Division of Livestock Sciences, BOKU—University of Natural Resources and Applied Life Sciences Vienna, Gregor-Mendel-Strasse 33, 1180 Vienna, Austria
Institut für Populationsgenetik, University of Veterinary Medicine Vienna, Josef Baumanngasse 1, 1210 Vienna, Austria
Department of Farm Animal Behaviour and Husbandry, FB 11, University of Kassel, Nordbahnhofstraße 1a, 37213 Witzenhausen, Germany
Georg-August-University of Göttingen, Department of Animal Sciences, Location Vechta, Driverstrasse 22, 49377 Vechta, Germany
1 Corresponding author: s.dippel{at}web.de
| ABSTRACT |
|---|
|
|
|---|
Key Words: lameness dairy cow risk factor generalized estimating equation
| INTRODUCTION |
|---|
|
|
|---|
Lameness prevalence varies considerably between farms and regions; Winckler and Brill (2004), for example, reported a lameness prevalence range of 25 to 58%. Furthermore, the type of farming system used has an influence; lameness prevalence is usually lower on organic farms because of more extensive production (Rutherford et al., 2009). The strongest impact on lameness prevalence, however, is the specific combination of risk factors on a given farm. There is a large range of factors that could potentially increase risk of lameness, including the implementation of claw trimming (Manson and Leaver, 1988), deep litter versus cubicle housing (Webster, 2001), access to pasture (Hernandez-Mendo et al., 2007), social rank (Galindo et al., 2000), and predisposing physiological stages such as parturition and lactation (Knott et al., 2007). Strong effects of nutrition have also been found repeatedly (e.g., Manson and Leaver, 1988). Experiments with respect to lying behavior, on the other hand, are scarce and sometimes yield contradictory results (Leonard et al., 1994; Galindo and Broom, 2000).
Increased awareness of lameness as a problem and the development of herd health plans in the United Kingdom (Bell et al., 2006) raised the question of key risk areas on farms (i.e., areas that should always be included in farm assessment). Most publications regarding epidemiology of lameness investigate lameness only in similar groups of farms. Our objective was to identify risk factors for lameness that are common across a broad range of farms.
| MATERIALS AND METHODS |
|---|
|
|
|---|
|
The number of animals in the milking herd (referred to as herd size below) ranged from 24 to 145 (median = 48). All farms were members of performance recording agency and complied with certain criteria, such as uniformity of housing equipment (e.g., no mix of freestall or flooring types in milking herd). Herds were not visited in the case of peak occurrences of painful digital or interdigital dermatitis stages or if more than 50% of the animals had been trimmed within the past 4 wk. Single animals that had been trimmed within that period were excluded from examination. Average overall lameness prevalence was 34% and average prevalence of severe lameness was 16%.
Interobserver Agreement
Observers met 3 times before and once after farm visits for data collection training and to test agreement on BCS and gait scores. We used prevalence-adjusted bias-adjusted kappas (PABAK) for each observer pair as measures of agreement, which we interpreted as follows: PABAK
0.75 = excellent agreement, 0.4 to 0.75 = fair to good agreement, and <0.4 = poor agreement.
Interobserver agreement for lame versus not lame (see Table 2 for definition) was excellent in 17% and fair to good in 83% of all tests. Mean PABAK before data collection was 0.58 (range = 0.49–0.68; n = 135–150) and after data collection was 0.70 (range = 0.44–0.88; n = 50–144; see also Brenninkmeyer et al., 2007). The PABAK for BCS ranged from 0.65 to 0.95.
|
Flooring and Space Allowance.
Flooring grip was scored subjectively by standing with bent knees and weight evenly distributed, using the same rubber boots on every farm. Scores ranged from very slippery (score 0 = no grip when braking, very easy spinning) to rough (score 4 = sliding and spinning not possible, coarse and abrasive surface). The number of ridges, holes, and so on in each functional zone (e.g., main and feed alleys, parlor) was used as a measure of flooring quality (variable for analysis = more than 5 such items present, yes vs. no). Space allowance in the loafing area, both including and excluding outdoor loafing areas, was collapsed into binary variables by using the median over all farms as the threshold (Table 3).
|
We compared the diagonal distance between the neck rail and curb as well as the lunging space with recommendations based on animal size. The respective sizes were obtained by measuring subsamples of 364 HF and 295 FV cows. To ensure appropriate dimensions for 90% of cows in the herd, we used 90% quantiles of measurements. The 90% quantile for height at withers (HW) was 148 cm for HF and 143 cm for FV, and the 90% quantile for rump diagonal (RD) was 171 cm and 170 cm for HF and FV, respectively.
Neck rail–curb diagonals were defined as too short when in at least 1 of the sampled stalls the distance from the end of the bed or the inner side of curb to the lower side of the neck rail was shorter than {the square root of [(0.92 x RD)2 + (0.75 x HW)2]} cm (modified from Winckler and Knierim, 2004a). Head lunge impediment was considered to be present in any of 3 conditions: 1) the brisket board height was >30 cm (Winckler and Knierim, 2004b); 2) the front rail was between 30 cm and (0.55 x HW) cm high and the stall was shorter than (0.92 x RD + 15 + 0.56 x HW) cm (Winckler and Knierim, 2004a); or 3) the front rail was at the latter height and the horizontal distance between the brisket board and the rail was <69 cm (Cook, 2005). Stall width was not used because of its lack in variation (Table 1).
Lying Behavior.
Lying behavior was observed during 2 h in the afternoon and, in some cases, in the evening. Average frequency of abnormal lying behavior per cow in the milking herd within 2 h was recorded using continuous behavior sampling. Abnormal lying behavior included interrupted lying down and rising movements, lying down or rising lasting longer than 20 s, reversed lying (lying down with hindquarters first), horse-like rising (rising with forequarters first), and dog-like sitting (sitting on hindquarters like a dog). The total durations of 4 to 43 (mean = 19) lying-down movements were recorded with a stop watch on all but 1 farm, where no such movements were observed. A movement was measured from bending the first front leg until the cow had reached its final lying position. Rising was also recorded but there were too few valid observations on several farms. Lying-down movements that took longer than 20 s were recorded as "20 s" and were included as such in farm median calculations. Abnormal lying behavior and lying-down movements were collapsed into binary variables using the farm median as a threshold (Table 3).
Body Condition and Locomotion.
Body condition was assessed, while cows were fixed in the feed rack, using a 5-score key with 0.25-unit intervals (Metzner et al., 1993; Jilg and Weinberg, 1998). The BCS range on each farm was transformed into a binary variable by using the median over all farms as threshold (Table 3). At animal level, BCS were coded in a 4-level categorical variable based on quartiles by breed. Body condition score quartiles for HF were first = 1.25 to 2.50, second = 2.75, third = 3.00 to 3.25, and fourth = 3.25 to 4.50; BSC quartiles for FV were first = 2.50 to 3.50, second = 3.75, third = 4.00, and fourth = 4.25 to 5.00. After BCS scoring, cows were released one by one and their locomotion was scored following Winckler and Willen (2001; Table 2). During gait assessment, cows walked along the alleys inside the barn at their own speed. The observer followed behind and, if needed, encouraged the cow by calling or gently nudging to make her walk continuously. Gait scores were transformed into binary lameness scores by classifying scores 1 and 2 as not lame and scores 3 to 5 as lame (Table 2).
In herds with up to 30 lactating animals present, all animals were scored. In larger herds sample size was based on Dohoo et al. (2003), resulting in 22 to 52 (mean = 34) cows being scored per farm. Cows were selected randomly in the feed rack, in the milking parlor, or from a list. Nonlactating animals in the milking herd and cows in sick pens were excluded.
Data Management and Analysis
Data quality with respect to errors, missing values, variable distribution, and outliers was assured using descriptive statistics (PROC FREQ and PROC UNIVARIATE) in SAS (version 9.1.3; SAS Institute, 2008). All continuous variables that did not satisfactorily cover the whole range of measurements were categorized such that at least 20% of observations fell in each class. If this was not possible, the variable was excluded from analysis. The latter was the case for transition feeding in the strict sense of gradually changing forage and concentrate over more than 21 d (applied on only 7% of farms) and routine claw trimming, which was implemented at least once per year by 85% of farms overall and all farms in data subset A. The factors BCS, parity, and fat:protein ratio were kept because we considered them to be important factors even though only 19% of observations fell in a class.
Several cows had to be excluded after locomotion scoring because of events unknown at the time of scoring that interfered with locomotion (e.g., single animal claw trimmed less than 4 wk prior, or animal acquired less than 1 yr prior). Cows with more than 650 DIM were also excluded, resulting in a data set with 3,258 cows.
Finally, the data set was split into a model-building sample (MOD) containing 85% of observations of each farm (n = 2,720 cows), and a cross-validation sample (VAL) with 15% of observations (n = 538) (PROC SURVEYSELECT, METHOD = SRS, STRATA = farm). Mean lameness prevalence was 34% overall before splitting and 33% and 36% in sample data sets MOD and VAL, respectively.
Logistic Regression
We calculated logistic regression models with generalized estimating equations (GEE; Liang and Zeger, 1986) with compound symmetry covariance structure (Dohoo et al., 2003) using the REPEATED statement and logit link function in PROC GENMOD in SAS (version 9.1.3; SAS Institute, 2008). Compound symmetry matrices and GEE account for the data set covariance structure of correlated measurements (cows within the same farm; Dohoo et al., 2003; SAS Institute, 2008).
Identification of statistically significant risk factors comprised several steps, all of which were performed with sample data set MOD. First, all variables in Table 4 were screened for their univariate association with the outcome, using a Wald statistic P-value
0.2 as a threshold (SAS option WALD, version 9.1.3; SAS Institute, 2008).
|
After manual backward selection within each cluster using a significance threshold of PWald
0.05, all significant variables in a particular cluster were combined into 1 model that was also backward selected. The resulting overall model formed the base for manual stepwise selection (PWald
0.05) from all variables not included in the model. All remaining variables were retested one by one in the model and the variable with the lowest PWald was added. After each variable inclusion, any variables with PWald > 0.05 were removed before new variables were tested. The procedure was stopped when no significant variable could be entered without causing collinearity problems.
Finally, the remaining variables were evaluated for confounding in the form of estimate changes greater than 30% in variables of interest (Dohoo et al., 2003) by adding the possible confounders one by one to the model. No such changes were caused and no variables were added to the model. Interactions were not estimated because they made the model unstable. P-values for least squares means differences were step-down Bonferroni-corrected.
| RESULTS |
|---|
|
|
|---|
![]() |
) ijklmnop; µ = intercept; βi to βo = estimates for variables Xi to Xo, respectively.
Risk for lameness increased with decreasing lying comfort, that is, more frequent abnormal lying behavior, mats or mattresses used as a stall base compared with deep-bedded stall bases, the presence of head lunge impediments, or neck rail–curb diagonals that were too short (Table 5). High-parity cows as well as cows in the lowest BCS quartile (BCS from 1.25 to 2.50 in HF and 2.50 to 3.50 in FV) generally had a distinctly higher risk of being lame. Factors abnormal lying behavior, BCS, stall base, and parity were highly significant in the MOD calculation (PWald < 0.001). Neck rail–curb diagonal and head lunge impediment were the least significant factors (PWald = 0.017 and 0.034, respectively). Wald statistics based on sample VAL were much lower. Parity was still highly significant, with PWald < 0.001, followed by abnormal lying behavior (PWald = 0.013). None of the other variables were significant at the PWald
0.05 level. Only 2 out of 15 significant odds ratios (OR) changed direction when calculated on the smaller sample. They belonged to the 2 variables with the highest P-values in the model, neck rail–curb diagonal and head lunge impediment. No OR with a P-value <0.01 changed direction.
|
|
|
| DISCUSSION |
|---|
|
|
|---|
There is a possible reversed causation between abnormal lying behavior and lameness because severe lameness can also cause abnormal or prolonged lying–standing transitions. It would have been more accurate to exclude lame cows from lying behavior observations, but prestudies showed that lying behavior observations with animal identification were not feasible because of visibility and time constraints. However, because the average prevalence of severe lameness in the data set was numerically rather low (16%), the observed behavior can essentially be regarded as an indicator for uncomfortable stall design.
Risk for lameness was more than twice as high in farms with more frequent abnormal lying behaviors than on the average farm, with very similar significant OR during cross-validation. Results to this effect have also been found by Faull et al. (1996) and in data subset A alone (Dippel et al., 2009). According to Mülleder and Waiblinger (2004), one of the crucial triggers for abnormal lying behavior is short freestall length, which impinges on head lunge space and thus hinders lying–standing transitions. This agrees with our result of an increased lameness risk on farms with a head lunge impediment. However, the OR for head lunge impediment was not very high and did not stay significant in cross-validation. Besides a possible lack in statistical power, there might be 2 reasons for this. First, our threshold of at least 1 sampled stall having an impediment might have been too strict. And second, it is just one among many factors that influences lying behavior. If head lunge is impeded, it might be balanced by, for example, wider stalls (Tucker et al., 2004). The same applies to neck rail–curb diagonal. Consequently, integrative animal-based parameters such as abnormal lying behavior are preferable to single-stall measures.
Cows not only prefer to lie on soft, deep-bedded stall bases rather than on commercial mattresses, but they also lie down for longer periods of time on deep bedding (Tucker and Weary, 2004). Again, the resulting lying times are likely to have an effect on lameness, which is reflected in various on-farm surveys (Bergsten, 1994; Espejo et al., 2006). Likewise, in the present study, risk for lameness was increased on farms that used rubber mats or cow mattresses as stall bases as opposed to straw–manure mattresses or bedded concrete. Bedded concrete was comparable to straw–manure mattresses because the bedding was usually deep enough to provide cushioning. In data subset A alone, the proportion of cows that were lying compared with the number of cows using a stall in some way (lying, standing in the stall, standing half in the stall) was also a good predictor for lameness risk (Dippel et al., 2009). However, we were not able to test it in this analysis because of an insufficient number of valid observations in one data subset.
Metabolism
We chose to use animal-based parameters, rather than laborious and expensive feed analyses, as problem indicators. Of these and the additional feeding management characteristics, only BCS predicted lameness risk across all farms. Cows in the first BCS quartile had the highest risk of being lame, which has also been observed by Espejo et al. (2006). Espejo and colleagues concluded that the low body condition was a result of lameness. They based their conclusion on the negative association between body condition and lameness score observed by Manson and Leaver (1989), as well as the shorter feeding times in lame animals found by Winckler and Brill (2004). Nevertheless, low body condition may also be a risk factor for, rather than a result of, lameness. First, feeding time is not always reduced by lameness (Singh et al., 1993). Second, DMI decreases only in severely lame cows (Bach et al., 2007), which in data subsets A and O were not very prevalent [prevalence of severe lameness (scores 4 and 5) in data subset A = 12%, O = 11%, and G = 26%]. On the other hand, low body condition predisposes cows to ketotic conditions, particularly at the start of lactation. This in turn reduces the function of the digital cushion, thereby facilitating damage to the corium (Mülling and Greenough, 2006). Because all HF cows in the first BCS quartile were underconditioned (according to the limits suggested by Metzner et al., 1993), we very likely observed the effect of body condition on lameness rather than vice versa.
Usually, increased risk for lameness is also proposed for high-condition cows as a result of overconditioning at dry-off (Gearhart et al., 1990) or higher loads on the claws (Wells et al., 1993). This was not obvious in the present study; the reason probably differs for each breed. Only 3.27% of all HF cows had BCS higher than the recommended maximum of 3.75 (Metzner et al., 1993), yet the fourth quartile contained 15% of all HF cows. Thus, the highest quartile did not represent overconditioned cows. By contrast, in FV cows the fourth quartile did represent cows considered to be overconditioned (Jilg and Weinberg, 1998), but FV represents a dual-purpose breed for which high BCS may have less effect on lameness. Moreover, FV accounted for only 27% of all cows in the model.
Parity
The strong influence of parity number agrees with other studies in this field (e.g., Groehn et al., 1992) and was established in data subset A alone (Dippel et al., 2009). Higher risk for lameness in first-parity cows caused by the combined effects of physiological, housing, and management changes around the time of parturition has been described (Bergsten, 1994). However, our result of increasing lameness risk with increasing parity number is a more consistent finding in the literature (Groehn et al., 1992; Espejo et al., 2006). The main reason for this is accumulated susceptibility: cows that have been lame are at a higher risk of becoming lame again than healthy cows (Hirst et al., 2002).
Analysis
Model sensitivity might have been improved had we investigated separate claw lesions such as sole ulcer or white line disease instead of the general parameter lameness. Risk factors for single lesions are more specific than the broad spectrum of lameness risk factors and thus are easier to determine. However, there are 3 arguments for investigating lameness. First, the relevance of single lesions for the animal could not yet clearly be determined (Flower and Weary, 2006), whereas lameness has been established as a painful condition (Whay et al., 1997). In addition, lameness restricts the natural expression of behavior, as in the previously mentioned reduced feeding times in severely lame cows (Bach et al., 2007). Last, there are practical constraints to claw lesion investigations. Farm records of lesion treatments are not a reliable source of data because farms differ in treatment protocols as well as in recordkeeping quality. Also, collecting standardized records of claw lesions in an on-farm survey is far more time consuming and expensive than recording lameness prevalences.
Model predictive ability in general was high with 71% correctly classified observations. Sensitivity, Sp, PPV, and NPV were also high, especially in the face of the complex nature of lameness causation. Furthermore, the model was reliable, as PCCO, Se, Sp, PPV, and NPV changed only little during cross-validation. The high predictive ability of abnormal lying behavior for lameness was confirmed by cross-validation, yet, other than this factor, only confounders stayed significant in the VAL calculation (Wald statistic). This could have been caused by the limited size of the cross-validation sample.
The major limitations of our study are, from a statistical point of view, the limited number of farms in the data set and its cross-sectional characteristic. In cross-sectional studies there can be issues of cause-and-effect (such as for BCS and abnormal lying behavior in this study) and of representativity because data are collected at only one point in time. However, we strove to maximize representativity by sampling only barns that had been in use for at least 1 yr with the current fittings and choosing animal-based parameters that are comparatively stable over time (e.g., milk compounds). In addition, we are positive to have solved the cause-and-effect problems of BCS and of abnormal lying behavior at a satisfactory level based on additional information in the data set.
| CONCLUSIONS |
|---|
|
|
|---|
| ACKNOWLEDGMENTS |
|---|
|
|
|---|
Received for publication April 10, 2009. Accepted for publication August 5, 2009.
| REFERENCES |
|---|
|
|
|---|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |