Accepted Manuscript Title: Housing and management factors associated with indicators of dairy cattle welfare Author: M. de Vries E.A.M. Bokkers C.G. van Reenen B. Engel G. van Schaik T. Dijkstra I.J.M. de Boer PII: DOI: Reference:
S0167-5877(14)00406-1 http://dx.doi.org/doi:10.1016/j.prevetmed.2014.11.016 PREVET 3693
To appear in:
PREVET
Received date: Revised date: Accepted date:
25-5-2014 14-11-2014 17-11-2014
Please cite this article as: de Vries, M., Bokkers, E.A.M., van Reenen, C.G., Engel, B., van Schaik, G., Dijkstra, T., de Boer, I.J.M.,Housing and management factors associated with indicators of dairy cattle welfare, Preventive Veterinary Medicine (2014), http://dx.doi.org/10.1016/j.prevetmed.2014.11.016 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Housing and management factors associated with
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indicators of dairy cattle welfare
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M. de Vriesa,*, E.A.M. Bokkersa, C.G. van Reenenb, B. Engelc, G. van Schaikd, T. Dijkstrad and I.J.M. de Boera
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a
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[email protected];
[email protected];
[email protected],
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Livestock Research, Wageningen UR, 8200 AB Lelystad, the Netherlands. E-mail address:
[email protected],
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Biometris, Wageningen University, 6700 AC Wageningen, the Netherlands. E-mail address:
[email protected],
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GD Animal Health Service, 7400 AA Deventer, the Netherlands. E-mail addresses:
[email protected];
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Animal Production Systems group, Wageningen University, 6700 AH Wageningen, the Netherlands. E-mail addresses:
[email protected].
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* Corresponding author at: Animal Production Systems group, Wageningen University, P.O. Box 338, 6700 AH Wageningen, the
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Netherlands. Tel.: +31 317 484626. E-mail address:
[email protected].
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Knowledge of potential synergies and trade-offs between housing and management factors for different aspects
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of animal welfare is essential for farmers who aim to improve the level of welfare in their herds. The aim of this
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research was to identify and compare housing and management factors associated with prevalence of lameness,
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prevalence of lesions or swellings, prevalence of dirty hindquarters, and frequency of displacements (social
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behavior) in dairy herds in free-stall housing. Seven observers collected data regarding housing and management
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characteristics of 179 Dutch dairy herds (herd size: 22-211 cows) in free-stall housing during winter. Lame
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cows, cows with lesions or swellings, and cows with dirty hindquarters were counted and occurrence of
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displacements was recorded during 120 min of observation. For each of the four welfare indicators, housing and
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management factors associated with the welfare indicator were selected in a succession of logistic or log linear
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regression analyses. Prevalence of lameness was associated with surface of the lying area, summer pasturing,
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herd biosecurity status, and far-off and close-up dry cow groups (P < 0.05). Prevalence of lesions or swellings
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was associated with surface of the lying area, summer pasturing, light intensity in the barn, and days in milk
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when the maximum amount of concentrates was fed (P < 0.05). Prevalence of dirty hindquarters was associated
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with surface of the lying area, proportion of stalls with fecal contamination, head lunge impediments in stalls,
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and number of roughage types (P < 0.05). Average frequency of displacements was associated with the time of
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introducing heifers in the lactating group, the use of cow brushes, continuous availability of roughage, floor
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scraping frequency, herd size, and the proportion cows to stalls (P < 0.05). Prevalences of lameness and of
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lesions or swellings was lower in herds with soft mats or mattresses (odd ratio (OR) = 0.66 and 0.58, confidence
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interval (CI) = 0.48-0.91 and 0.39-0.85) or deep bedding (OR = 0.48 and 0.48, CI = 0.32-0.71 and 0.30-0.77) in
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stalls, compared with concrete, and in herds with summer pasturing (OR = 0.68 and 0.41, CI = 0.51-0.90 and
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0.27-0.61), compared with zero-grazing. Deep bedding in stalls was negatively associated with prevalence of
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dirty hindquarters (OR = 0.50, CI = 0.29-0.86), compared with hard mats. It was concluded that some aspects of
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housing and management are common protective factors for prevalence of lameness, lesions or swellings, and
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dirty hindquarters, but not for frequency of displacements.
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Abstract
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Keywords: 1
dairy
cattle,
animal
welfare,
risk
factor,
environment,
housing,
management
Abbreviation: composite health score (CHS)
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Introduction
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The level of animal welfare varies considerably among dairy herds. Prevalences of lameness and hock injuries,
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for example, have been reported ranging from 0% up to 100% (Fourichon et al., 2001; Von Keyserlingk et al.,
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2012; Brenninkmeyer et al., 2013). At the same time, considerable variation between farms exists in housing and
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management conditions that are expected to affect dairy cattle welfare (Von Keyserlingk et al., 2012). This
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suggests there is room for improvement of dairy cattle welfare.
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Improvement of the level of welfare on a farm by adjusting housing or management factors is complicated
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because animal welfare is a multidimensional concept (Fraser, 1995). This multidimensionality is illustrated by
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the fact that animal welfare comprises not only physical (i.e. health and vigor), but also psychological aspects
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(i.e. sense and feeling; Webster, 2005). Consequently, animal welfare assessment requires the use of multiple
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indicators. The Welfare Quality protocol for cattle, for example, includes indicators relating to the aspects of
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feeding, housing, health, and behavior (Welfare Quality, 2009). Welfare indicators relating to similar aspects of
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animal welfare have been associated with similar housing and management factors. For example, lameness and
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skin lesions are welfare indicators related to dairy cattle health, and both have been associated with surface of the
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lying area in free-stalls and with pasturing (e.g. Haskell et al., 2006; Brenninkmeyer et al., 2013; Chapinal et al.,
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2013). This may be partly due to biological relations between these two indicators. For indicators related to
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different aspects of animal welfare, however, it is largely unknown whether they are influenced by similar-, or
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by different housing and management factors, and whether changing a factor has opposite (trade-off) or synergic
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effects on these indicators. Positioning the neck rail of the free-stall further from the rear curb, for example, was
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a protective factor for lameness and for hair loss at the hocks (synergy), but it has also been associated with
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decreased cow cleanliness due to defecation in the stall (trade-off; e.g. Bernardi et al., 2009; Dippel et al., 2009;
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Fregonesi et al., 2009; Potterton et al., 2011).
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Knowing potential synergies and trade-offs of housing and management factors for different indicators of animal
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welfare is essential for farmers who aim to improve the overall welfare level of their herd. Because housing and
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management factors associated with dairy cattle welfare can differ across regions, due to, for example,
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geographical differences in housing design and popular opinions of best practices in the area (Chapinal et al.,
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2013), identification and comparison of factors associated with dairy cattle welfare is preferably done in the
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same population. Only in a few studies associations between housing and management factors and indicators
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relating to different aspects of dairy cattle welfare have been considered simultaneously (e.g. Burow et al., 2012;
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Husfeldt and Endres, 2012; Coignard et al., 2013). In the present study, we considered four indicators included
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in the Welfare Quality protocol for dairy cattle (2009) relating to three aspects of animal welfare: prevalence of
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lameness (relating to health), prevalence of lesions or swellings (health), prevalence of dirty hindquarters
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(cleanliness), and average frequency of displacements (behavior). A displacement is the act of an animal giving
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up its present position as a consequence of an agonistic interaction. These indicators were selected because of the
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data availability of potentially relevant explanatory housing and management factors for each individual
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indicator, and because they encompassed different aspects of animal welfare (e.g. health and behavior). This
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allowed us to examine the extent to which indicators relating to the same or different aspects of animal welfare
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were influenced by the same or different housing and management factors. The aim of this research was to
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identify and compare housing and management factors associated with prevalence of lameness, prevalence of
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lesions or swellings, prevalence of dirty hindquarters, and average frequency of displacements in dairy herds
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with free-stall housing.
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Materials and methods
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Herd selection
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In order to evaluate associations between housing and management factors and animal welfare indicators with
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some confidence, a wide range of the level of animal welfare is required. This cannot be achieved with random
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sampling of herds when prevalence of herds with poor welfare is low, because the necessary sample sizes would
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be too large to be covered by the costs of observations. Therefore, herds were selected, in order to obtain a
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sufficiently wide range of animal welfare. We used several national databases containing routine herd data
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relating to demography, milk production, and milk composition to calculate a composite health score (CHS)
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between 0 (worst) and 50 (best) for approximately 5,000 herds (approximately 30% of the national population)
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participating in a health program of a Dutch dairy cooperative. Data stored in these databases are routinely
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collected from Dutch dairy farms by the Dutch identification and registration system, the rendering plant, the
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milk quality assurance company, the animal health service, and the cattle improvement syndicate. The CHS, for
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which data was used from January 2008 through June 2009, consisted of five variables of routine herd data
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shown to be associated with animal welfare (De Vries et al., 2011): cow and young stock mortality, bulk tank
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milk somatic cell count, new udder infections, and fluctuations in standardized milk production. A herd was
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assigned zero points per variable when it was among the 10% worst values, and 10 points when it was among the
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90% best values of all herds in the databases in 2004. Subsequently, 500 herds were approached to participate in
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the study: 250 herds were randomly selected from the 5% lowest CHS (i.e. CHS ≤ 40) and 250 herds from the
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95% highest CHS (i.e. CHS > 40). From these 500 herds, 163 farmers responded positively, 75 negatively and
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262 failed to respond. Non-responders were contacted by phone. In total, 196 farmers agreed to participate: 90
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from the 5% lowest CHS, and 106 from the 95% highest CHS.
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Of the selected herds, 13 herds were housed in tie-stalls and two in straw yards. Because the number of herds for
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these two housing systems was too small for a reliable statistical analysis of risk factors involved here, herds in
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tie-stalls and straw yards were excluded from the analysis. Data of two herds in free-stall housing were also
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excluded, because the WQ protocol could not be executed correctly in these herds. In the remaining 179 herds,
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herd size ranged from 22 to 211 cows and average milk production was 25.9 ± 4.2 kg per cow/d.
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Data collection and processing
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Three herd health practitioners, one veterinarian, and three animal scientists, each with previous experience in
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dairy production and handling, were trained to use the Welfare Quality assessment protocol for dairy cattle
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(Welfare Quality, 2009). Herds were distributed among these observers based on proximity to their home
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address. Observers were not informed about the herds’ CHS. Each observer visited 14 to 48 herds once from
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November 2009 through March 2010 (winter), when cows had been denied access to pasture for at least 2 weeks.
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Observers collected data for lameness, lesions and swellings, dirty hindquarter, displacements, and housing- and
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management factors (Table 1). Data collection methods are described briefly below (details can be found in
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Welfare Quality (2009)).
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Lameness
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Lameness was assessed for a predefined number of lactating and dry cows (sample size depended on herd size,
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see Welfare Quality, 2009), walking in a straight line and on a hard, level surface, using a 5 points scoring
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system described by Winckler and Willen (2001). Cows were grouped into classes ‘not lame’ (scores 1 and 2),
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and ‘lame’ (score 3, 4 and 5). Data were expressed at the herd level, as percentages of assessed cows that were
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lame.
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Lesions and swellings
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For the same cows as assessed for lameness, lesions and swellings with a minimum diameter of 2 cm at the
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largest extent were counted on the left or the right (as a 50:50 ratio) lateral side of the whole body. These data
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were expressed at the herd level, as percentages of assessed cows with at least one lesion or swelling.
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Dirty hindquarter
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For the same cows as assessed for lameness, lesions and swellings, the presence of separate or continuous
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plaques of dirt amounting to at least the size of the palm of a hand was recorded for one hindquarter on a
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randomly chosen side of the body. These data were expressed at the herd level, as percentages of assessed cows
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with a dirty hindquarter.
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Displacements
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For the observations of displacements, the observer first divided the barn in a number of imaginary segments.
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The number of segments depended on herd size (Welfare Quality, 2009), with a maximum of about 25 lactating
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cows per segment. In each segment, occurrence of displacements was recorded using continuous behavior
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sampling (Martin and Bateson, 1993). A displacement was described as an interaction involving physical contact
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where the actor is butting, hitting, thrusting, striking, or pushing the receiver with a forceful movement, and the
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receiver gives up its present position with at least half a body length or width (Welfare Quality, 2009).
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Observations did not start earlier than one hour after morning feeding. Total observation time was 120 min, with
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a minimum of 10 min per segment. In case the number of segments was below six, segment observations were
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repeated in the second hour of observation. A displacement was recorded only when the actor’s head was inside
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the segment of observation. Animals present in the segment were counted at the start and the end of each
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segment observation, and observation time per segment was recorded. Data collected at the segment level was
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expressed as average frequency of displacements per cow per hour at the herd level as in Eq. (1).
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(1)
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where n is the number of segments, s is segment 1, ..., n , DPs is the number of displacements in segment s, OTs
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is observation time (h) in segment s, nstarts is the number of animals present at the start of the observation in
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segment s, and nends is the number of animals present at the end of the observation in segment s.
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Housing and management data
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Measures relating to herd characteristics, housing, feeding, milking, dry cow and young stock, and other
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management practices (Table 1) were collected using a checklist and an interview with the stockperson.
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Data analyses
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To explore associations between welfare indicators, Spearman rank correlations (rs) were calculated. They were
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preferred over Pearson correlations, because indicators could not be assumed to be normally distributed. Next,
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separate regression analyses were carried out for each welfare indicator, with the welfare indicator as the
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response variable, variables described in Table 1 as explanatory variables, and herd as experimental unit.
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Continuous explanatory variables (e.g. herd size) were converted into class variables. The two tertiles, i.e. the
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points that divide the ordered observations in three approximately equal groups, were taken as threshold values
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for the classes (Table 1). All calculations were performed with GenStat (VSN International Ltd., 2011).
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First, univariable analyses were performed with complete cases to evaluate the association between a response
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variable and each of the explanatory variables separately. Logistic and log linear regression analyses were
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performed for prevalence data (essentially proportions) and for frequency data (essentially counts), respectively,
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using quasi-likelihood estimation (McCullagh and Nelder, 1989), employing software for generalized linear
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models. A binomial distribution with a logit link function was specified for the prevalence of lameness, lesions
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or swellings, and dirty hindquarters, whereas a Poisson distribution with a log link function was specified for the
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average frequency of displacements. In both cases, a multiplicative overdispersion parameter was estimated from
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Pearson’s chi-square statistic divided by its degrees of freedom, and included in the variance function.
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Explanatory variables showing an association with the response variable with P-value < 0.20 of the approximate
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F-test (adapted from the quasi-likelihood ratio test) were included in subsequent analyses with multiple
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explanatory variables. Pearson’s chi-square test for independence was used to check for multicollinearity
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between two explanatory variables. Second, in the multivariable regression analyses, backward and forward
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stepwise selection of explanatory variables was used, with adjusted R2 as selection criterion. Explanatory
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variables that were selected by either of the two stepwise procedures were included in best subset selection,
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again with adjusted R2 as the selection criterion. Explanatory variables in the subset with the highest adjusted R2
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that were significantly (P < 0.05) associated with the response variable were retained in the final model. As a
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final check on possible confounding, each explanatory variable that was dropped from consideration was added
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to the final model in turn, to inspect its effect upon the contribution of the other selected variables. Variables that
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were (partially) confounded were not simultaneously included in the model. Only the variable that made most
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biological sense was retained. Two-way interactions among the explanatory variables that were retained in the
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final model were inspected. Standardized deviance residuals in the final model were visually inspected. Outliers
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were identified based on large standardized residuals. Outliers were checked for recording errors and the model
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was refitted without the outlier(s) to determine the impact upon conclusions. Effects of explanatory variables
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were shown as odds ratios and relative risks for logistic and log-linear analyses, respectively.
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For numerical reasons, both for lameness prevalence and frequency of displacements, the number of explanatory
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variables to be retained in the final models of the stepwise procedures proved to be too large for the best subset
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selection procedures. Therefore, the explanatory variables were put in a random order and split in two groups,
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which could then be analyzed separately in best subset selection. To reduce effects on selection, the splitting
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procedure was repeated fifteen times. Explanatory variables that were significantly associated with the response
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variable (P < 0.05) in the thirty models were combined in a final best subset selection, and the same approach as
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described above was followed for retaining significantly associated explanatory variables in the final model, and
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checking for possible confounding.
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Results and discussion
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The median within-herd prevalence observed was 32.3% lame cows (range 0-97.7%), 35.9% cows with lesions
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or swellings (range 0-97.6%), and 33.3% cows with dirty hindquarters (range 0-100%). The median number of
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displacements per cow per hour was 0.43 (range 0-1.85 displacements/cow per hour). Data were complete for
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prevalence of lameness, prevalence of dirty hindquarters and frequency of displacements. There was a missing
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value for prevalence of lesions or swellings in one herd. The correlation between prevalence of lameness and
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lesions or swellings was significant (rs = 0.37, P < 0.001). Prevalences varied considerably among herds (Figure
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1), which indicated room for improvement. Ranges found in the present study were similar to those found in
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other studies where welfare indicators were investigated (e.g. Von Keyserlingk et al., 2012). However, because
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herds in the present study were not randomly selected, the observed prevalence was not representative of the
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population of Dutch dairy farms as a whole.
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Herds in this study were selected on the basis of a CHS to achieve more variation in the level of animal welfare.
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In a recent literature review (De Vries et al., 2011), we showed that, so far, associations between the variables in
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this CHS and dairy cattle welfare indicators had been reported mainly at the level of the individual animal or in
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experimental settings. The present study showed that CHS is useful in selecting for variation in the level of
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welfare of dairy cows at herd level under commercial conditions as well; herds selected from the 5% lowest CHS
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tended to show more lame cows and more cows with dirty hindquarters than herds selected from the 95% highest
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CHS (P < 0.10; results presented in De Vries et al. (2013)). Yet there are a number of aspects of this selection
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procedure that may restrict the interpretation of the results. First, the choice of parameters in the CHS may have
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resulted in selecting a specific group of herds with poor welfare, and with specific farm characteristics in terms
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of housing and management. We expect, however, that the influence of the choice of parameters for the selection
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of dairy herds on farm characteristics (and ultimately on explanatory variables in our regression models) was
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limited, because the selected herds differed in many respects. Herd size, for example, ranged from 22 to 211
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cows, milk production ranged from 13.5 to 34.5 kg per cow/d, cows were pastured in three-fourth of the herds,
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and an automated milking system was present in one-fourth of the herds. Second, our selection procedure likely
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increased variation in welfare among herds, which may have inflated the association between management and
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housing factors and welfare indicators obtained in the present study. The evaluation of the multivariable
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regression models, however, can be expected to be markedly more accurate, and hence more efficient, for
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selected herds than for random herds. This was the decisive argument for selection of herds in the present study.
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Data quality of welfare indicators may have influenced performance of prediction models. We did not evaluate
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reliability (i.e., the extent to which the same results are obtained among and within observers (Knierim &
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Winckler 2009)) of the four welfare indicators in this study, because the objective of Welfare Quality was to
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develop a protocol built on evidence-based indicators. This does not necessarily imply, however, that reliability
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of these indicators was high. Therefore, additional studies are required to further substantiate the associations
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between welfare indicators and risk factors identified in the present study
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Factors associated with lameness
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Twenty-six explanatory variables were to some extent (P < 0.20) associated with prevalence of lameness in the
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univariable regression (Appendix). In the multivariable regression, average stall width was dropped in favor of
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predominant surface of the lying area, since these were confounded. Two outliers were identified, but removal of
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these outliers did not markedly affect the results. Odds ratios and associated confidence intervals of the
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explanatory variables retained in the final model are shown in Table 2. Prevalence of lameness was negatively
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associated with the use of soft mats or mattresses, or deep bedding compared to concrete as the predominant
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surface of the lying area, pasturing, a closed herd status, and separating dry cows into a far-off and a close-up
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group.
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The negative association between prevalence of lameness and the use of soft mats or mattresses, or deep bedding
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in stalls and pasturing was consistent with other studies (e.g. Haskell et al., 2006; Hernandez-Mendo et al., 2007;
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Dippel et al., 2009; Burow et al., 2012; Husfeldt and Endres, 2012; Chapinal et al., 2013). Studies have reported
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a higher prevalence of lame cows in herds with mattresses compared to deep bedding (e.g. Cook et al., 2004; Ito
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et al., 2010). Such a difference was not evaluated in our study because stall surfaces were compared to concrete
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only. Similar to the positive association between the prevalence of lameness and an open biosecurity status of
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herds in our study, Frankena et al. (1991) and Holzhauer et al. (2008) showed a higher risk of lameness and sole
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ulcers for farms purchasing heifers. A possible explanation might be that a closed herd prevents introduction of
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lameness-related infectious agents. To our knowledge, no other studies have found associations between
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prevalence of lameness and separation of dry cows in far-off and close-up groups. The negative association
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between lameness and dry cow groups might indicate a beneficial effect of strategic feeding in these groups. Diet
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composition around calving, for example, is thought to affect the occurrence of laminitis via lactic acidosis
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(Nocek, 1997; Donovan et al., 2004). Another explanation for this negative association might be that dry cow
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groups are more often kept in straw yards instead of free-stalls. A lower occurrence of hoof problems has been
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found in straw yards compared to free-stalls (Webster, 2002; Somers et al., 2003). On the other hand, Barker et
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al. (2007) found that keeping dry cows in straw yards was associated with increased lameness. Barker et al.
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(2007) hypothesized that keeping cows temporarily in straw yards can thin the sole horn, which may lead to sole
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ulcers when cows are kept on hard floors after calving. Contrary to other studies, we did not find an association
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between the prevalence of lameness and other housing and management factors, e.g. other aspects of stall design
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(e.g. Bernardi et al., 2009; Rouha-Mulleder et al., 2009), alley flooring (Barker et al., 2010; Fjeldaas et al.,
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2011), space allowance (Barker et al., 2007), or claw trimming routines (Barker et al., 2007). Possibly, a lack of
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association was due to the type of measures considered in our study (e.g. height of the neck rail instead of
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distance to the rear curb).
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Factors associated with lesions or swellings
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Twenty explanatory variables were to some extent (P < 0.20) associated with the prevalence of lesions or
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swellings in the univariable regression (Appendix). In the multivariable regression, frequency of footbaths was
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positively associated with the prevalence of lesions or swellings. The strength of this association changed when
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prevalence of lameness was introduced to the model. Because the use of footbaths was probably practiced
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because of poor claw health rather than being a cause of lesions and swellings, it was dropped from the model.
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One outlier was identified, but removal of this outlier did not markedly affect the results. Odds ratios and
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associated confidence intervals of the explanatory variables retained in the final model are shown in Table 3.
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Prevalence of lesions or swellings was negatively associated with the use of soft mats or mattresses, or deep
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bedding compared to concrete as the predominant surface of the lying area, pasturing, light, and cows being at
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least 29 days in milk (DIM) compared to 22-28 DIM when the maximum amount of concentrates is fed. In
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particular, the combination of zero grazing and little light intensity was positively associated with prevalence of
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lesions or swellings.
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The negative association between the prevalence of lesions or swellings and the use of soft mats or mattresses, or
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deep bedding in stalls and pasturing was consistent with results of other studies (e.g. Weary and Taszkun, 2000;
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Haskell et al., 2006; Fulwider et al., 2007; Lombard et al., 2010; Husfeldt and Endres, 2012; Brenninkmeyer et
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al., 2013; Burow et al., 2013). To our knowledge, there are no other studies that have found associations between
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prevalence of lesions or swellings and light intensity in the barn, or DIM when the maximum amount of
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concentrates is fed. Lesions and swellings were possibly higher with lower light intensity due cows colliding
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more often with housing equipment as a result of reduced sight, or from cows spending more time resting, as
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was shown in calves offered lower light intensities (Dannenmann et al., 1985). Alternatively, we hypothesize
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that a higher light intensity reflects a number of superior underlying or associated housing and management
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practices, because herds with a light barn more often had, e.g., higher feeding racks, wider alleys, and longer,
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cleaner stalls with a higher neck rail and no head lunge impediments (P < 0.01). This could also explain the
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interaction between pasturing and light intensity; effects of superior housing and management practices become
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more important when cows are indoors year-round. To our knowledge, there are no other studies that have
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shown an association between prevalence of lesions or swellings and the rate of increase in the amount of
312
concentrates fed in the first weeks after calving. Prevalence of lesions or swellings was lower in herds where
313
cows were at least 29 DIM when the maximum amount was fed, compared to herds where cows were 20-28
314
DIM. Possibly, a more gradual increase in the amount of concentrates improves rumen health and lowers the risk
315
of laminitis. Improved leg health, in turn, could contribute to fewer lesions or swellings. This might partially
316
explain the effect of the rate of increasing concentrates on lesions and swellings, as prevalence of lesions or
317
swellings and prevalence of lameness were associated. Odds ratios for the association between concentrate
318
feeding and lesions or swellings dropped about 10% when lameness prevalence was introduced in the model. We
319
did not find associations between lesions or swellings and other housing and management factors, contrary to
320
other studies that found associations with, e.g., aspects of stall design (e.g. Brenninkmeyer et al., 2013), feed
321
space (Rutherford et al., 2008), or breed (Burow et al., 2013). Other studies, however, mostly investigated
322
lesions and swellings on the hock, whereas we considered lesions and swellings on the whole body.
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Factors associated with dirty hindquarters
325
Fourteen explanatory variables were to some extent (P < 0.20) associated with the prevalence of dirty
326
hindquarters in the univariable regression (Appendix). The multivariable regression showed that temporal fixing
327
of cows after milking was positively associated with the prevalence of dirty hindquarters, but temporal fixing of
328
cows was also collinear with the use of deep bedding in stalls (χ2 = 13.3, P = 0.004). Because temporal fixing of
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Page 12 of 30
cows was probably practiced for reasons of udder health rather than a cause of dirty hindquarters, it was dropped
330
from the model. Odds ratios and associated confidence intervals of the explanatory variables retained in the final
331
model are shown in Table 4. Prevalence of dirty hindquarters was negatively associated with deep bedding
332
compared to hard mats as the predominant surface of the lying area, less than 50% stalls with fecal
333
contamination, fewer stalls with head lunge impediments (e.g. a wall or bars), and feeding different types of
334
roughage.
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335
To our knowledge, few other studies have investigated factors associated with cleanliness of the hindquarter, but
337
similar associations have been found between surface and cleanliness of the lying area and udder cleanliness
338
(e.g. Fregonesi et al., 2009; Plesch and Knierim, 2012). The positive association between the prevalence of dirty
339
hindquarters and head lunge impediments seems difficult to explain because more restricted stalls have often
340
been associated with cleaner cows (e.g. Fregonesi et al., 2009; Plesch and Knierim, 2012). However, a similar
341
association was found in a study by Ruud et al. (2010). Their results also showed that the presence of a lower
342
head rail increases the amount of faeces fallen on the stall base (Ruud et al., 2011). The association between
343
dirty hindquarters and feeding one type of roughage only was due to manure plaques found on both sides of the
344
tail, probably caused by diarrhea. Hence, feeding a single type of roughage is likely accompanied by digestive
345
problems and more liquid manure, causing an increased risk of dirty hindquarters (Ruud et al., 2010). Manure
346
plaques on both sides of the tail were most observed in herds that fed one type of roughage, compared to herds
347
feeding different types of roughage mixed and separately (5.6%, 1.6% and 0%; P < 0.001). Contrary to other
348
studies, we did not find associations between dirty hindquarters and other housing and management factors, e.g.
349
neck rail height or stall bed length (e.g. Bernardi et al., 2009; Fregonesi et al., 2009; Plesch and Knierim, 2012).
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Factors associated with frequency of displacements
352
Twenty-three explanatory variables were to some extent (P < 0.20) associated with the average frequency of
353
displacements in the univariable regression (Appendix). In the multivariable regression, routine herd claw
354
trimming was negatively associated with the frequency of displacements, but routine herd claw trimming was
355
also collinear with floor scraping frequency (χ2 = 7.9, P = 0.017) and the use of cow brushes (χ2 = 15.4, P
79 cows compared to < 61 cows, and a proportion cows to stalls
362
between 0.91 and 1.04 compared to a proportion of cows to stalls of > 1.04.
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Three of the six factors associated with the frequency of displacements were likely to be related to competition
365
around resources with limited access, such as feed, cow brushes, and stalls. Average frequency of displacements
366
was lower in herds that introduced heifers in the lactating group before calving, compared to introduction after
367
calving. Introduction of new animals in a group is known to increase displacements due to re-establishment of
368
social relationships (Kondo and Hurnik, 1990; Bøe and Færevik, 2003), and can lead to a decrease in dry matter
369
intake of regrouped cows by 10% (Schirmann et al., 2011). Fewer displacements might have been observed due
370
to pregnant heifers being less motivated to compete for feed, because they require less energy prepartum
371
compared to postpartum. Besides this, frequency of displacements increased with continuous availability of feed
372
at the feed bunk. This could be explained by the fact that feed availability attracts cows to the feed bunk and
373
displacements occur more often at the feed bunk than in other alleys and stalls (Miller and Wood-Gush, 1991).
374
Moreover, the number of displacements has been shown to increase over 3.5 times when feeding non-uniform
375
feed (Huzzey et al., 2013). A higher frequency of displacements, therefore, might be explained by a larger
376
variation in quality of the feed after the feed was selected by cows during morning feeding. The frequency of
377
displacements was lower among herds with no cow brushes, which might indicate that cows are motivated for
378
using brushes (DeVries et al., 2007). Possibly, the ratio brushes to cows was too small. Similar to the results of
379
Fregonesi and Leaver (2002), frequency of displacements was lower in herds with 0.9 to 1.04 cows per stall
380
compared to herds with more than 1.04 cows per stall. This can be due competition for stalls (Fregonesi et al.,
381
2007) or to cows spending more time in alleys instead of stalls (Wierenga and Hopster, 1990), which increases
382
the chance of encountering a conspecific. A frequency of 3-5 floor scraping events per day was associated with
383
fewer displacements, compared with < 3 floor scraping events. This was contrary to our expectation because a
384
higher floor scraping frequency usually results in dryer concrete floors, which enable cows to show a higher
385
walking speed, less slipping, and longer strides compared to cows walking on slurry-covered concrete (Phillips
386
and Morris, 2000; Rushen and de Passille, 2006). Therefore, with a higher floor scraping frequency, it was
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Page 14 of 30
expected that cows feel more secure to start agonistic interactions, such as displacements. Possibly, this effect is
388
only found when the floor scraping frequency is > 5 (Table 5). Contrary to Telezhenko et al. (2012), we found an
389
association between herd size and displacements. The negative association between herd size and displacements
390
might imply that a cow can use relatively more space in a larger herd than in a smaller herd (given an equal
391
amount of space per animal), because more space is shared (described for broilers in Bokkers et al (2011)). This
392
relative additional space in large herds might be used by cows to avoid conflicts with conspecifics. Contrary to
393
other studies, we did not find an association between frequency of displacements and other factors, e.g. feed
394
space per cow (DeVries et al., 2004; Huzzey et al., 2006). Possibly, this was due to that fact that occurrence of
395
displacements were recorded at a specific time of the day in our study (i.e. at least one hour after feeding).
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Factors associated with multiple welfare indicators
398
Housing and management factors identified in our study were partly the same for prevalences of lameness,
399
lesions or swellings, and dirty hindquarters. The two welfare indicators that were most correlated - prevalence of
400
lameness and lesions or swellings – had two explanatory factors in common. Results of this study suggest that
401
changing the surface of the lying area and pasturing can help decrease the occurrence of welfare problems
402
underlying multiple welfare indicators. However, associations of these factors with other indicators of dairy
403
cattle welfare, e.g. prevalence of mastitis, should be investigated.
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Housing and management factors did not show conflicting effects for different welfare indicators. Conflicts were
406
expected due to associations found in other studies. For example, introducing heifers to the lactating group
407
before calving was associated with a lower frequency of displacement in our study, but has been associated with
408
increased lameness in a study by Barker et al. (2007).
409 410
No common housing and management factors were found for frequency of displacements and prevalence of
411
lameness, lesions or swellings, and dirty hindquarters. This might be partly due to absence of a biological
412
relation between the average frequency of displacements and other indicators, which was supported by our
413
finding that they were not correlated. Nevertheless, significant associations between being displaced and
414
increased lameness have been found at the animal level (e.g. Galindo et al., 2000), and it has been suggested that
415
these low-ranking cows spent more time walking and standing. Results of our study suggested that lameness,
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Page 15 of 30
416
lesions or swellings, and dirty hindquarters were primarily influenced by the quality (e.g. softness, space, and
417
cleanliness) of lying and walking surfaces, whereas frequency of displacements was mainly influenced by
418
competition around limited resources.
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Conclusions
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Fifteen housing and management factors were significantly associated with four indicators of dairy cattle
423
welfare. Two of these factors, surface of the lying area and access to pasture, were associated with prevalences
424
of lameness, lesions or swellings, and dirty hindquarters. No common housing and management factors were
425
identified for frequency of displacements and prevalence of lameness, lesions or swellings, and dirty
426
hindquarters. Lameness, lesions or swellings, and dirty hindquarters were primarily associated with factors
427
relating to the quality of lying and walking surfaces, whereas frequency of displacements was mainly associated
428
with factors relating to limited resources.
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Acknowledgements
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This research was funded by the Animal Health Service Deventer. The authors gratefully acknowledge farmers
433
for participating in this study, observers for their commitment to collecting the welfare data, and Willem Buist
434
(Biometris, Wageningen University, the Netherlands) for his help with the data analyses.
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Figure 1. Box-and-whisker plots of prevalence of lameness, lesions or swellings, dirty hindquarter, and frequency of displacements among the selected herds. Boxes cover the medial 50% of the data with the median
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dividing the box. Ends of whiskers represent minimum and maximum values.
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Table 1. Herd-level housing and management factors and observed number of herdsa per factor level
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cr
ip t
Factor Level (number of herds) General herd characteristics Herd size (n lactating cows) < 61 (62) 61 – 79 (58) > 79 (59) Breed (in at least 10% of the cows) Holstein-Fr. (157) Other (22) Housing Air inlet side walls Yes (150) No (29) Air inlet roof top Yes (137) No (42) Light intensityb Light (108) Dark (68) Cow brushes No brushes (46) Fixed (51) Rotating (80) Average width of alleys (cm) < 222 (79) 222 - 250 (52) > 250 (39) Average width of passages (cm) < 185 (57) 185 - 223 (57) > 223 (56) Alleys with dead ends No (79) Yes (100) Type of flooring system Slatted (169) Solid (8) Slippery floorc No (165) Yes (14) Floor scraping frequency (times/day) < 3 (91) 3 - 5 (28) > 5 (60) Rims or pits in the floor No (134) Yes (45) Stalls Proportion cows to stalls < 0.91 (60) 0.91 - 1.04 (57) > 1.04 (58) Predominant surface of lying area Concrete (32) Hard mat (39) Soft mat/mattress (70) Deep bedding (33) Stall divisions Cantilever (85) Mushroom (57) Other (37) Average stall width (cm) < 110.2 (71) 110.2 – 111.5 (50) > 111.5 (57) Average stall length (cm) < 220.5 (64) 220.5 – 228.7 (54) > 228.7 (60) Average height of stall neck rail (cm) < 109.2 (62) 109.2 - 114.5 (59) > 114.5 (58) Head lunge impediments All stalls (28) Some stalls (127) No stalls (24) Bedding height (cm) < 0.56 (52) 0.56 - 1.75 (54) > 1.75 (60) Stalls with fecal contaminationd (%) < 50 (76) ≥ 50 (103) Cleaning frequency (times/day) ≤ 2 (110) > 2 (69) Littering frequency (times/day) < 2 (78) ≥ 2 (101) Feeding Average feed space per cow (cm) < 56.0 (57) 56.0 - 67.7 (57) > 67.7 (58) Average feeding rack height (cm) < 138 (58) 138 - 146 (57) > 146 (59) Roughage fed at fixed times of the day No (48) Yes (131) Different types of roughage No (29) Yes, fed mixed (93) Yes, fed separately (57) Continuous availabilitye of roughage No (27) Yes (152) Roughage contaminated with manure and/or moulds, or No (154) Yes (25) heat coming out Concentrate dispensers in the stable No (47) Yes (132) Max. amount of concentrates (kg DM/cow/day) < 9.5 (86) 9.5 – 10.0 (41) > 10.0 (52) DIM when max. amount of concentrates is fed < 22 (93) 22 - 28 (25) > 28 (52) Group drinkers No (22) Yes (156) Sufficient number and/or lengthf of drinkers Yes (83) Partly (65) No (31) Milking practices Automatic milking No (137) Yes (42) Lactation groups No (164) Yes (15) Maximum waiting time for milking (min) < 45 (61) 45 - 75 (69) > 75 (49) Temporary fixing of cows in feeding rack after milking No (143) Yes (36) Dry cows and young stock Dry cow groups (far-off and close-up) No (104) Yes (75) Length of transition period (weeks) ≤ 4 (51) > 4 (126) Predominant place of calving Calving pen/pasture (145) Other (32) Heifer housing Same building (96) Other building (50) Both (21) Time of introducing heifers in lactating group Before calving (87) After calving (92) Way of introducing heifers in lactating group Individually (153) In groups (26) Other management practices Routine herd claw trimming Yes (132) No (47) Indiv. cow claw trimming between herd trimming events Yes (146) No (33) Who trims claws Professional (35) Farmer/employee (47) Both (97) Frequency of footbaths (times per month) Never (53) ≤ 1 (58) > 1 (68) Access to pasture Zero-grazing (41) Summer pasturing (138) Winter OLAg for dry cows and/or young stock No (163) Yes (16) Cows in heat are fixed or separated No (114) Yes (59) Herd biosecurity status Open (83) Closed (98) a The distribution among levels is not representative for the Dutch dairy population because herds were not selected randomly b ‘Light’ (versus ‘dark’) was described as the observer being able (versus not being able) to read a newspaper in a cubicle around midday c ‘Slippery’ was described as the observer experiencing slipping and having little grip during turning d ‘Fecal contamination’ of a stall was described as cow droppings or >20% manure cover in the rear 1/3 part of the lying area e ‘Continuous availability’ was described as at least 180 L (1 wheelbarrow) roughage per 25 cows anytime during the farm visit
23
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f
‘Sufficient’ refers to at least 1 water bowl for 10 cows and/or 6 cm of through per cow; ‘partly sufficient’ refers to at least 1 water bowl for 15 cows and/or 4 cm of through per cow; ‘not sufficient’ refers to otherwise (adapted from Welfare Quality, 2009) Outdoor loafing area
g
Table 2. P-valuesa of effects of selected factors for prevalence of lameness (adjusted R2 = 12.7%), and odds
1) P-value
95% CI of odds ratio
P-value pairwise comparison
1 0.76 0.66 0.48
0.54-1.09 0.48-0.91 0.32-0.71
0.14 0.01 0.00
1 0.68
0.51-0.90
0.01
1 0.76
0.60-0.97
0.03
1 0.74
0.57-0.96
0.02
Ac ce p
te
d
M
an
Predominant surface of lying area Concrete 42.8 0.00 Hard mat 36.5 Soft mat/mattress 33.4 Deep bedding 26.6 Access to pasture Zero grazing 39.1 0.01 Summer pasturing 30.5 Herd biosecurity status Open 37.8 0.03 Closed 31.8 Dry cow groups No 38.1 0.02 Yes 31.5 a Based on an approximate F-test (adapted from the quasi-likelihood ratio test)
Odds ratio
cr
Estimated prevalence (%)
us
Factor and level
ip t
ratios with associated P-values for pairwise comparison of factor levels with a reference level (i.e. odds ratio =
24
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Table 3. P-valuesa of effects of selected factors for prevalence of lesions or swellings (adjusted R2 = 18.0%), and odds ratios with associated P-values for pairwise comparison of factor levels with a reference level (i.e. odds
58.4 59.8 46.0 41.8
0.00
1 1.07 0.58 0.48
0.70-1.63 0.39-0.85 0.30-0.77
0.77 0.01 0.00
61.6 41.3
0.00 0.00
1 0.41
0.27-0.61
0.00
1 0.50
0.34-0.75
0.00
0.71 1 0.52
0.46-1.08 0.32-0.83
0.11 0.01
1 0.34 0.27 0.21
0.16-0.69 0.14-0.55 0.10-0.40
0.00 0.00 0.00
an
59.2 43.8
cr
P-value pairwise comparison
0.01 51.2 59.0 44.3
0.04
73.6 49.6 44.7 38.0
Based on an approximate F-test (adapted from the quasi-likelihood ratio test) ‘Light’ (versus ‘dark’) was described as the observer being able (versus not being able) to read a newspaper in a cubicle around midday
te
b
95% CI of odds ratio
Ac ce p
a
Odds ratio
M
Predominant surface of lying area Concrete Hard mat Soft mat/mattress Deep bedding Access to pasture Zero grazing Summer pasturing Light intensityb Dark Light DIM when maximum amount of concentrates is fed < 22 22 – 28 > 28 Interaction pasturing and light intensity Zero grazing and dark Zero grazing and light Pasturing and dark Pasturing and light
P-value
us
Estimated prevalence (%)
d
Factor and level
ip t
ratio = 1)
25
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Table 4. P-valuesa of effects of selected factors for prevalence of dirty hindquarters (adjusted R2 = 20.6%), and odds ratios with associated P-values for pairwise comparison of factor levels with a reference level (i.e. odds
Factor and level
Estimated prevalence (%)
P-value
Odds ratio
ip t
ratio = 1) 95% CI of odds ratio
P-value pairwise comparison 0.07 0.50 0.01
0.00 0.00 0.00 0.01 0.00
Ac ce p
te
d
M
an
us
cr
Predominant surface of lying area Concrete 41.0 0.03 0.64 0.39-1.03 Hard mat 51.2 1 Soft mat/mattress 47.8 0.86 0.55-1.33 Deep bedding 35.9 0.50 0.29-0.86 Stalls with fecal contaminationb ≥ 50% 50.2 0.00 1 < 50% 37.8 0.57 0.41-0.80 Head lunge impediments All stalls 59.8 0.00 1 Some stalls 39.1 0.41 0.26-0.65 No stalls 33.0 0.31 0.17-0.57 Different type of roughage No 54.4 0.01 1 Yes, fed mixed 39.6 0.52 0.33-0.82 Yes, fed separately 37.9 0.48 0.29-0.78 a Based on an approximate F-test (adapted from the quasi-likelihood ratio test) b ‘Fecal contamination’ of a stall was described as cow droppings or >20% manure cover in the rear 1/3 part of the lying area
26
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Table 5. P-valuesa of effects of selected factors for average frequency of displacements (DP) per cow per hour (adjusted R2 = 19.8%), and relative risks with associated P-values for pairwise comparison of factor levels with a
Factor and level
95% CI of relative risk
Estimated frequency (DP/cow/hour)
ip t
reference level (i.e. relative risk = 1)
Ac ce p
te
d
M
an
us
cr
P-value pairwise comparison P-value Relative risk Time of introducing heifers in lactating group Before calving 0.29 0.02 0.76 0.61-0.95 0.02 After calving 0.38 1 Cow brushes No brushes 0.26 0.01 0.63 0.47-0.85 0.00 Fixed 0.34 0.84 0.64-1.09 0.19 Rotating 0.40 1 Continuous availabilityb of roughage No 0.25 0.00 0.62 0.43-0.88 0.01 Yes 0.41 1 Floor scraping frequency (times/day) 5 0.37 0.90 0.70-1.16 0.42 Herd size < 61 0.37 0.00 1 61 – 79 0.39 1.07 0.83-1.38 0.62 > 79 0.23 0.62 0.46-0.84 0.00 Proportion cows to stalls < 0.91 0.34 0.01 0.87 0.67-1.14 0.32 0.91 – 1.04 0.26 0.65 0.49-0.87 0.00 > 1.04 0.39 1 a Based on an approximate F-test (adapted from the quasi-likelihood ratio test) b ‘Continuous availability’ was described as at least 180 L (1 wheelbarrow) roughage per 25 cows anytime during the farm visit
27
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Appendix. Resultsa of one-way analyses of single potential risk factors for the prevalence of lameness, lesions or swellings, cow with dirty hindquarter, and frequency of displacements % cows with dirty flank *
** ***
*** * ** * *** **
****
*
**** * *** **
M
**** ** *** * ****
an
****
***
*
d
** *
*** * ***
* ** *** **** *** ****
** ***
***
*** * *
us
****
Freq. of displacements
cr
*
te
Ac ce p
% cows with lesions/swellings
ip t
% lame cows Potential risk factor General herd characteristics Herd size Breed Housing Air inlet side walls Air inlet roof top Light intensity Brushes Average width of alleys Average width of passages Alleys with dead ends Type of flooring system Slippery floor Floor scraping frequency Rims or pit in the floor Stalls Proportion cows to stalls Predominant surface of lying area Stall divisions Average stall width Average stall length Average height of stall neck rail Head lunge impediments Bedding height Stalls with fecal contamination Cleaning frequency Littering frequency Feeding Average feed space per cow Average feeding rack height Roughage fed at fixed times of the day Different types of roughage Continuous availability of roughage Roughage contaminated with manure and/or moulds, or heat coming out Concentrate dispensers in the stable Maximum amount of concentrates DIM when max. amount of concentrates is fed Group drinkers Sufficient number and/or length of drinkers Milking practices Automatic milking Lactation groups Maximum waiting time for milking Temporary fixing of cows after milking Dry cows and young stock Dry cow groups (far-off and close-up) Length of transition period Predominant place of calving Heifer housing Time of introducing heifers in lactating group Way of introducing heifers in lactating group Other management practices Routine herd claw trimming Individual cow claw trimming between herd trimming events Who trims claws Frequency of footbaths Pasturing Outdoor loafing area for dry cows and/or young stock Cows in heat are fixed or separated Herd biosecurity status
* * **
* **
** * ****
* * **
**
*
****
*** **** ** *
*** **
*
**
***
*** ** ** *** *
*
*** *** *
* **** ****
*** *
* ***
*
***
28
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ip t cr us an M d te Ac ce p
564
a P-value based on an approximate F-test (adapted from the quasi-likelihood ratio test). Significance of association indicated by * (0.10 < P < 0.20) , ** (0.05 < P < 0.10), *** (0.01 < P < 0.05), **** (P < 0.01)
29
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564
Housing and management factors associated with indicators of dairy cattle welfare
565
De Vries et al.
566
Highlights
568
•
Data on animal welfare, housing and management was collected on 179 Dutch dairy farms
569
•
Soft mats or mattresses and deep bedding in stalls were common protective factors for lameness, lesions or swellings and dirty hindquarters.
571
•
Summer pasturing was a common protective factor for lameness and lesions or swellings.
572
•
There was no common protective factor for frequency of displacements and other welfare indicators.
cr
us
570
ip t
567
Ac ce p
te
d
M
an
573
30
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