The association of hoof lesions at claw trimming with test-day milk yield in Danish Holsteins

Preventive Veterinary Medicine 79 (2007) 224–243 www.elsevier.com/locate/prevetmed

The association of hoof lesions at claw trimming with test-day milk yield in Danish Holsteins Jehan Frans Ettema a,*, Nynne Capion b, Ashley E. Hill c a

Danish Institute of Agricultural Sciences, Department of Herd Health and Production Management, P.O. Box 50, DK-8830 Tjele, Denmark b Department of Clinical Studies, Large Animal Surgery, Royal Veterinary and Agricultural University, Dyrlægevej 48, DK-1870 Frederiksberg, Copenhagen, Denmark c Animal Population Health Institute, College of Veterinary Medicine and Biomedical Sciences, Colorado State University, Fort Collins, CO 80523-1678, USA Received 25 April 2006; received in revised form 20 December 2006; accepted 21 December 2006

Abstract In a cross-sectional study, performed between October 2002 and April 2003 on 55 Danish dairy herds with 6161 predominantly Holstein Friesian cows the prevalence of 9 hoof lesions was determined. All test-day yields (TDY) of kg energy corrected milk (ECM) in the lactation of diagnosis were recorded. For the purpose of including hoof lesions in a decision support model an attempt was made to aggregate the lesions into digital dermatitis (DD), other interdigital diseases (OID, infectious diseases other than DD) and hoof horn diseases (HHD, related to metabolic disorders and trauma). A division was made based on the stage of lactation in which the lesions were diagnosed; during the first 100 days in milk, between days 101 and 200 and between days 201 and 305. Associations between the presence of hoof lesions at trimming and milk production were analyzed by linear mixed modeling at the cow level, clustered within herd. The data of primiparous cows was analyzed separately from the multiparous cows. Based on the associations between TDY and the individual lesions aggregated into HHD, this aggregation as initially planned could not be justified and was therefore not maintained. For OID the value of early diagnosis was apparent; an early diagnosis and early treatment (<101 DIM) was

* Corresponding author. Tel.: +45 8999 1371; fax: +45 8999 1500. E-mail address: [email protected] (J.F. Ettema). 0167-5877/$ – see front matter # 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.prevetmed.2006.12.007

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associated with either a positive value or a value less negative compared to a diagnosis and treatment in late lactation (201–305 DIM). This pattern was not as clearly present for the other lesions. # 2007 Elsevier B.V. All rights reserved. Keywords: Dairy cattle; Hoof lesions; Associations; Milk yield

1. Introduction Claw lesions in dairy cattle are commonly observed in high producing dairy cows worldwide (Alban, 1995; Clarkson et al., 1996; Manske et al., 2002a; Melendez et al., 2003; Somers et al., 2003). The relation of hoof lesions with milk production is a difficult one to study because a high milk yield level is known to be a risk factor for hoof lesions and at the same time hoof lesions are known to reduce the cow’s milk production. Green et al. (2002) found a milk loss between 160 and 550 kg per lactation for cows with a form of clinical lameness. Warnick et al. (2001) reported a milk loss between 104 and 295 kg per lactation for cows that became lame at 100 days in milk (DIM). Green et al. (2002) also qualified milk production level as a risk factor for lameness in their study; on days that these cows were not lame, they produced a mean increased milk yield of 1.12 kg compared to cows that were never lame. A comparable result was found in a cross-sectional study by Hultgren et al. (2004) who studied the association between the occurrence of sole ulcers and the total milk yield per lactation. The energy corrected milk (ECM) yield of cows with a sole ulcer was on average 479 kg higher. Milk yield is therefore not only important as an effect of hoof lesions but also as a risk factor. The overall purpose of the field study performed during the housing season of 2002 and 2003 was to improve claw health in Danish dairy herds. The objectives of this analysis were to estimate the association of the hoof lesions detected and treated at different stages of lactation with energy corrected milk produced on test days by Danish Holsteins in modern dairy management systems. A secondary objective was to identify hoof lesions for which early detection and treatment was associated with different outcomes compared to later detection and treatment. 2. Materials and methods 2.1. Selection of herds Of all professional claw trimmers that were asked to join the study, only four agreed. The claw trimmers included all client herds that met eligibility criteria: predominantly Holstein Friesian (HF) cows housed in free-stalls with concrete floors and cubicles. Only herds where all cows were routinely trimmed during the visit were included in the study. The few cows in these herds that were not trimmed were either recently dried-off or too close to calving. Visits that included the trimming of a few cows with more acute lameness were not included in the data. Fifty five Danish dairy herds were clients of the participating hoof trimmers and met eligibility criteria. These herds were visited once during the housing

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season from October 2002 to April 2003; all cows trimmed were inside at the time of trimming in order to minimize variation caused by season. Herds with a herd size smaller than 25 cows were excluded (n = 1). The mean herd size of the remaining herds was 114 (S.D. = 63). The median number of cows per herd was 100 and ranged from 48 to 436. 2.2. Trimming and recording of lesions In total 6161 cows were trimmed and all skin and horn lesions related to the distal part of all four limbs were recorded. This included heel horn erosion (HHE), sole haemorrhage (SH), sole ulcer (SU), interdigital dermatitis (ID), digital dermatitis (DD, Mortellaro’s disease), interdigital hyperplasia (IH), white line abscess (WLA), white line disease (WLD) and double sole (DS). Lesions and abnormalities were evaluated during and at the completion of trimming; records of both new and older lesions were recorded. The methodology used by the second author to standardize lesion diagnosis by the participating trimmers was a 50-page slide show and scoring of a 60-cow herd together. HHE, SH, and WLD were scored on a scale from 0 to 2; 0 represents absence of the lesion, 1 presence of a mild form of the lesion on one or more legs and 2 the presence of a severe form of the lesion. DD, ID, IH, DS, WLA and SU were not scored by severity, because it was difficult to get agreement between the trimmers. For these lesions 0 represents absence of a lesion, 1 the presence of the lesion on one leg and 2 the presence on more legs. Multiple different lesion types on the same cow were registered when they were present. Besides identification, all lesions got the usual treatment; curative trimming, shoe, bandage, cleaning and/or dressing with disinfecting products depending on the type of lesion. According to a decision support model in which lameness is modeled as the cause of three aggregations of diseases (Ettema and Østergaard, 2006) the lesions were aggregated by etiology. The lesions WLD, WLA, SH, SU and DS were aggregated as hoof horn diseases (HHD). These lesions are all associated with disturbed horn growth and are believed to be related to nutritional disorders, calving or trauma (Toussaint Raven et al., 1985; Greenough and Vermunt, 1991). Several of these lesions are reportedly correlated: SH and WLD increase susceptibility for SU and WLA, respectively (Collick, 1997). The remaining lesions IH, HHE, ID, and DD have an infectious origin. DD was maintained as a separate outcome and the lesions IH, HHE, and ID were aggregated as other infectious diseases (OID). The OID and DD lesions are associated with poor hygienic conditions and flooring system (Somers et al., 2003). Etiology and risk factors are comparable for the OID and DD diseases, except that DD is found more often in primiparous cows (Blowey and Sharp, 1988; Holzhauer et al., 2003; Somers et al., 2005a,b). This is possibly due to development of immunity in older cows (Blowey and Sharp, 1988) or because the more susceptible cows are culled; Argaez-Rodriguez et al. (1997) found a re-infection rate of 68% in the following lactation. The aggregations are justified by the results reported in literature on correlations of disease occurrence at both cow and herd level (Manske et al., 2002a; Holzhauer et al., 2003). For the aggregation concerning the lesions HHE and SH that were scored by severity, we transformed these scorings into dichotomous variables with no- and mild lesions in the one category and severe lesions in the other category. Mild lesions were considered as first indications of disturbed hoof health but no painful disorders

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on their own. Interdigital phlegmon (IP), an acutely painful infectious lesion that is likely to be treated at onset, rather than detected by a hoof trimmer, was also included in the category OID when it occurred in the same lactation stage as periodic trimming. When IP was identified and treated in a different stage of lactation than the periodic trimming, the cow was deleted from the dataset. 2.3. Lactation stage at detection Hoof lesions, both aggregated and separate, were categorized by lactation stage at detection to allow comparison of outcomes between cows with lesions identified and treated early in lactation and those identified and treated later. In this cross-sectional study, lesions (other than IP) were diagnosed and treated at trimming; the time of lesion onset is not known. Each hoof lesion variable was categorized as follows: 0 = was not identified; 1 = identified in the dry period or in the first 100 days in milk; 2 = identified between 101 and 200 days in milk; 3 = identified between 201 and 305 days in milk. 2.4. Cow-level information: data management Information on breed, calving number, calving date, insemination dates, conception date, dry-off date, removal date, milk production, breeding value for milk yield (MY index) and the occurrence of other diseases during the lactation was supplied by the Danish Cattle Organisation (Dansk Kvæg, 2003). Administrative errors that were made during on-farm recording made it impossible to retrieve any information on 643 cows, for this reason they were not included in the analysis. Of the remaining 5518 cows, 5322 were Holstein Friesians (96.5%), 127 were of an undefined crossbreed (2.3%), 43 were Danish Red Cattle (RDM, a dual purpose breed, 0.8%) and the remaining fraction of the cows were of another breed (0.5%). Breed could not be used as a covariate because of small category sizes, for that reason only HF cows were included in the analysis. All available test-day milk yields (TDY) in a cow’s lactation prior to 305 days in milk were included in the analysis. The first 305 DIM are considered the most objective part of the lactation to base a comparison on. Other studies also focused on only this part of the lactation (Warnick et al., 2001; Green et al., 2002; Hultgren et al., 2004). One thousand one hundred and fifteen cows without recordings (no participation of the farm in milk recording on 1 farm (212), infrequent milk sampling (76) and just missing values (827)) were deleted from the dataset. There is no reason to believe that data was systematically missing in certain groups differing by parity, disease status or milk yield potential. Four thousand two hundred and seven cows from 53 herds remained in the dataset for the analysis on test-day milk yield. In some herds, inseminations were not or poorly recorded; for all cows without recorded conception dates but with a subsequent calving date, conception date was estimated by subtracting 280 days from the calving date recorded in the Danish cattle database (Dansk Kvæg, 2003). 2.5. Statistical analysis The first lactation is considered the most tumultuous period of the cow’s life in which she undergoes many changes and much is physiologically demanded of her. For this reason,

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the analysis on TDY was done separately for the primiparous cows and the multiparous cows. The dataset for the former included 1492 cows of which 1226 conceived within 305 days and another 30 after 305 days, 113 were culled within 305 days and 123 were culled after 305 days. The multiparous dataset included 2715 cows of which 1920 conceived within 305 days and another 25 after 305 days, 494 were culled within 305 days and 268 cows were culled within the same lactation after 305 days. Separately for heifers and multiparous cows, a PROC MIXED (SAS, 2001) repeated measurements analysis of variance for a three-level model with random herd effects was performed to study the association between the hoof lesions and TDY. Milk yield was recorded on the same animal over time where animal was clustered in herd. A first order autoregressive covariance structure was used to account for the correlation between measurements within the same cow. Trimming diagnosis included in the analyses were the ones between days 1 and 305 of the lactation for primiparous cows and the ones between day 50 pre-partum (dry period) and 305 days post-partum for multiparous cows. All hoof lesions were entered in the model together as categorized variables with values 0–3 as described in Section 2.3. The effect of claw trimmer was accounted for by including it as fixed effect and including interaction terms between claw trimmer and every hoof lesion variable. Correction for claw trimmer was considered unnecessary when there was no variation in diagnosis caused by claw trimmer. This was established by logistic regression analyses with the (aggregated) lesion as dichotomous outcome variable and trimmer as one of the explanatory variable. This study was performed earlier by Ettema and Capion (2006). Other clinical diseases included in the analysis were the occurrence of one or more cases of mastitis (MAST) during the first 305 DIM and retained placenta (RP) as diagnosed and registered by the veterinarian on-farm. Other cow-level variables included in the initial model were parity (categorical in the multiparous model, parity 2 or parity >2), culling (binary, yes or no before 305 DIM), pregnancy status (categorical, days to conception), milk yield index (categorical), age at first calving (categorical in the primiparous model, days). Pregnancy status, milk yield index and age at first calving were included as categorical rather than continuous variables because they did not have a linear relationship with milk yield. These variables were grouped in tertiles, dividing the study population consequently in three categories of low, medium and high milk yield index and low, medium and high age at first calving. Days to conception were divided into five categories: 1 for not conceiving and the other 4 divided the cows that conceived in quartiles. Milk yield index for breeding value was the weighted average of breeding value for ECM production and the total milk quantity produced by the cow itself or its relatives (Dansk Kvæg, 2003). The associations between the explanatory variables were investigated by looking at the correlation coefficients (Spearman’s Rho) on cow level. Coefficients higher than 0.15 were never found, indicating no problem of multicollinearity. kg ECM, the outcome variable of the repeated measurement analysis, was calculated using formula 1 (Anonymous, 2002):  ECM ¼ milk ðkgÞ 

383  fat ð%Þ þ 242  protein ð%Þ þ 783:2 3140

 (1)

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Besides ECM, somatic cell count (SCC) was recorded every test day and included as a categorical, explanatory variable. Somatic cell count on a given test day was considered high if over 300,000 cells/ml and low otherwise. Lactation stage was categorized into ten classes of 30 days in milk each; the 10th category included 35 days in milk (271–305). The management strategies initially included as fixed effects in the model were feeding system (binary; total mixed ration or not), milking system (binary; automatic milking system or conventional milking parlor) and grazing strategy (binary; grazing in summer or not). For the inclusion of two-way-interactions of the hoof lesions with the other variables a balance was chosen between model fit and interpretability of the results. Interactions between the other variables were included if they changed the estimates of the effects of hoof lesions by >25%. Both final models were the result of a backward-step-wise procedure (F-test of fixed effects P  0.05 using Satterthwaite-type approximation (Satterthwaite, 1941)). After elimination of all non-significant variables, these variables were re-entered into the model one by one and retained if they had a significant effect (F-test P < 0.05) when entered alone. Variables considered to be potential confounders were forced singly into the model and retained if they changed estimates of effect by >25%. Model goodness-of-fit was assessed by examining residuals graphically (gg-plot and q-plot) and performing the Kolmogorov–Smirnov test for normal distribution of the residuals (probability 0.05 of Dstatistic being larger than the critical D-statistic) (Weisstein, 2006). Besides analysis on the aggregated lesions, the association between TDY and the separate lesions was analyzed. Depending on the extent of agreement between the associations of the separate lesions the aggregation was maintained, rejected or adjusted. When division of hoof lesions with low prevalence into lactation stage of diagnosis resulted in very low numbers per category, the lesions were categorized and analyzed as a dichotomous variable; diagnosed or not diagnosed within 305 DIM (0/1). For model building strategy and inclusion of interactions in the analysis on separate lesions the same techniques and considerations were applied as described above.

3. Results 3.1. Descriptive statistics Prevalence of hoof lesions within early (<101 DIM), mid (101–200 DIM) and late (>200 DIM) stages of lactation are shown in Table 1. Prevalences of OID and HHD are presented along with the diseases that are aggregated into them. For SH and HHE the prevalences refer only to the severe cases. For WL the prevalences refer to both cases of WLA and WLD. Of the farms included in this study, 62% implemented a type of grazing strategy during spring and summer, 34.6% fed a total mixed ration and 7.7% had an automatic milking system. In 20% of the lactations of primiparous cows there were one or more cases of mastitis, as compared to 31.4% of multiparous cows’ lactations. A retained placenta occurred after 5.9 and 12.4% of primi- and multiparous cows’ parturitions, respectively. The mean value of ECM for 12,258 test-day recordings of primiparous cows was 26.0 kg (S.D. = 5.0). For the multiparous cows the mean value of ECM for 21,599 test-day

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Table 1 Overall prevalence of hoof lesions (All) and divided in stages of lactation; before 101 DIM (1), between 101 and 200 DIM (2) and after 200 DIM (3) Parity > 1

Parity 1 All

1

2

3

All

1

2

3

Digital dermatitis

23.3

6.2

10.3

6.8

21.3

9.8

6.0

5.5

Other interdigital diseases Heel horn erosion Interdigital hyperplasia Interdigital dermatitis

32.9 7.2 3.6 27.9

10.5 1.6 1.3 9.1

12.9 3.7 1.0 10.8

9.5 7.2 1.3 8.0

41.2 9.1 6.4 28.7

16.8 4.1 2.7 14.0

15.4 2.1 2.1 8.0

9.0 2.9 1.6 6.7

Hoof horn diseases Sole ulcer White line diseases Sole haemorrhage Double sole

44.1 4.7 3.4 40.4 3.1

16.4 1.2 0.7 15.5 0.7

16.8 2.7 0.8 15.2 1.5

10.9 0.8 1.9 9.7 0.9

42.2 6.9 7.8 35.8 6.7

17.4 2.3 3.4 14.8 2.5

12.9 2.2 2.0 11.1 2.2

11.9 2.4 2.4 9.9 2.0

The percentages per stage of lactation represent the % of all cows (including those not trimmed at that time) positively diagnosed with specified lesions; 1492 primiparous cows; 2715 multiparous cows.

recordings was 30.2 kg (S.D. = 7.4). A SCC over 300,000 cells/ml was registered on 9.7 and 25.9% of the test days for primi- and multiparous cows, respectively. 3.2. Associations with test-day milk yields The results of the analyses of variance of TDY are displayed in Tables 2 and 3 for the primiparous cows and Tables 4 and 5 for the multiparous cows. Estimates for lactation stage for cows without lesions and the estimates for trimmers are omitted from Tables 2–5 in order to limit table size. For the primiparous model, baseline for comparison is a cow in late lactation (271–305 DIM), without a diagnosed hoof lesion, that did not conceive, had the highest MY index, was not culled before 305 DIM, had access to pasture in the spring and summer, had an age at first calving (AFC) >887 days, no retained placenta and a SCC below 300,000 cells/ml on a given test day. An interaction term for trimmer and lesion was included for DD, OID and SH. The estimates for trimmer and the interaction terms are omitted from the table; the trimmer that trimmed most cows (45%) is used as a reference in the analysis. For the other lesions interaction with trimmer was not significant in the final model (SU) and trimmer was not significant in the logistic regression model (DS and WL) (Ettema and Capion, 2006). Aggregation of SH, WL, DS and SU into HHD could not be justified judging from the differences in associations of the separate lesions with TDY. Due to the low numbers of WL, DS and SU division into stages of lactation (DS, SU) or inclusion of interaction terms (WL) was not possible. There was no significant interaction between SU and MYI; all primiparous cows with a diagnosis of SU produced on average 0.59 kg (95% CI: 0.24, 0.95) ECM more per test day. Cows with a low MYI produced 1.19 kg (1.93, 0.45) less per test day when DS was diagnosed and treated during the first 100 days of lactation. For the multiparous model, baseline for comparison is a cow of parity >2 in late lactation (271–305 DIM), without a diagnosed hoof lesion, that did not conceive, had the

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Table 2 Associations of hoof lesions at claw trimming at different stages of lactation with test-day yield for primiparous cows (n = 1492); kg ECM and 95% confidence interval Variable Intercept

Estimate

95% CI

23.23

22.26

24.21

DD <101 DIM 101–200 DIM >200 DIM <101 DIM  MYI low <101 DIM  MYI med 101–200 DIM  MYI low 101–200 DIM  MYI med >200 DIM  MYI low >200 DIM  MYI med

S1.22 0.61 0.46 1.17 0.06 S1.60 0.39 S0.83 0.06

1.99 0.02 0.29 0.34 0.86 2.27 1.04 1.66 0.71

0.46 1.20 1.21 1.99 0.74 0.93 0.26 0.01 0.83

OID <101 DIM 101–200 DIM >200 DIM <101 DIM  MYI low <101 DIM  MYI med 101–200 DIM  MYI low 101–200 DIM  MYI med >200 DIM  MYI low >200 DIM  MYI med

0.45 S0.74 S1.66 0.55 0.16 1.13 0.88 0.89 0.62

0.22 1.32 2.25 1.21 0.52 0.53 0.30 0.20 0.03

1.12 0.16 1.08 0.11 0.84 1.72 1.47 1.58 1.28

DD  OID <101 DIM 101–200 DIM >200 DIM

1.32 1.37 0.39

0.44 0.65 1.18

2.20 2.10 0.39

SH <101 DIM 101–200 DIM >200 DIM <101 DIM  MYI low <101 DIM  MYI med 101–200 DIM  MYI low 101–200 DIM  MYI med >200 DIM  MYI low >200 DIM  MYI med

0.33 0.39 0.09 0.02 0.48 0.61 0.75 0.11 0.55

0.22 0.14 0.72 0.61 0.07 0.04 0.22 0.83 0.10

0.89 0.91 0.90 0.57 1.03 1.18 1.29 0.61 1.20

0.25 0.65 S0.82

1.28 1.45 1.45

0.77 0.15 0.20

0.20 S1.39 0.14

0.49 2.40 0.82

0.89 0.38 1.10

0.59

0.24

0.95

WL <101 DIM 101–200 DIM >200 DIM DS In 305 DIM In 305 DIM  MYI low In 305 DIM  MYI med SU In 305 DIM

DD, digital dermatitis; OID, other interditgital diseases; SH, sole haemorrhages; WL, white line disease; DS, double sole; SU, sole ulcer; MYI, milk yield index. Bold values are significant (P < 0.05).

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Table 3 Associations of cow-level predictors, other than hoof lesions, with test-day yield for primiparous cows (n = 1492); kg ECM and 95% confidence interval (CI) Variable

Estimate

95% CI

MYI Low Medium High

S4.68 S2.66 0

4.94 2.92

4.42 2.40

Conception Quartile 1 a Quartile 2 Quartile 3 Quartile 4 Not conceived

S0.52 0.09 0.61 1.00 0

0.80 0.19 0.34 0.74

0.24 0.36 0.87 1.25

High SCC Present on test day Not present

S0.37 0

0.61

0.13

Culled < 305 Culled within 305 DIM Not culled

S2.24 0

2.61

1.87

1.25 0

0.19

2.32

S2.09 S1.09 0

2.29 1.27

1.88 0.90

Grazing No access to pasture Access to pasture AFC <809 days 809–887 days >887

MYI, milk yield index; SCC, somatic cell count; AFC, age at first calving. Bold values are significant (P < 0.05). a DIM at conception are divided into four quartiles. Table 4 Associations of hoof lesions at claw trimming at different stages of lactation with test-day yield for multiparous cows (n = 2715); kg ECM and 95% confidence interval (CI) Variable

Estimate

Intercept

95% CI

21.50

20.47

22.53

DD <101 DIM 101–200 DIM >200 DIM <101 DIM  MYI low <101 DIM  MYI med 101–200 DIM  MYI low 101–200 DIM  MYI med >200 DIM  MYI low >200 DIM  MYI med

0.26 0.15 1.10 0.45 S1.04 0.02 0.33 1.34 1.16

0.34 0.60 0.34 1.14 1.69 0.88 0.46 2.22 2.01

0.85 0.89 1.87 0.24 0.39 0.84 1.12 0.47 0.30

OID <101 DIM 101–200 DIM

0.01 0.18

0.56 0.43

0.55 0.79

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Table 4 (Continued ) Variable

Estimate

95% CI

>200 DIM <101 DIM  parity 2 101–200 DIM  parity 2 >200 DIM  parity 2 <101 DIM  MYI low <101 DIM  MYI med 101–200 DIM  MYI low 101–200 DIM  MYI med >200 DIM  MYI low >200 DIM  MYI med

S1.70 0.97 0.69 0.12 S0.57 0.32 0.58 0.43 0.29 013

2.41 0.52 0.17 0.47 1.12 0.22 1.22 1.07 0.43 0.84

1.00 1.41 1.22 0.70 0.03 0.85 0.07 0.20 1.01 0.57

HHD* <101 DIM 101–200 DIM >200 DIM <101 DIM  parity 2 101–200 DIM  parity 2 >200DIM  parity 2 <101 DIM  MYI low <101 DIM  MYI med 101–200 DIM  MYI low 101–200 DIM  MYI med >200 DIM  MYI low >200 DIM  MYI med

S0.73 0.44 S1.21 0.01 0.89 0.52 0.03 0.40 0.43 0.19 0.92 0.51

1.30 1.09 1.90 0.46 0.39 0.02 0.61 0.15 0.23 0.82 0.20 0.16

0.16 0.22 0.52 0.44 1.39 1.07 0.56 0.94 1.08 0.44 1.63 1.19

DS <101 DIM 101–200 DIM >200 DIM <101 DIM  MYI low <101 DIM  MYI med 101–200 DIM  MYI low 101–200 DIM  MYI med >200 DIM  MYI low >200 DIM  MYI med

S1.38 S1.33 1.15 3.21 1.17 0.76 0.84 0.98 0.72

2.23 2.25 0.16 1.95 0.04 0.48 0.43 2.40 0.56

0.52 0.40 2.13 4.47 2.37 2.00 2.11 0.43 2.00

DD, digital dermatitis; OID, other interdigital diseases; HHD*, hoof horn diseases (all hoof horn disease, except double sole); DS, double sole; MYI, milk yield index. Bold values are significant (P < 0.05).

highest MY index, was not culled before 305 DIM, did not have a retained placenta or mastitis and had a low SCC on a given test day. An interaction term for trimmer and lesion was included for DD, OID and HHD. The estimates for trimmer and the interaction terms are omitted from the table; the trimmer that trimmed most cows (45%) is used as a reference in the analysis. For DS trimmer was not significant in the logistic regression model (Ettema and Capion, 2006). All lesions originally aggregated into HHD showed comparable associations with TDY when analyzed separate, except for DS which is therefore presented as a separate lesions. In Tables 6 and 7 the associations between the lesions diagnosed at different stages of lactation and TDY are presented for different categories of MY index for primiparous and multiparous cows, respectively.

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Table 5 Associations of cow-level predictors, other than hoof lesions, with test-day yield for multiparous cows (n = 2715); kg ECM and 95% confidence interval (CI) Variable

Estimate

95% CI

Parity 2 Parity 3

0.28 0

0.82

0.26

MYI Low Med High

S4.68 S2.27 0

5.01 2.59

4.34 1.95

Parity 2 MYI low MYI med MYI high

S0.73 S0.90 0

1.11 1.27

0.35 0.55

Conception Quartile 1 a Quartile 2 Quartile 3 Quartile 4 Not conceived

S0.65 0.17 0.81 1.53 0

0.90 0.42 0.57 1.29

0.40 0.08 1.08 1.78

High SCC Present on test day Not present

S1.43 0

1.60

1.26

0.38 0

0.21

0.54

RP Present Not Present

S0.85 0

1.08

0.62

Culled < 305 Culled within 305 DIM Not culled

S3.04 0

3.30

2.78

Mastitis Present in 305 DIM Not Present

MYI, milk yield index; SCC, somatic cell count; RP, retained placenta. Bold values are significant (P < 0.05). a DIM at conception are divided into four quartiles.

More negative associations between DD and TDY are found for primiparous cows compared to multiparous cows, especially the ones diagnosed early in lactation (Tables 6 and 7). For cows of all parities and all MY indexes a diagnosis of OID in late lactation is associated with a stronger negative association compared to a diagnosis early in lactation. A diagnosis of a severe SH is associated with higher test-day yields in the primiparous model, except for the cows with a high MY index. More negative associations of hoof horn diseases and TDY are found in the multiparous model as parity and MY index go up. Both positive and negative associations are found for the diagnosis of DS at different stages of lactation for cows with different MY indexes. A diagnosis of DS in late lactation is associated with a higher TDY for cows of both medium and high MY index. In case DS is observed during early or mid lactation, the association with TDY is negative for cows with a high MY index.

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Table 6 Associations of hoof lesions diagnosed at different stages of lactation with test-day yield (kg ECM) specified for different levels of MY index (MYI) of primiparous cows; parameter estimates and 95% confidence intervals (CI) <101 DIM

95% CI

101–200 DIM

95% CI

>200 DIM

95% CI

Digital dermatitis Low MYI 0.06 Med MYI 1.28 High MYI 1.22

0.78 2.01 1.99

0.66 0.55 0.46

S0.99 0.22 0.61

1.55 0.28 0.02

0.44 0.73 1.20

0.37 0.52 0.46

1.12 0.17 0.29

0.37 1.22 1.21

Other interdigital diseases Low MYI 0.10 Med MYI 0.61 High MYI 0.45

0.76 0.02 0.22

0.56 1.23 1.12

0.39 0.15 0.74

0.16 0.40 1.32

0.94 0.70 0.16

0.78 1.04 1.66

1.48 1.70 2.25

0.07 0.37 1.08

Sole haemorrhages Low MYI 0.31 Med MYI 0.88 High MYI 0.33

0.27 0.30 0.22

0.89 1.33 0.89

1.00 1.14 0.39

0.48 0.67 0.14

1.53 1.61 0.91

0.02 0.64 0.09

0.92 0.18 0.72

0.88 1.47 0.90

Bold values are significant (P < 0.05).

3.3. Model fit For the outcomes of the repeated measurement analysis, the residuals were studied by farm. In the primiparous model, 36 of the 53 residuals fitted a normal distribution based on the Kolmogorov–Smirnov test in the univariate procedure. In the multiparous model 28 of the 53 residuals fitted a normal distribution. The proportion of the variation explained by herd in the TDY analysis was 17 and 15% in the primi- and multiparous model, respectively.

4. Discussion 4.1. Prevalence of health disorders In this study hoof lesions were diagnosed on as many as 80% of all cows in Danish dairy herds. Of these disorders infectious digital dermatitis (DD) was more prevalent in primiparous than multiparous cows, whereas the hoof lesions aggregated into OID were more prevalent in multiparous than primiparous cows. These findings are consistent with others reports. A recent Dutch study reported an OR of 1.87 and 2.07 at the end of the pasture and housing season, respectively, for primiparous cows having DD compared to cows of parity 3 and up (Somers et al., 2005a). Somers et al. (2005b) reported an OR of 2.34 and 3.98 for older cows having interdigital dermatitis at the end of the pasture and housing season, respectively. In the current study severe sole haemorrhages were with 40.4% versus 35.8% more prevalent among primiparous than multiparous cows. All other lesions initially aggregated into HHD were more prevalent among multiparous cows compared to primiparous cows; SU (6.9% versus 4.7%), WL (7.8% versus 3.4%), DS (6.7% versus 3.1%). Manske et al. (2002b) reported comparable results with high OR’s for

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Table 7 Associations of hoof lesions diagnosed at different stages of lactation with test-day yield (kg ECM) specified for different levels of MY index (MYI) and parity of multiparous cows; parameter estimates and 95% confidence intervals <101 DIM 95% CI

>200 DIM 95% CI

101–200 DIM 95% CI

Digital dermatitis Low MYI 0.19 Med MYI 0.78 High MYI 0.26

0.80 0.42 1.33 0.23 0.34 0.85

0.13 0.48 0.15

0.61 0.20 0.60

0.86 0.25 1.15 0.05 0.89 1.10

0.96 0.80 0.34

Other interdigital diseases Parity 2 Low MYI 0.39 Med MYI 1.28 High MYI 0.96

0.16 0.75 0.46

0.93 1.80 1.45

0.29 0.44 0.87

0.36 0.17 0.26

0.95 1.30 1.05 1.72 1.48 1.59

1.99 0.60 2.39 1.06 2.21 0.97

1.10 0.06 0.20 0.82 0.56 0.55

0.40 0.25 0.18

0.98 0.84 0.43

0.19 1.41 0.34 1.84 0.79 1.70

2.01 0.81 2.52 1.16 2.41 1.00

Hoof horn diseases (except double sole) Parity 2 Low MYI S0.77 1.40 0.13 Med MYI 0.34 0.93 0.24 High MYI 0.74 1.31 0.18

0.88 0.27 0.46

0.21 0.36 0.19

1.56 0.23 0.89 0.18 1.10 0.69

0.48 0.93 0.85 0.50 1.36 0.02

1.31 0.21 0.01 0.87 0.19 S0.62 1.30 0.16 0.44

0.61 0.59 0.30 1.19 0.06 0.70 0.22 1.21 1.09

0.88 0.28 1.33 0.06 1.90 0.52

0.90 2.77 0.57 1.07 0.65 0.49 2.23 0.52 S1.33

1.41 0.28 1.37 0.41 2.25 0.40

0.84 0.99 0.16

Parity > 2 Low MYI Med MYI High MYI

0.58 0.31 0.01

Parity > 2 Low MYI 0.76 Med MYI 0.34 High MYI S0.73 Double sole Low MYI Med MYI High MYI

1.83 0.21 S1.38

0.16 1.87 1.15

0.48 0.69 1.87

1.16 2.74 2.13

Bold values are significant (P < 0.05).

sole ulcer and separations; 2.41 and 3.33, respectively, for cows over parity 4 compared to primiparous cows. Manske et al. (2002b) only qualified parity as high as 5 as a risk factor for haemorrhages (OR = 1.38). Parity 2, 3 and 4 had an OR significantly below 1 versus parity 1. In the current study, a higher proportion of older cows had mastitis (31.4% versus 20%), elevated somatic cell count levels (25.9% versus 9.7%) (higher probability of having a sub clinical udder infection (Brolund, 1990)) and retained placenta (12.4% versus 5.9%). Østergaard and Gro¨hn (1999) reported a higher incidence of a clinical udder infection in multiparous (33%) compared to primiparous (23%) Danish Holsteins. A higher frequency of RP in older cows was also found by Emanuelson et al. (1993) and Rajala and Gro¨hn (1998), although the latter reported overall lower prevalences (3.1% versus 2.0%) than the current study.

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4.2. Associations between TDY and hoof lesions: the value of early diagnosis Analysis of the association between OID and test-day yield has revealed an interesting pattern. The association of an early diagnosis and treatment was either positive or less negative compared to a diagnosis and treatment in late lactation (201–305 DIM). The positive association of TDY with an early diagnosis of OID, especially in parity 2 cows, may indicate that high yielding cows are more susceptible to OID. Similar findings have been reported in other studies (Dohoo and Martin, 1984; Rowlands and Lucey, 1986; Enevoldsen et al., 1991; Barkema et al., 1994; Rajala-Schultz et al., 1999; Green et al., 2002; Hultgren et al., 2004). A high production level is known to be a risk factor for other production diseases as well (Fourichon et al., 1999). The consistent decline in test-day yield associated with later detection of OID may indicate the positive value of early diagnosis. No effect of a disease is claimed here, just an association of its diagnosis and treatment with TDY. When OID is detected and treated early in lactation, the cow has a ‘‘lesion-free’’ lactation ahead of her, whereas when OID is detected and treated later, her ‘‘lesion-free’’ lactation is shorter and she may have been walking around with the lesion for some time. It is assumed here that many of the detected lesions have not been causing clinical lameness and have therefore not been treated earlier and have only come to the attention during routine claw trimming. Although this hypothesis cannot be tested in the current study because onset of the lesion is not known, a study by Green et al. (2002) supports this theory. Green et al. (2002) found reduced milk yield 5 months prior to detection of clinical lameness. In the current study, more significant and stronger associations were found in multiparous versus primiparous cows. This is consistent with more milk loss due to OID in multiparous than primiparous cows. A similar finding was reported by Warnick et al. (2001) (375 kg versus 141 kg lost per lactation for second and first lactation cows, respectively, suffering from lameness). Similar patterns were not detected for the other lesions; almost the opposite seems true for primiparous cows with medium and high MY index with DD. A diagnosis early in lactation shows a negative association with TDY, whereas there is a, positive, nonsignificant association with a diagnosis later in lactation. These different associations between DD and test-day yield may be due to painfulness of DD and its effective management on farms in the study. Studies on painfulness of hoof lesions found a lower nociceptive threshold for acute digital tissue infection (Whay et al., 1998). In the same study DD showed a higher lameness score compared to heel erosion for example, one of the lesions aggregated into OID. Manske et al. (2002a) found all hoof lesions more prevalent in lame than in non-lame cattle, except for dermatitis. Dermatitis was an aggregate in this study which comprised predominantly HHE and ID (only 3% DD). Due to the higher painfulness of DD it is likely that these diseases get treated more adequately with footbaths or individual treatment. DD is therefore less likely to go unnoticed for a long period of time. Footbaths are often used in the treatment and prevention of DD, which is done with varying products with varying success (Rodriguez-Lainz et al., 1996; Laven and Proven, 2000; Laven and Hunt, 2002). In this study population, 41 herds used footbaths either on a regular basis or when needed. In these 41 herds, DD is treated all year through which may keep the disease level and severity at an acceptable level, thus minimizing long term

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suffering from the disease and an effect on milk yield. The negative association of DD diagnosed in early lactation on primiparous cows might be an indication of milk loss due to short term suffering of DD during peak lactation (Table 6). A solid conclusion cannot be made due to this study’s design. A previous study by Argaez-Rodriguez et al. (1997) found a non-significant (P = 0.35) decrease (122 kg) in milk yield in DD affected cows. The positive association between DD and TDY in high yielding, multiparous cows and negative or no association in low or medium-yielding cows support the hypothesis that high milk yield is also a risk factor for DD, consistent with the previously mentioned studies. The associations between the various hoof horn diseases and TDY differed and aggregation was therefore rejected in the primiparous model and modified in the multiparous model. Associations between TDY and severe sole haemorrhages were positive in the primiparous model, although not significant for the category of high yielding cows. With respect to SU, interaction with MY index was insignificant and the positive association therefore goes for all primiparous cows. Hultgren et al. (2004) reported a positive association between sole ulcer and milk yield, with an increased lactational yield of 479 kg ECM for cows with a sole ulcer. In this Swedish study parity and milk yield index were both included in the model, although interaction terms with sole ulcer were not. Both WL and DS showed a negative association with TDY. Clearly aggregation into HHD could not be justified. Not only is it hard to separate milk yield as a cause and effect of hoof lesions, there are also differences in association with milk yield between the several diseases that affect the cow’s hoof horn. Except for DS, aggregation of the lesions into HHD as initially planned could be justified for multiparous cows. The associations with TDY however were mainly negative, in contrast to the positive values for SH, and SU in the primiparous model and positive value for SU found by Hultgren et al. (2004). The negative values for multiparous cows may be due to the composition of the control group for the older cows. Older cows with a hoof lesion are compared to other, non-diseased older cows. One of the reasons for these older cows to be maintained in the herd is their high milk production. Diseased, older cows are therefore compared to high yielding control cows. Diseased primiparous cows are compared to all other primiparous cows, a group that has not yet been selected for milk yield; the baseline milk production is likely higher in the cows of parity 3 and up. A comparison with the study of Hultgren et al. (2004) is hard to make, since the analysis was not performed for different parity groups and sole ulcer was analyzed as a single lesion. For double sole extreme associations, both positive and negative, were found in the multiparous model. A case diagnosed and treated early in lactation was associated with a lower TDY for high yielding cows and higher TDY for low yielding cows. A late diagnosis was associated with a higher TDY for cows with medium and high MY index. To draw solid conclusions about the effect of DS in different stages of lactation, more knowledge about the onset of the disease is necessary. Because of this study’s cross-sectional design, it is difficult to draw conclusions about causality of the associations. It is not known what happened to the studied cows before or after trimming for most hoof lesions. Whether the cow suffered from any lesions later on is not known and cannot be corrected for. The exception was the occurrence of IP, which was dealt with by including it when occurrence was in the same stage of lactation as periodic trimming and deleting it otherwise. These IP cases were excluded because there were not

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enough to use as a variable, and because IP reportedly affects production and reproduction (Hernandez et al., 2001). 4.3. Other cow-level predictors for milk yield Grazing appeared to be the only farm-level effect significantly associated with TDY. In primiparous cows, grazing was associated with decreased milk yield of 1.25 kg (95% CI: 0.19, 2.32). This is likely because the ration of cows not grazed is more stable and of higher energy content than the grass the cows take in when they are grazing. The lower TDY in grazed cows may also be due to confounding by herd size. Milk production is on average higher for larger dairy farms than smaller dairy farms in Denmark (Tinderup and Enemark, 2003). Additionally, as farm size increases, implementation of a grazing strategy gets more difficult. The effect of age at first calving on TDY found in this study differed from other reports. Ettema and Santos (2004) reported significantly lower milk yield for heifers in the low AFC group compared to the medium group, but not for the medium group compared to the high AFC group, whereas the current study reported significantly lower milk yield for both heifers in the low and medium AFC groups compared to the high AFC group. Although both studies divided AFC into three categories, the cut-off points for Ettema and Santos (2004) (<701, 701–750, >750 days) differed from the current study (<809, 809– 887, >887 days); different cut-off points may explain the different results. Non-claw diseases were not consistently associated with decreased test-day yield. Retained placenta was associated with a decreased test-day milk yield in only multiparous cows; 0.85 kg ECM (1.08, 0.62). In primiparous cows, mastitis at least once in the lactation was not significantly associated with test-day yield, although a high somatic cell count was negatively associated with milk yield recorded on the same test day. In multiparous cows mastitis was positively associated with TDY and high SCC showed a stronger, negative association with TDY. The association of clinical mastits with TDY should be considered together with an elevated SCC level; their combined association was stronger in the multiparous cows compared to the primiparous cows. This is consistent with the findings of Østergaard and Gro¨hn (1999), who reported losses of 122 kg for primiparous and 220 kg for multiparous cows per case of clinical mastitis. 4.4. Aggregation of hoof lesions An attempt was made to do the analysis on the aggregated lesions instead of the lesions separate. Dairy cattle lameness is caused by many different claw and hoof disorders. The lesions causing lameness often differ in risk factors, etiology and effect on the cow’s heath. In studies on the effect of lameness, distinction is not always made among the causes of this health disorder (Warnick et al., 2001; Green et al., 2002). In risk factor analysis the different lesions are often split up (Manske et al., 2002a; Somers et al., 2003), although in the study of Manske et al. (2002a) interdigital dermatitis and heel horn erosion were aggregated. Somers et al. (2003) however aggregate every kind of dermatitis and heel horn erosion into one. A comparable aggregation was made by Collick et al. (1989) in a study on the associations between types of lameness and fertility. They included interdigital phlegmon (IP) and all forms of dermatitis into ‘‘interdigital diseases’’. The same is done in

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this study, except that digital dermatitis is not included in our OID category. This seems justifiable, judging from the prevalences among different parity groups and the different associations with TDY found for OID and DD. ‘‘Separation’’ is another disease that is aggregated by Manske et al. (2002b); including all white line fissures and double sole. Somers et al. (2003) categorized them into white line disease, white line abscess and double sole. They separated sole ulcer from other disease to the sole (white line abscess, foreign bodies in the sole and pricked or punctured sole). Together with what Manske et al. (2002b) called ‘‘separations’’, other lesions associated with damage to the sole are aggregated into hoof horn diseases in this study. For both primiparous and multiparous cows, aggregation of HHE, ID, IH and IP into OID could be justified based on the comparable associations between separate lesions with TDY. The original aggregation of SH, SU, WLD and DS into HHD was not maintained. Especially in the primiparous model there was poor agreement in the associations between the separate lesions and TDY. In the multiparous model the aggregation was adjusted by taking DS out of the aggregation. Agreement in risk factors as described in literature was used as reasoning for aggregation in planning the current study. Based on the outcomes of this study the aggregation of HHD cannot be justified for decision problems where the associations between the lesions and TDY are important. However, the aggregation of ID, IH and IP into OID appears to be justified both regarding risk factors and associations with milk yield. 4.5. Model fit For the outcomes of the repeated measurement analysis 36 out of 53 and 28 out of 53 residuals fitted a normal distribution in the primi- and multiparous models, respectively. When the qq-plots and g-plots were studied it appeared that a low number of high and low values caused the non-normality. Prior to the analysis the data was already studied for biologically, reasonable values and extreme values were deleted. Inclusion of the other health disorders (mastitis, retained placenta) in interaction terms with MY index and parity might have improved fit. These interaction terms were not included because they did not affect parameter estimates for the hoof lesions, and severely compromised interpretability of results. 4.6. External validity and bias The study population was a selection of 55 farmers on Jutland, the Danish peninsula. Extrapolation to all Danish dairy herds is to some extent justifiable because the largest proportion of the dairy farms and cows in Denmark are located on the mainland instead of on the islands. The herds selected were all housed in free-stalls with slatted floors and with predominantly Holstein Friesian cows producing on average 9000 km Energy Corrected Milk per lactation. Although these herds are not representative for all Danish farms (Tinderup and Enemark, 2003), the selected population is a good sample of the large scale Danish dairy farms of the future, which are the target population for this study. Selection of the herds by the hoof trimmers was not done selectively; trimmers simply included all client herds with the requested housing type (slatted floors) and dominant breed (HF) in order to represent the target population. The small set of hoof trimmers that

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agreed to join the study might have introduced bias. They might not represent all hoof trimmers and the herds selected by them might therefore not be a representative sample of the entire population. Although on all farms a form of periodic trimming was applied, the frequency of annual trimmings per farm differed; questionnaires revealed that the majority of the herds got trimmed twice a year (38), 10 herds got trimmed once a year and 6 herds got trimmed three times. It can be expected that lesions found in herds that were only trimmed once a year might be more severe. On the other hand, the necessity of only one annual trimming might be an indication of good hoof health on these farms. Many other management strategies are of influence here and correction was made for this by defining the clustered structure of cows within herd in all analyses.

5. Conclusion The associations of hoof lesions diagnosed at trimming with milk production were studied in a cross-sectional study with follow up. This revealed some new insights in the role of sub clinical lameness in dairy cattle. Judging from the found associations, aggregation of white line disease, sole haemorrhages, sole ulcer and double sole into hoof horn diseases could not be justified. Whether a study is done on hoof lesion’s risk factors or association with milk yield should be taken into account when making aggregates. The concept of the value of early diagnosis was introduced with respect to other interdigital disease (interdigital hyperplasia, heel horn erosion and interdigital dermatitis). A diagnosis and treatment late in lactation was associated with a lower TDY compared to cows treated during early and peak lactation. This finding may be related to the length of time that the lesion has been present and affecting milk yield prior to detection, although that cannot be confirmed in the current cross-sectional study because lesion onset is unknown. A change in the dairy man’s management practice to trim cows an extra time early in lactation might be worth considering. An intervention study or a study based on longitudinal observational data is recommended to confirm the theory of the value of early diagnosis.

Acknowledgements The authors wish to thank Pia Flagstad from Dansk Kvæg for her efforts in data supply and interpretation from the Danish cattle database. Besides, Annette Kjær Ersbøll, Mogens Krogh and Søren Østergaard are thanked for their assistance with the analysis.

References Alban, L., 1995. Lameness in Danish dairy cows: frequency and possible risk factors. Prev. Vet. Med. 22, 213–225. Anonymous, 2002. Handbog i kvæghold (Handbook in Cattle Husbandry). Landbrugets Ra˚dgivningscenter, Landbrugsforlaget, Grenaa, Denmark (in Danish).

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J.F. Ettema et al. / Preventive Veterinary Medicine 79 (2007) 224–243

Argaez-Rodriguez, F.J., Hird, D.W., Hernandez, J., Read, D.H., Rodriguez-Lainz, A., 1997. Papillomatous digital dermatitis on a commercial dairy farm in Mexicali, Mexico: incidence and effect on reproduction and milk production. Prev. Vet. Med. 32, 275–286. Barkema, H.W., Westrik, J.D., van Keulen, K.A.S., Schukken, Y.H., Brand, A., 1994. The effects of lameness on reproductive performance, milk production and culling in Dutch dairy farms. Prev. Vet. Med. 20, 249–259. Blowey, R.W., Sharp, M.W., 1988. Digital dermatitis in dairy cattle. Vet. Rec. 122, 505–508. Brolund, J., 1990. Cellhatens tekniska utnyttende i kokontrollen (Technical Utilization of Cell-Count in the Milk Recording System). Swedish Association of Livestock Breeding Production, Eskilstuna, Sweden, pp. 40–42. Clarkson, M.J., Downham, D.Y., Faull, W.B., Hughes, J.W., Manson, F.J., Merritt, J.B., Murray, R.D., Russell, W.B., Sutherst, J.E., Ward, W.R., 1996. Incidence and prevalence of lameness in dairy cattle. Vet. Rec. 138, 563–567. Collick, D.W., 1997. Interdigital hyperplasia. In: Greenough, R.D., Weaver, P.R. (Eds.), Lameness in Cattle. pp. 119–120. Collick, D.W., Ward, W.R., Dobson, H., 1989. Associations between types of lameness and fertility. Vet. Rec. 125, 103–106. Dansk Kvæg, 2003. Danish Cattle Organisation. http://www.lr.dk. Dohoo, I.R., Martin, S.W., 1984. Disease, production and culling in Holstein-Friesian cows. IV. Effects of disease on production. Prev. Vet. Med. 2, 755–770. Emanuelson, U., Oltenacu, P.A., Gro¨hn, Y.T., 1993. Nonlinear Mixed Model Analyses of Five Production Disorders of Dairy Cattle, pp. 2765–2772. Enevoldsen, C., Gro¨hn, Y.T., Thysen, I., 1991. Heel erosion and other interdigital disorders in dairy cows: associations with season, cow characteristics, disease, and production. J. Dairy Sci. 74, 1299–1309. Ettema, J.F., Capion, N., 2006. A cross sectional study into prevalence, correlations and risk factors of claw lesions in Danish Holsteins. In: Proceedings of the 24th Word Buiatrics Congress (CD-ROM). Ettema, J.F., Østergaard, S., 2006. Modeling costs of lameness in dairy herds with representation of uncertainty in the state of nature. In: Proceedings of the 11th International Symposium on Veterinary Epidemiology and Economics (CD-ROM). Ettema, J.F., Santos, J.E.P., 2004. Impact of age at calving on lactation, reproduction, health, and income in firstparity Holsteins on commercial farms. J. Dairy Sci. 87, 2730–2742. Fourichon, C., Seegers, H., Bareille, N., Beaudeau, F., 1999. Effects of disease on milk production in the dairy cow: a review. Prev. Vet. Med. 41, 1–35. Green, L.E., Hedges, V.J., Schukken, Y.H., Blowey, R.W., Packington, A.J., 2002. The impact of clinical lameness on the milk yield of dairy cows. J. Dairy Sci. 85, 2250–2256. Greenough, P.R., Vermunt, J.J., 1991. Evaluation of subclinical laminitis in a dairy herd and observations on associated nutritional and management factors. Vet. Rec. 128, 11–17. Hernandez, J., Shearer, J.K., Webb, D.W., 2001. Effect of lameness on the calving-to-conception interval in dairy cows. JAVMA 218, 1611–1614. Holzhauer, M., Hardenberg, C., Bartels, C.J.M., Frankena, K., 2003. Preliminary results of prevalences of and correlations between major rear claw disorders in 348 Dutch dairy herds. In: Proceedings of the 13th International Symposium and 5th Conference of Lameness in Ruminants. pp. 40–43. Hultgren, J., Manske, T., Bergsten, C., 2004. Associations of sole ulcer at claw trimming with reproductive performance, udder health, milk yield, and culling in Swedish dairy cattle. Prev. Vet. Med. 62, 233–251. Laven, R.A., Hunt, H., 2002. Evaluation of copper sulphate, formalin and peracetic acid in footbaths for the treatment of digital dermatitis in cattle. Vet. Rec. 151, 144–146. Laven, R.A., Proven, M.J., 2000. Use of an antibiotic footbath in the treatment of bovine digital dermatitis. Vet. Rec. 147, 503–506. Manske, T., Hultgren, J., Bergsten, C., 2002a. Prevalence and interrelationships of hoof lesions and lameness in Swedish dairy cows. Prev. Vet. Med. 54, 247–263. Manske, T., Hultgren, J., Bergsten, C., 2002b. The effect of claw trimming on the hoof health of Swedish dairy cattle. Prev. Vet. Med. 54, 113–129. Melendez, P., Bartolome, J., Archbald, L.F., Donovan, A., 2003. The association between lameness, ovarian cysts and fertility in lactating dairy cows. Theriogenology 59, 927–937. Østergaard, S., Gro¨hn, Y.T., 1999. Effects of diseases on test day milk yield and body weight of dairy cows from Danish research herds. J. Dairy Sci. 82, 1188–1201.

J.F. Ettema et al. / Preventive Veterinary Medicine 79 (2007) 224–243

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Rajala, P.J., Gro¨hn, Y.T., 1998. Effects of dystocia, retained placenta, and metritis on milk yield in dairy cows. J. Dairy Sci. 81, 3172–3181. Rajala-Schultz, P.J., Gro¨hn, Y.T., McCulloch, C.E., 1999. Effects of milk fever, ketosis, and lameness on milk yield in dairy cows. J. Dairy Sci. 82, 288–294. Rodriguez-Lainz, A., Hird, D.W., Carpenter, T.E., Read, D.H., 1996. Case-control study of papillomatous digital dermatitis in Southern California dairy farms. Prev. Vet. Med. 28, 117–131. Rowlands, G.J., Lucey, S., 1986. Changes in milk yield in dairy cows associated with metabolic and reproductive disease and lameness. Prev. Vet. Med. 4, 205–221. SAS, 2001. Users Guide (Release 8.02). SAS Inst. Inc., Cary, NC, USA. Satterthwaite, F.E., 1941. Synthesis of variance, pp. 309–316. 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. Somers, J.G.C.J., Frankena, K., Noordhuizen-Stassen, E.N., Metz, J.H.M., 2005a. Risk factors for digital dermatitis in dairy cows kept in cubicle houses in The Netherlands. Prev. Vet. Med. 71, 11–21. Somers, J.G.C.J., Frankena, K., Noordhuizen-Stassen, E.N., Metz, J.H.M., 2005b. Risk factors for interdigital dermatitis and heel erosion in dairy cows kept in cubicle houses in The Netherlands. Prev. Vet. Med. 71, 23–34. Tinderup, M., Enemark, P.S., 2003. Kvæginfo no. 1112. Dansk Kvæg. http://www.lr.dk/kvaeg/informationsserier/ lk-meddelelser/1112.htm. Toussaint Raven, E., Halstra, R.T., Peterse, D.J., 1985. Cattle Foot Care and Claw Trimming. Farming Press, Ipswich, United Kingdom. Warnick, L.D., Janssen, D., Guard, C.L., Gro¨hn, Y.T., 2001. The effect of lameness on milk production in dairy cows. J. Dairy Sci. 84, 1988–1997. Weisstein, E.W., 2006. Kolmogorov–Smirnov Test. From Mathworld. A Wolfram Web Resource. http:// mathworld.wolfram.com/Kolmogorov-SmirnovTest.html. Whay, H.R., Waterman, A.E., Webster, A.J.F., O’Brien, J.K., 1998. The influence of lesion type on the duration of hyperalgesia associated with hindlimb lameness in dairy cattle. Vet. J. 156, 23–29.