Case-control study of papillomatous digital dermatitis in Southern California dairy farms

ELSEVIER

PREVENTIVE VETERINARY MEDICINE Preventive Veterinary Medicine 28 ( 19%) 117- 131

Case-control study of papillomatous digital dlermatitis in southern California dairy farms Alfonso Rodriguez-Lainz a, David W. Hird aV*,Tim E. Carpenter a, Deryck H. Read b aDeportment of Medicine and Epidemiology, School of Veterinary Medicine, Universiry of California, Davis, CA 95616, USA b California Veterinary Diagnostic Laboratory System. School of Veterinary Medicine, University of California, Davis, CA 9.5616, USA

Accepted 2 December 1995

Abstract

Data from 37 southern California dairy farms, with an annual average proportion of > 5% of cows affected by papillomatous digital dermatitis (PDD) (cases), were compared with those from 20 dairy -farms with 5 5% cows affected (controls). Information on dairy environment, management and PDD occurrence was obtained from dairy managers, veterinarians and hooftrimmers, and by direct measurements at the farms. Odds of having a higher proportion (> 5%) of cows affected were about 20 times greater in dairy farms with muddier corrals than in drier dairy farms. Buying replacement heifers was associated with a 4.7-fold increase in the odds of higher PDD prevalence, compared to dairy farms that did not buy heifers. In addition, a positive association was found between risk and number of heifers purchased. Spatial analysis (used to examine distribution patterns of the study dairy farms) showed no evidence of clustering among case or control dairy farms. There was no association between case dairy farms and proximity to the major local river. Keywords:

Papillomatous digital dermatitis; Lameness; Dairy cattle; Case-control;

Dairy cattle diseases

1. Introduction

Papillomatous digital dermatitis (PDD; footwarts) (Read et al., 1992; Read and Walker,

1994a),

* Comxponding

also known

as ‘interdigital

papillomatosis’

(Rebuhn

author.

0167-5877,/96/$15.00 Copyright PI1 SO167-5877(96)01024-O

0 1996 Elsevier Science B.V. All rights reserved.

et al.,

1980)

or

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‘digital dermatitis’ (Cheli and Mortellaro, 1974; Blowey and Sharp, 1988), is an apparently contagious, painful, inflammatory wart-like condition of the skin of the bovine digit of unknown etiology. During recent years, the incidence of PDD has reportedly increased in many countries worldwide (Gourreau et al., 1992). Its economic impact on affected farms can be important, due to the large number of animals frequently affected, and the losses associated with the severe lameness it can cause (Rebuhn et al., 1980; Nutter and Moffit, 1990; Read and Walker, 1994a). PDD lesions are most common on the hind limbs and on the plantar border of the interdigital space adjacent to or involving the heel bulbs (Cheli and Mortellaro, 1974; Blowey and Sharp, 1988; Read and Walker, 1994a). The lesions are associated with minimal or no digital swelling (Blowey and Sharp, 1988; Read et al., 1992). Gross lesions usually appear as demarcated red, raw, granular areas (strawberry-like), often interspersed with yellow, grey or brown papillary proliferations (Cheli and Mortellaro, 1986; Read and Walker, 1994a). The histopathology of PDD lesions has been described (Blowey et al., 1994; Read and Walker, 1994b). Before the late 1970s PDD apparently occurred only sporadically in the United States (Rebuhn et al., 1980; Allenstein, 1992; Read, 1995), but in the past few years its prevalence seems to be increasing in many US states, although few actual data are available (Read, 1995). In California, a recent statewide postal survey (Rodriguez-Lainz et al., 1996) showed that PDD is a widespread disease in California dairy farms especially in the south region (where 75% of 239 responding farms reported the disease, with up to 85% of cows affected on some farms>. In the case-control study reported here, we compared information between dairy farms with a reportedly-high level of PDD occurrence ( > 5% of cows affected per year) (cases), and dairy farms with less disease ( < 5% of cows affected) (controls), in order to describe PDD in those farms and to identify farm-level risk factors for high PDD occurrence (while simultaneously controlling for potential confounding factors). We hoped that further studies of these risk factors might provide a rationale for manipulation, prevention or control of the disease. In addition, we examined the spatial distribution of dairy farms in the study area, and evaluated the hypothesis that case dairy farms were located closer to the major local river (the Santa Ana River). 2. Materials and methods 2.1. Study design Data collection was accomplished between July and September, 1994, on dairy farms located in San Bernardino and Riverside counties, southern California, USA. Preliminary meetings were held with local hooftrimmers to encourage their participation in the project and to ascertain their knowledge of PDD and of foot lesions in general. Four hooftrimmers provided lists of their regular clients (10, 13, 16 and 24 dairy farms, respectively). Information on participating dairy farms was obtained through interviews with managers and hooftrimmers (in person), and with veterinarians (by phone), using standardized questionnaires (available from the authors upon request). Managers were shown color pictures of different stages of PDD lesions during the interview for PDD

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identification. Direct measurements on items of interest were also performed on the farms. All information was collected by the senior author. Mana.gers were asked questions regarding their length of employment at the dairy, herd demographics and milk production, cattle replacement policy, farm installations, corral maintenance, footcare practices, and occurrence and treatment of PDD. Most questions referred to management practices at the time of the survey (1994). However, for some risk factors information was also obtained for the 1990-1994 period, in order to ascertain changes in practices. Partic:ipating veterinarians and hooftrimmers provided information on number of years working at the dairy farms, frequency of visits, and occurrence and treatment of PDD. VSeterinarians were also asked to evaluate footbath management, and to indicate the degree or level of animal health management practices they would change in each client dairy if they were the dairy farm owner and had absolute decision-making power: (1 (would change few practices), 2 (would change a moderate number of practices), to 3 (would change a large number of practices)). Managers, veterinarians, and hooftrimmers were each also asked to score muddiness of both the feedbunk and loafing areas in dairy farms following rains, using a scoring ranging from 1 (stays fairly dry) to 10 (stays muddy long after a rain). The average corral muddiness score for a given dairy was obtained by averaging the six loafing and feedbunk scores for that farm obtained from the three interviewees and then running the six averages. Two final broad categories were defined: dry corrals (average 5 30) and muddy corrals (average > 30) (maximum score = 601, which were used in the analysis. For the spatial analysis, all 57 dairy farms were geocoded using MapInfo software (MapInfo for Windows 3.0, MapInfo Corporation, Troy, New York) and information on either 1993 nine-digit zipcodes (51 dairy farms>, or 1992 (six dairy farms) five-digit zipcodes. 2.2. Definitions of cases and controls Case dairy farms were defined as those with an annual proportion of > 5% of cows reported to be affected by PDD during the study period (January 1993 through August 1994). Control dairy farms were those with an annual proportion of 5 5% of cows affected in the same period. Identical analyses were performed with cases defined as > 10% affected and controls defined as < 10% affected, in order to assess the robustness of the statistical models with regard to the cutoff point for case definition. Hooftrimmers, using their billing records, provided estimates of the number of cows treated for PDD each month in a dairy during 1993 and 1994. Then, for each dairy, the average monthly number of cows treated in that period was calculated, multiplied by 12, and expressed as a percentage of the total number of cows at the farm (as of 7 January 1994), to obtain an estimate of the annual proportion of cows affected. 2.3. Statistical analysis The dairy farm was the unit of analysis in this study. The kappa statistic was calculated to provide an estimate of the agreement between observers, after adjusting for chance, for corral muddiness scores (Fleiss, 1973).

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2.3.1. Logistic regression analysis

Unconditional odds ratios (OR) for dairy farms having a high (> 5%) annual proportion of cows affected by PDD - given exposure to each individual risk factor were tested for statistical significance using logistic regression (Dixon, 1990). Factors showing moderate statistical significance ( P < 0.15) and those considered biologically important were tested in a multivariable logistic model. (Dixon, 1990). Variables expected to be highly associated (i.e. those using different categorization schemes for similar or identical data) were not included in the same model. Forward- and backwardstepping algorithms were used to test the significance of variables in the model, using P-values for entry and removal of 0.25 and 0.60, respectively (to allow for a richer model). Confounding variables were considered those that produced a change on the OR of main factors in the model greater than 10% when they entered or exited the model. All possible two-way interactions between main factors in the model were also tested for statistical significance (Hosmer and Lemeshow, 1989). The final models were selected based on goodness-of-fit criteria and biological plausibility. 2.3.2. Spatial analysis First, the Kth nearest neighbor (NN) procedure (Thompson, 1956) was used to test fo_rclustering of case and control dairy farms separately, by comparing mean distances (d) between the Kth closest points to their respective mean expected distances (E(D)) if points were randomly distributed. The ratio (R) is defined as [ ;i/E(D)]. Values of R > 1 indicate a uniform distribution, R = 1 a random distribution, and R < 1 a clustered distribution. The z-statistic was used to test the null hypothesis of random distribution (R = 1) of the dairy farms. The study area used to calculate the nearest neighbor index was defined as the smallest polygon enclosing the dairy farms being examined. Case and control dairy farms were analyzed up to the 6th nearest neighbor (SPCSTAT, University of California, Davis, CA). If the distribution of case dairy farms were found to be nonrandom, it may be due to the fact that all (case and control) dairy farms, and not just case dairy farms follow this distribution. In such a case, the nonparametric Cuzick-Edwards’ method (Cuzick and Edwards, 1990) should be used to test the null hypothesis of no clustering of case dairy farms. This test examines combined case and control data and is based on the number of cases among the K nearest neighbors for each case, compared with the expected number given the proportion of cases in the sample. For example if there were six case and five control dairy farms, a given case dairy would be compared with the other five case and five control dairy farms. Therefore, on average the probability that a case dairy would have another case dairy as its nearest neighbor is 0.50. For the six case dairy farms, the expected number of nearest neighbors that are also case dairy farms is 3.0, or 6 * 0.5. Calculated values exceeding the expected value would imply clustering of case dairy farms. The upper and lower bounds on the test statistic were obtained up to the 10th nearest neighbor (STAT!, Biomedware, Ann Arbor, MI). The significance of the results was also tested with a z-statistic. Both spatial tests were done separately, first for the subset of 46 dairy farms located closer to the river of interest (San Bernardino), and second for the subset of 11 dairy

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farms located about 40 km from the first subset (San Jacinto). Finally, to evaluate the hypothesis (based on clinical impression) that case dairy farms were located closer to the Santa Ana River than controls, buffers of different distances (up to 12.8 km) were created
3. Results 3.1. Summary of information about practices concerning PDD Of the 63 dairy managers contacted, 57 agreed to participate in the study. Two managers could not be located, and four declined to take part in the study. Thirty-seven dairy fams (65%) were classified as cases, and 20 (35%) as controls. At the time of the study, only two dairy farms had not been affected at all by PDD. Herds were housed outdoor on dry lot dirt corrals. Most cows (99.6%) were Holstein-Friesian, and the rest were Jersey or Brown Swiss. Cows were separated into pens by milk production level and/or stage of lactation. All dairy farms had a herringbone milking parlor and used a wash pen with impulse sprinklers to wash cows before milking. Hooftrimmers visited the study dairy farms at least once a month (51 dairy farms) or every 2 months (six dairy farms), and trimmed from 50 to 100 cows per day. Based on

35 -

33 --

25 --

0

5

10

:nnua;bo

P&&?d

COG

40

45

a50

Fig. 1. Frequency distribution of the annual proportion of cows affected by papillomatous digital dermatitis (PDD) among 57 dairy farms in a case-control study of PDD in 57 southern California dairy herds, 1993-1994.

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45

40

35

30 e 0

25

@ z

20

s 15

10

5 -~

11

+

OJ 1907

1988

1989

1990

1991

Year

1992

1993

1994

Fig. 2. Proportional distribution of year of first observation of papillomatous digital dermatitis (PDD) by different interviewees in 57 southern California dairy herds, 1994.

their estimates, the overall mean annual proportion of cows affected by PDD on the dairy farms during the study period (January 1993-August 1994) was 15% (SE = 1.89) with a median of 11.4%, and a range of 0 to 75% (Fig. 1). Since 1993, all hooftrimmers have used only topical oxytetracycline and bandaging (in 48 dairy farms), or topical formaldehyde (in nine dairy farms> to treat PDD, but they also reported trying different treatments in previous years. Only seven managers kept records of PDD cases. The first manager observation of PDD on a study farm occurred in 1987. Most managers, veterinarians and hooftrimmers reported seeing PDD for the first time on study dairy farms during 1991 to 1994 (Fig. 2). Thirty-one managers (54%) did not have an opinion as to how PDD had entered their farms, 16 (28%) believed the disease was introduced by purchasing infected heifers, and ten (18%) indicated different causes (e.g. hooftrimmers, other dairy personnel, cattle trucks). When asked which age group was first affected by PDD, 27 (47%) managers indicated first-calf heifers, 14 (25%) mentioned second lactation and older cows, six managers (Ii%), believed all age groups, from first lactation to older cows, two (4%) responded that 18-month old heifers were initially affected, and eight (14%) did not know. However, when asked which groups have been most affected by PDD during the previous 12 months, 26 managers (46%) indicated all age categories, from first lactation to older cows, 16 (28%) responded second lactation and older cows. Only eight (14%) considered first-calf heifers as the most affected, and seven (12%) did not know. Scores on overall corral muddiness in dairy farms, given by managers, hooftrimmers and veterinarians showed moderate agreement (kappa = 0.56).

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In 31 (54%) dairy farms, other personnel, in addition to the hooftrimmer, were also currently treating individual PDD cases, mostly in the milking parlor. Products used were topical oxytetracycline (15 dairy farms); parenteral antibiotics (i.e. penicillin, lincomycin, ceftiofur) (seven dairy farms); and a variety of other products (e.g. formaldehyde spray, iodine, muriatic acid) (nine dairy farms). Twenty-eight of those 31 dairy farms also reported having tried different treatments since 1990. Thirty-nine of 57 dairy farms reported not to have changed heifer raising policies since 1990. Fifteen of the 36 dairy farms that purchased heifers first did so during 1990-1994. No dairy reported buying calves. Twelve of the 16 veterinarians working on the study dairy farms were available for interview. They visited the study farms one to four times a month. In general, veterinarians could not provide useful information on prevalence of PDD on the dairy farms, or about adequate footbath management, because they were mainly responsible for aspects of animal health other than foot care. 3.2. Logistic regressions Dairy farms with muddy corrals, buying heifers (especially those not born in California) and buying heifers at saleyards were more likely to be high PDD-affected dairy farms in the unconditional analyses (Table 1). Dairy farms sending heifers to a custom ranch and those raising them on the farm were both less likely to be highly affected herds than dairy farms that purchased heifers. In the multivariable logistic regressions (Table 21, corral muddiness score and heifer buying policy were the most important risk factors for higher PDD levels in dairy farms. Dairy farms classified as having muddier corrals were about 20 times more likely to have higher PDD prevalence than drier dairy farms. Because several variables related to heifer-buying practices had been constructed, the two most significant (i.e. buying vs. not buying, and number of heifers bought in 1993) were fit into separate models. In the first model, dairy farms that bought replacement heifers since 1990 were about six times more likely to be highly affected than those that did not buy heifers. The second model incorporated the number of heifers bought during 1993 and showed a dose effect. In both models, dairy farms where cows walked longer distances to the milking parlor had about two times higher odds of being a highly-affected herd than those in which cows walked less. Number of milking cows was kept in the models to control for confounding. No two-way interactions were statistically significant in either model. When the multivariable logistic regressions were repeated using a 10% prevalence as the cut-off point between cases and controls, the same risk factors were associated with a higher level of PDD in dairy farms. 3.3. Spatial analysis Fig. 3 shows the distribution of case and control dairy farms, and the location of the Santa Ana River. In the Km-nearest-neighbor analysis, all R ratios for both subsets of dairy farms suggested a tendency for uniform (highly dispersed) distribution of case and

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Table 1 Risk factors for dairy farms with high level ( > 5% of cows affected per year, cases) of papillomatous digital dermatitis (PDD), compared with lower level dairy farms (I 5%, controls), in 57 southern California dairy herds, 1993- 1994 Risk factor

Categories

Case(%) (n = 37)

Control(%) (n=20)

No. milking cows m

350-900 901-2100 6818-9545 > 9545 4-15 16-80 onfarmc Custom d 76 Don’t buy

51 49 38 62 16 84 5 19 40 24 76 32 14 54 32 14 54 32 57 11 57 43 89 11 60 40 27 73 27 22 51 27 35 38 27 57 16 79 21 87 13 54 46 50 50 43 57

50 50 40 60 25 75 10 50

Herd milk production (kg cow - ’ year- ‘1 Age of dairy b

a.m

(years) Heifer raising policy since 1990 m Buy ’ Heifer buying policy since 1990 m.” No. heifers bought in 1993 m.” Birthplace of heifers bought in 1993 m.n Heifer buying source in 1993 Heifer replacement rate in 1993 (o/o) Buy adult cows since 1990 Buy bulls since 1990 Use of footbath since 1990 Time using a footbath since 1990 (months) Footbath content

Frequency of footbath use Depth of footbath: solution (cm) Cows selection for hooftrimming m* of corral per milking cow m of feedbunk per milking cow Farthest walking (m) im

Buy 0 l-60 >60 Don’t buy California Other states Don’t buy Saleyard Other ’ O-30 > 30 No Yes No Yes No Yes No use l-14 > 14 No use Copper sulphate Other products No use Every day Sporadically s O-7.6 > 7.6 Only lame cows Healthy cows h 90-150 151-230 0.40-0.70 0.71-1.12 15-457 458-1070

60 40 65 10 25 60 15 25 60 25 15 65 35 80 20 65 35 45 55 45 20 35 45 20 35 45 25 30 82 18 85 15 55 45 55 45 55 45

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Table 1 (continued) Risk factor

Categories

Case(%) (n= 37)

Control(%) (n=20)

Distance to nearest dary PDD treatment personnel Average corral muddiness m.” Animal health management score ‘.m.”

Fenceline j Farther Hooftrimmer Other k Dry Muddy

16 84 46 54 24 76 45 55

30 70 45 55 75 25 77 23

1 2

a Current (1993) rolling herd average (kg cow- ’ year- ’ ). b No. of years there has been a dairy at the same location.’ All heifers born and raised on the premises.d Heifers sent to another location to be raised? Dairy bought heifers.f e.g. a cattle dealer or a heifer ranch. s Periods of time when footbath is not usedh Hooftrimming of cows when they dried up or freshed up, in addition to lame c0ws.I Distance from farthest corral gate to milking parlor, multiplied by no. of times cows are milked each day.j Dairy farms sharing a common fenceline.k Other dairy personnel also treats individual PDD cases.’ Proportion of animal health management practices the veterinarian would change in a dairy: 1 (small), 2 (moderate), 3 (large number of practices).‘” Selected as candidate variable for logistic regression models because of biological importance.” ’ < 0.15: selected as candidate variable for logistic regression models.

control dairy farms, which was statistically significant after the first nearest neighbor (P < 0.05) (Table 3). The Cuzick and Edwards’ test results indicated absence of clustering at any of the Table 2 Two logistic regression models for high annual prevalence ( > 5%) of papillomatous case-control study, in 57 southern California dairy herds, 1993- 1994 Risk facto] Model 1: Heifer buying policy since 1990 Average corral muddiness Farthest walking distance (A) No. milking cows

Model 2: No. heifers bought in 1993 Average corral muddiness Farthest walking distance (A) No. milking cows

See Table

I for key.

digital dermatitis

Categories

OR

95% CI(OR)

Don’t buy

1.oo 5.76

1.32-25.1

Buy Dry Muddy 15-457 458- 1070 350-900 901-2100

0 I-60 61 or more Dry Muddy G-457 458- 1070 350-900 901-2100

1.oo 19.2 1.00 2.23 1.00 2.84

1.00 3.01 6.49 1.00 22.4 1.00 2.07 1.00 2.99

3.13-l

18.0

0.44-I

1.3

0.42- 19.4

0.27-33.5

1.30-32.3 3.48-144.0 0.41-10s 0.42-21.1

in a

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SAN BERNARDINO COUNN

San Jacinto *

. l l

RIVERSIDE COUNN

.

*1 *

l

10 miles

t

I J

Fig. 3. Map showing location of dairy farms and the Santa Ana river in a case-control study of papillomatous digital dermatitis in 57 southern California dairy farms, 1994. (*: cases, n : controls).

levels of nearest neighbor examined. Similar nonsignificant P-values were obtained when all dairy farms were examined (Simes P = 0.60), as when the two subsets of dairy farms were analyzed separately (Simes P = 0.55for San Bernardino, and P = 0.59 for San Jacinto).

Table 3 Results of the Kth nearest neighbor test for a case-control southern California dairy farms, 1993-1994 Nearest neighbor

1

San Bernardino (n = 46) Cases ( n = 29) Ra b controls (n = 17)

0.23

1.22 3.32

R knJacinto(n=

1.21 1.69

Cases (n = 8) R controls (n = 3)

R Z

11)

1.02

study of papillomatous

3

2

4

digital dermatitis 5

6

1.19 3.45

1.14 3.08

1.12 2.84

1.12 3.04

8.56

1.84 11.7

1.75 12.2

1.81 14.9

1.82 16.5

1.28 1.64

2.64 12.0

2.73 15.6

3.06 1.69

2.79 8.56

3.91 11.7

1.75

a R < 1 indicates clustering of points; R = 1 indicates a random uniformly dispersAb Standard variate of the normal curve.

distribution;

and R > 1 suggests

in 57

points

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70 -is

60

F := .!!

w--

E 0

40.-

30 --

20 --

10

O-

i

0.0

4

24

3.2

4.0

5.6

Distance (kms.)

I

7.2

0.6

12.6

Fig. 4. Cumulative percentage distributions of case and control dairy farms\ by their distance (in miles) from the Santa ha river, in a case-control study of papillomatous digital dermatttA s m 57 southern California dairy farms, 1994.c A : cases, n : controls).

When the cumulative proportions of case and control dairy farms were compared at different buffer distances from the Santa Ana River, their distributions were not different (P = 0.95); contrary to our initial hypothesis, case dairy farms were not located closer to the Santa Ana River (Fig. 4).

4. Discussion The cut-off point of 5% of cows affected was selected to divide dairy farms into case and control categories after examination of Fig. 1 and because that was the within-herd median percentage of cows affected in dairy farms on the California state survey (Rodriguez-Lainz et al., 1996). We emphasize that dairy farms for this study were not randomly selected - the results can be strictly applied only to these dairy farms. However, study dairy farms were similar to most dairy farms in the area in terms of herd size, breed, milk production, and type of housing. Also, about 90% (of 354) of southern California dairy farms were visited by a hooftrimmer during 1993 (Rodriguez-Lainz et al., 1996). The value of information obtained from professional hooftrimmers in lameness studies has been previously reported (Enevoldsen et al., 1991). In our case, we considered hooftrimmers the most reliable source of information on levels of PDD on the farms because they regularly treated most foot lesions, demonstrated ample clinical knowledge of PDD and other cattle foot conditions and, since 1993, had been keeping

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records of the number of cows treated for PDD for billing purposes. In contrast, local veterinarians were not usually responsible for individual cattle foot care, and managers have been reported to underestimate the number of cows lame or with PDD lesions on their dairy farms (Wells et al., 1993; Frankena et al., 1991). However, hooftrimmers’ prevalence estimates did not take into account repeated treatments of the same animal (animal identification numbers were not recorded); hooftrimmers did not review all animals on client farms, only those that were presented for trimming; and prevalence estimates were not confirmed by independent methods. Therefore, prevalence estimates were not used as quantitative data, but instead dichotomized as the dependent variable in our analysis. The percentage of dairy farms affected by PDD in our study (97%) was similar to Read’s estimates for the same area (Read and Walker, 1994a), but larger than managers’ estimates obtained in the state survey (75%) (Rodriguez-Lainz et al., 1996). The latter was expected because (as we mentioned earlier) managers may not be aware of the existence of specific foot conditions in their dairy farms. The annual proportion of cows affected by PDD on the study dairy farms showed a wide range. Reported prevalences of the disease in dairy farms in other countries also varied widely: from 12 to 80% (Rebuhn et al., 1980; Nutter and Moffit (1990). In The Netherlands (Frankena et al., 1990, most herds studied had less than 15% of cows affected, with a maximum of 58%. In our study, the variable most consistantly associated with higher PDD levels in dairy farms was the average muddiness of dirt corrals. In general, ‘dry-lot’ corrals are difficult to keep dry and free of wet manure. Even during summer (when temperatures are very high) the areas most used by cows (shaded areas, feed-bunk aprons) can remain very wet. Poor foot hygiene and continually- wet conditions (e.g. cows standing in slurry) have been suggested as important predisposing factors for PDD and other infectious digital diseases (Greenough et al., 1981; Cheli and Mortellaro, 1986; Blowey and Sharp, 1988; Frankena et al., 1993). In such an environment, the digital horn tends to soften and becomes more susceptible to abrasion and invasion by microorganisms (Greenough et al., 1981). Also, as Read et al. (1992) indicated, PDD in cattle histologically resembles yaws in humans; yaws is a skin disease of the lower extremities that it is favored by poor hygiene and hot and humid conditions where the skin is constantly moist (Manson-Bahr and Beel, 1987). However, other authors have also reported PDD outbreaks when in-house hygiene was excellent (Basset et al., 1990) or even in cattle at pasture (Gourreau et al., 19921, suggesting other factors might be important for the outbreak of the disease. The degree of muddiness of dry-lot corrals may depend on different factors: corral characteristics (size, drainage system, soil type>, cleaning management, stocking density, and local weather, among others. In our survey, we included questions relating to corral-cleaning management, but cleaning frequency and methods varied greatly among dairy farms - and even within a dairy, depending on the areas of the corrals (e.g. feedbunk aprons vs. loafing areas), and time of the year (rainy vs. dry season). Frequently, managers’ responses indicated intentions more than actual practices. They also reported differences in levels of muddiness among corrals. For the above reasons, information on cleaning management was considered too complex and unreliable to be

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used in the analysis. Instead, the average muddiness scores for corrals obtained from all different interviewees were used to broadly categorize dairy farms into those with muddier or drier corrals. Those average scores represented an overall evaluation that included all the above-mentioned individual factors that influence corral muddiness. Future research on those factors and their association with occurrence of PDD in dairy farms would be useful. Although high animal corral density has been considered to predispose to higher levels of infectious foot diseases including PDD in cattle (Blowey, 1994) - and might cause muddier corrals - we did not find any association of this variable with higher PDD levels. One possible explanation is that in dry-lot corrals, animals tend to spend most time concentrated in certain areas (e.g. feedbunk aprons, around a water trough, or under a shade). Dairy farms that purchased replacement heifers or that purchased large numbers in 1993 were more likely to be more affected by PDD. Previous reports suggested that PDD is first introduced on dairy farms through the entry of infected replacement heifers (Nutter and Moffit, 1990; Weaver, 1992). Although most dairy farms had the same heifer-replacement policy since 1990, practices might have differred in previous years. The number and origin of purchased heifers were obtained only for 1993 because of the difficulty in obtaining precise information for previous years. Use of a footbath was positively associated with high PDD prevalence in the uncondil:ional log odds analysis, but causal interpretation of this variable is not possible in this retrospective study. During dairy farm visits, almost all footbaths did not appear to be properly managed, i.e. it was uncommon to find a footbath in which the solution was changed at appropriate intervals; they were often full of manure. Therefore, it could be reasoned that the positive association of footbaths with PDD prevalence indeed may have been causal. However, it could also be argued that farms with a greater history of foot problems (PDD or other problems) were more likely to have constructed a footbath. In this case the association is not causal; the footbath was constructed as a treatment for PDD or another foot problem. Levels of different nutrients in the diet have been considered potential risk factors for PDD occurrence: deficits in zinc or manganese (Cheli and Mortellaro, 1986), and excessive protein intake (Bargai, 1994). Others may also be of importance. We also interviewed dairy nutritionists, but accurate relevant diet information could not be obtained retrospectively. The spatial analyses in this study evaluated the existence of clustering among study dairy farms and the potential for confounding due to dairy location. Case and control dairy farms were each significantly uniformly dispersed after the first nearest neighbor. Although the first nearest neighbors were more dispersed (R > 1) than expected, these results were not statistically significant and should be viewed as a lack of power of the test resulting from a small sample size rather than a practice of random location of the 1st nearest neighbors. Results of the Kth-nearest-neighbor test and their interpretation depend greatly on the size of the study area. Clustering is likely to be found if larger areas are used (Clark and Evans, 1’?54), such as our entire study area, and this is why the two subsets of dairy farms were analyzed separately. Because dairy farms were found not to be randomly distributed, the nearest neighbor

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test could not be correctly applied to the case data. The Cuzick and Edwards’ test is considered more appropriate for case-control studies, and (in contrast to the nearest neighbor test) does not require random distribution of the points and does not take area into consideration (Cuzick and Edwards, 1990; Jacquez, 1994). The hypothesis that affected dairy farms were more likely to be located closer to the river was based on clinical impressions from local veterinarians, and the belief that those dairy farms were in general older, with smaller corrals and less-adequate drainage. Our spatial results did not indicate any significant clustering of case dairy farms. Based on our results, one important factor for PDD control is to maintain corrals as dry and clean as possible. Also, purchase of heifers should be carefully considered in regard for disease potential. PDD has become a major cause of lameness in dairy cattle in California. Data are needed on PPD’s financial impact in affected dairy farms, so that benefits and costs of preventive and control measures can be adequately evaluated.

Acknowledgements

We are grateful to the southern California hooftrimmers, managers and veterinarians who participated in the study, and to the veterinarians of the California Department of Food and Agriculture for their collaboration in this project. We also thank Jim Reynolds, Rick Gutierrez and Richard Walker for their contributions to design of the study and questionnaire. This work was supported by grants from the California Dairy Research Foundation, and the Livestock Disease Research Laboratory of the School of Veterinary Medicine.

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