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Sole Ulcers in Dairy Cattle: Associations with Season,

Cow Characteristics, Disease, and Production


C. ENEVOLDSEN and Y. 1. GROHN
Section of Epidemiology
Department of Clinical Sciences
New York State College of Veterinary Medicine
Cornell University
Ithaca, NY 14853

1. THYSEN
National Institute of Animal Science
PO Box 39
DK-8830 mle, Denmark

ABSTRACT (Key words: epidemiology, lameness,


Epidemiological associations, ex- dairy cattle)
pressed as odds ratios between variables Abbreviation key: CI = confidence interval,
obtained from dairy cow records and sole DIM = days in milk, MF = more than one foot,
ulcer occurrence at claw trimmings were OR = odds ratio, SF = single foot.
estimated with logistic regression analysis
on data from 2204 and 1124 cows in INTRODUCTION
lactation 1 and lactations 2 to 9, respec-
tively. Sole ulcer in one foot or more than Sole ulcer (pododermatitis circumscripta) of
one foot occurred in 20.0 and 29.7% of varying severity occurs in 10 to 80% of lacta-
cows in lactation 1 and in 23.5 and 24.7% tions in Friesian type cattle (2, 14, 16, 27).
of cows in lactations 2 to 9. The analysis Although sole ulcers must cause considerable
revealed several complicated interactions. pain and discomfor&,only a small proportion of
Trimming or calving in summer to fall cows are treated for “claw disorders” by veteri-
was strongly associated with sole ulcer. narians in each lactation (19,20). Because claw
Trimming later than 1 to 2 mo after calv- disorders obviously are not recognized in herds,
ing was positively associated with sole the cows may suffer from pain and discomfort
ulcer depending on milk yield, body for a considerable period of time and probably
weight, or season of calving. If lactation have reduced productivity. The literature men-
1 cows were treated for disease (limb, tions the following risk factors: claw over-
metabolic, digestive, or severe reproduc- growth, interdigital dermatitis, acute systemic
tive disorders), sole ulcer in more than disease, “stress” associated with calving, m e n
one foot occurred earlier in lactation. acidosis, endotoxins, histamine, insufficient
Milk yield in early lactation and body supply of minerals and amino acids (cystine,
weight were positively associated with methionine), burdening (softness of bedding),
ratio of roughage to concentrate, excess protein
sole ulcer. Heel erosion was associated
supply, milk yield, body weight, structure of
with sole ulcer depending on season of
leg bones, size of claws, parity, time of year,
trimmjng and parity. Presence of sole ul-
and lack of exercise. The heritability of sole
cer but not heel erosion in a lactation ulcer is between .10 and .30,and Friesian cows
increased the risk of sole ulcer in the seem to be most susceptible (6, 12, 15, 16, 17,
subsequent lactation. The interval be- 28, 29). Presently, most workers regard sole
tween trimmings appeared to be impor- ulcers as one manifestation of the multifactorial
tant. metabolic disease laminitis (pododermatitis
aseptica diffusa).
Continuous measurement of disease inci-
Received January 8, 1990. dence and prevalence is essential to determine
Accepted August 30, 1990. efficiently the importance of such an endemic
1991 I Dairy Sci 741284-1298 1284
EPIDEMIOLOGY OF SOLE ULCERS 1285

disease in a herd, and subsequently, to select Animals were fed a feed ration of 5 kg DM of
the best and most efficient control strategies. folder beets, molasses, or beet pulp, approxi-
Knowledge about the cow’s health status is also mately 7 kg DM of silage or hay fed for ad
valuable when deciding which animals should libitum access, and 5 kg DM of concentrate.
receive special attention or the highest culling The flat rate feeding principle was applied in
priority. An inexpensive convenient source of all herds. All treatments requiring injections or
information is recordings made by professional use of antibiotics were performed by local prac-
claw trimmers or farm workers during the mu- ticing veterinarians who recorded all treat-
tine trimmings. The value of such data has been ments. Recordings were verified by the techni-
recognized (5). cians.
Efficient utilization of such routinely col- The claw health of each cow was recorded at
lected data requires consideration of all the least twice in each lactation at the time of claw
information about factors that influence the dis- trimming, which took place 4 times per year in
ease risk of the animals. Season of year, stage each herd. All claws of all cows were systemat-
of lactation, season of calving, parity, body ically trimmed during the first 3 to 4 mo of
weight, milk yield, and health status (both in lactation and again 6 mo later. Some cows
general and with respect to claw health) are required claw trimming more frequently. The
potential risk factors for sole ulcer which are or same technician performed all trimmings and
could be available. recordings of claw health from the start of the
The purpose of this study was to estimate study until April 1, 1979. Thereafter, trimming
the direction and magnitude of the epidemio- was performed by a local professional claw
logical associations between the potentially trimmer, and claw health was recorded by one
available information about possible risk fac- staff member at the Institute. At each trimming,
tors and recordings of sole ulcers in dairy cows. a detailed evaluation of the digits was made.
Such estimates should be useful for problem The condition of the central part of each of the
solving and monitoring the herd and for making claw soles was categorized as follows (21):
decisions about individual animals. degree 1 = a yellow spot, degree 2 = light
hemorrhages occurring in stripes, degree 3 =
MATERIALS AND METHODS confluent hemorrhage, degree 4 = dark spot,
and degree 5 = exposed pododerm.
The heel region of each foot was similarly
Data
examined for heel erosion (erosio ungulae). The
Data were from 23 Danish herds (average following categories (22) were recorded: degree
number of cows = 82; SD = 25) composed of 1 = superficial scattered erosions in the sole-
Danish Black and White cows, which are some- bulb junction, degree 2 = confluent erosions in
what comparable with Holstein Friesians. Data the sole-bulb junction, degree 3 = erosions
were collected from 1978 to early 1982 to forming a distinct grove in the sole-bulb junc-
investigate the effect of dairy cow housing tion, and d e p 4 = as in degree 3 with podo-
systems on health, reproduction, production, derm also exposed.
and economics. Seven herds were kept in dif- AU data were storsd in the database at the
ferent types of tie stalls, and the rest were kept Danish Institute of Animal Science after correc-
in loose housing systems with either a solid or tion of recording and coding errors revealed by
slated floor. Eight herds were fed pasture one built-in logical checks in the computer pro-
or more summer seasons during the study. grams.
Housing and management systems are
descrikd in detail elsewhere (27). statistical Analysis
Technicians from the National Institute of
Animal Science visited all herds weekly and The data were analyzed with a multivariate
were responsible for recording milk yield, body logistic regression technique (8). The epidemio-
weight at calving (actual weight at first calving logic measure of interest provided by logistic
and heart girth measurement at the subsequent regression is the odds ratio (OR).An odd is
calvings), body weight in spring and fall and at defined as the probability of an event or state
culling, and dates of calvings and cullings. (in this case sole ulcer) occurring (p) divided
Joarnal of Dairy Science Vol. 74, No. 4, 1991
1286 ENEVOLDSEN ET AL.

by 1 - p. The ratio between odds, calculated for sevem-those diseases considered as risk fac-
individuals “exposed” to a hypothesized risk tors for claw disorders (summer mastitis, left
factor (e&, high BW) and those not exposed displaced abomasum, intestinal atony, peritoni-
(low BW), provides an estimate of the ratio tis, and severe metritis); 2) Limb-limb disor-
between the prevalences in the exposed and the ders of which the vast majority of diagnoses
nonexposed populations, i.e., the relative effect were interdigital phlegmon and periarthritis of
of the exposure. Odds ratios provided by mul- the hock (the specific diagnosis sole ulcer was
tiple logistic regression (the antilogarithm of excluded from the data set); 3) other-those
the coefficient for an independent variable) are diseases not expected to be important risk fac-
conditional upon all other variables in the mod- tors (e.g., other mastitis, retained placenta, and
el. If a 95% confidence interval (CI)includes mild metritis).
1.0, the corresponding OR is statistically non- A cow was categorized as having experi-
significant at 5%. The statistical analysis was enced one of these three classes of disease if at
performed in four stages: 1) data editing, 2) least one treatment for a given disease was
data reduction, 3) model selection, and 4) es- performed between 21 d before calving and the
timation of effect (18). day of claw trimming. To analyze the effect
of several diseases in combination, the follow-
Data Edltlng ing categories were created: 1) disease occur-
ring in isolation-severe, limb, and other;
Because the available data were not col- 2) two disease groups occurring-severe
lected for the specific purpose of estimating plus limb, severe plus other, and limb plus
associations to sole ulcer occurrence, the vari- other; and 3) all three disease groups occurring
ables were edited examining the data and using simultaneously-severe plus limb plus other.
infonnation from the literature. Three mutually The variables herd and year of calving were
exclusive classes of sole ulcers were created: 1) combined into one variable (herd-year of cdv-
cows with no clinical signs, 2) cows with signs ing) that indicated the calving year and the herd
in one or both claws of a single foot only, and identity. Calving year was from November 1 to
3) cows with signs in more than one foot. In October 31. The data set contained only 239
addition, cows with sole ulcers were assigned a observations during the fourth to ninth parity.
score equal to the highest degree of sole ulcer Consequently, these data were combined leav-
recorded in any claw. Because of the small ing the variable parity with four classes.
number of observations in degrees 1 and 5 , they
were combined with degrees 2 and 4. respec- Data Reduction
tively.
All independent variables were analyzed as The model to explain sole ulcer was deve-
categorical variables. For instance, the variable loped using SAS Logist (8). The Logist proce-
FCM (4%, kg) at the first test day was catego- dure fits the logistic multiple regression model
rized into seven classes with approximately to a binary dependent variable or to an ordinal
equal numbers of observations. The classes dependent variable using the maximum likeli-
with less than approximately 5% of the obser- hood method. The sole ulcer was handled as an
vations were avoided when possible and ordinal dependent variable. For the ordinal
reasonable. For example, the variable season of model, the basic assumption is that the cause of
calving, was categorized into 2-mo intervals the increase in score value of a dependent
starting January 1. Variables heel erosion at variable (e&, from 1 to 2) is an extension of
present trimming and heel erosion at previous what causes it to increase from 0 to 1. This
trimming were assigned a score indicating assumption was checked by examining the
degree of heel erosion recorded for the digit graphs of the logit cumulative probability
with the highest degree of sole ulcer. If no sole curves to see if they were parael (7).
ulcer was observed, the heel erosion status of With sole ulcer as the dependent variable, all
the left hind foot was assigned. the categorized independent variables were! ana-
The variable disease included only animals lyzed with Roc Logist (step l). No interactions
subjected to veterinary treatments. The follow- (product terms) were included in this initial
ing three classes were created initially: 1) analysis. The effects of different categories
Journal of Dairy Science Vol. 74, No. 4, 1991
EmDEMIOLOGY OF SOLE u u = E R S 1287
(parameter estimates) were then examined bined milk yield-BW variable. For instance, if
graphically and a l l variables except herd-year the final model included the terms, A, B, and A
of calving were separated into high and low x B (A and B both dichotomized into high and
categories based on two criteria: 1) if two low, and the times sign indicating interaction
distinctly Merent groups or some “dose-re- between A and B), a model with the terms high
sponse-like” relationship occurred, then the A plus high B, high A plus low B, and low A
point that best separated the two groups was plus high B (codedas indicator terms) provides
selected as cutoff point, and 2) if no trend was estimates of the effects of these terms relative
obvious two groups of approximately equal size to low A plus low B. If the initial multiple
were formed. logistic regression analysis had revealed a clear
Variables BW at calving and milk yield are trend in the categories of a variable, or showed
strongly associated. Such strong association that the variable was ordinal, effects were esti-
may negate the effects of closely related vari- mated for all these Categories (indicator terms)
ables resulting in biased conclusions because of to provide a maximum amount of information
collinearity problem. For this reason and to about the relationship.
reduce the number of independent variables,
milk yield (4% FCM,kg) at the first test day in RESULTS AND DISCUSSION
a lactation and BW (kg) after calving were
combined to one variable in the following way: If the condition of the claws is to be re-
milk yield (FCM) and BW were both separated corded routinely and yet be objectively inter-
into high and low categories, and these categor- preted, recordings must be simple, quick to
ies were combined into the four possible com- perform, and have a high degree of repeatabil-
binations high FCM plus high BW, high FCM ity. The proposed classification was an attempt
plus low BW, etc. to fulfill these demands and has the following
These newly created variables were then an- advantages: 1) many different recordings in
alyzed (step 2) and excluded from further anal- eight claws can be combined logically for use
ysis if 1) no trends in the parameter estimates in quantitative analysis, and 2) the classifica-
in the first analysis (step 1) were evident, and tion can be compared with classifications in
2) the probability of the chi-square values of other studies. In the most frequently used
the parameter estimates in the second analysis methods of total lesion scores, the same score
were above 25%. In the fmst and second step of may represent one cow with one claw severely
the regression analysis, the variable herd-year affected or one cow with several claws mildly
of calving was included in the model. affected.
Cows with sole ulcer in one foot (SF), and
Model Selecllon
those with sole ulcer in more than one foot
(MF) were analyzed separately, i.e., they were
The remaining variables were then analyzed both compared with cows without sole ulcer.
with interaction terms (all two-way product The purpose of this separation was to utilize the
terms) included in the model (step 3). The herd- information about the degree of sole ulcer
year of calving variable was not included in within each of the classes, SF and MF, and to
any interaction terms. product and lower order simplify the interpretation of effect estimates.
terms were removed from the model until the Drawbacks of this separation are 1) a decreased
difference in values of -2 log (likelihood) of precision of the estimates and consequently
the models at the corresponding degrees of lower power of the tests (because of the
freedom were statistically significant at 10% reduced sample size), and 2) the estimates from
(likelihood ratio test). the two models cannot be directly compared
(because they are not conditional on each oth-
Effect Estlrnatlon er).
Calving, particularly the first one, is
To provide epidemiologically interpretable regarded as very important in the etiology of
effect estimates for the interaction terms, com- sole ulcer (1, 16). Cows in first lactation expe-
bined variables were created by forming indica- rience conditions before and near calving that
tor variables as described above for the com- differ markedly from conditions experienced by
Journal of Dairy Science Vol. 74, No. 4, 1991
1288 ENEVOLDSEN ET AL.

older cows. These two groups were, therefore, erosion, disease, season of trimming x disease,
and stage of lactation x FCM-BW (T.able 1).
analyzed separately. In the present analysis, SF
and MF occurred in 20.0 and 29.7% of cows in The term season of trimming x horn erosion
lactation 1 and in 23.5 and 24.7% of lactationswas the last term to be removed at probability
2 to 9, respectively. Approximately half the of .05 to .lo.
cows were aEfected by some degree of sole The term disease included the classes limb,
ulcer. limb plus severe, limb plus other, and severe
Nearly half the sole ulcer cases were SF. plus limb plus other. Because treatment for
Most reviews state that sole ulcer and lamhitislimb disorder was a component in all disease
apparently occur in several feet. However, the classes, it appears to be the most important
usual method of total lesion scores provides factor. Odds ratios estimated for disease ranged
little information about actual distribution offrom 1.7 to 7.8 depending on season of trim-
lesions found. Sole ulcer in one foot could be ming (interaction). Cows without disease had a
an early stage of MF, but because the median 1.5 times higher risk of SF if they were
number of days from calving to trimming trimmed in May to August. These cows may
among SF and MF were 63 and 66 in lactation have stepped on stones in the pasture or on the
1 and 74 and 84 in lactations 2 to 9, that
explanation seems unlikely. Furthermore, s e way to the pasture. Such traumatic sole ulcers
vere cases of SF were common. are likely to occur in one foot only. Williams et
al. (30) studied the effects of wet weather on
lameness and found significant but small ef-
Sole Ulcer in One Foot In Flrst Lactatlon
fects. Another possible explanation is that this
The fmal model of SF in the first lactation group of cows, which was trimmed early in
included the terms season of aimming, season lactation, was kept in stables during the entire
of calving, stage of lactation, FCM-BW, horn pregnancy and consequently had a higher risk

TABLE 1. Final logistic regression model of sole ulcer in one foot only (SF)in lactation 1. Sole ulcer of degrees 1to 2, 3,
and 4 to 5 occamd among 13.5, 102, and 4.8% of the 1550 cows.
Pacentage Odds 95%
Description of variable~l of n Illti0 CI
~ o n t hof trimming and disease*
Trimming M a y to Aug, no disease 19.8 15 1.1 to 2.0
'Iirimmiag Sep to Apr, disease 3.6 1.7 1.0 to 3.0
Trimming Sep to Apr, no dissase 75.7 1.o ...
Month of calving
May to Jun or Sep to Oct 33.3 1.4 1.1 to 1.8
Other months 67.7 1.o ...
Stage of lactation and pcM-BW3
Trimmiog 227 d in milk and
FCM 219.6 kg and B W 2490 kg (High FCM + High BW) 16.1 12.2 5.0 to 30
FCM 4 9 . 6 kg m BW <490 kg 55.4 8.7 3.6 to 21
Trimming Q 7 d in milk and
FCM 219.6 kg end B W 2490 kg (High EacM + J3igh BW) 6.0 1.o ...
FCM 4 9 . 6 kg or B W <490 kg 22.5 3.0 1 2 to 7.5
Heel erosion at f-j
Degrees 2 to 4 6.5 25 1.6 to 3.9
1 155 1.8 1.3 to 2.5
No heel erosion 78.0 1.o ...
'In addition, herd-year of calving is included in the model. Th+ combination himming M a y to Aug and disease was
omit&eddue to imprecision.
'Includes limb disorder alone (limb) or in combination with other distases (severe plus limb, limb plus other, severe
plus limb plus other). See text.
%CM = 4% at first test day after calving, B W = body weight after calving, U = confidence interval.

Journal of Dairy Science Vol. 74, No. 4, 1991


EPIDEMIOLOGY OF SOLE UL€E!RS 1289
of having claws exposed to manure, which revealed that the OR increased almost exponen-
softens the claw horn. Using a different classifi- tially until approximately 4 mo after calving
cation of claw disorders, Thysen et al. (24) [120 d in milk (DIM)], and after that a marked
studied the effect of the grazing areas (wet or decline was clear. A spontanwus cure of some
dry) and type of housing during pregnancy in of the sole lesions probably was responsible for
heifers but found no significant differences. the decrease in prevalence after approximately
Feeding is also frequently mentioned as an 90 to 120 DIM. A similar pattern is reported in
important factor for claw health. However, the almost a l l studies.
results of several investigations are inconclu- Body weight and milk yield have been
sive (3, 23), although feeding high amounts of postulated as risk factors for sole ulcers. Be-
crude protein (198 g vs. 161 g/kg DM) seems cause sole ulcers are located at the point of the
to be a risk factor (10, 11). sole where the pressure is highest, BW intui-
Although the combination of trimming in tively seems to be important. High milk yield is
May to August and disease involved only 14 stated to be an important risk factor for lamini-
(.9%) Observations, the very strong relative ef- tis (13, 15). Fatcorrected milk at the first test
fect of this combination (OR = 11.7, not day was used in the analysis because it is
shown) indicates that disease potentiates the expected to be relatively high for those cows
effect of season of trimming or vice versa. that are fed a relatively large amount of concen-
Thus, it may support the hypothesis that SF is trate relative to roughage immediately after
traumatic in origin. Disorders affecting the limb calving. Such a feeding procedm increases the
can be expected to compromise claw horn pro- risk of m e n acidosis and related disorders,
duction and thereby increasing susceptibility to which are expected to predispose the cow to
sole ulcers. Cows with a limb disorder probably laminitis.
shift their weight from the affected to Cows belonging both to the high FCM
nonaffected limbs, thus increasing their burden. group and the high BW group (high FCM plus
Sore feet could also cause a cow to lie down high BW) had the lowest risk of SF (OR = 2.9)
more often, thus increasing the risk of contract- before 27 DIM. Later in lactation, the risk
ing infectious skin disorders of the limb. "he increased to 12 for the high FCM plus high BW
feeding in spring-summer might also increase group. Peterse (16) states that milk production
susceptibility to both SF and disease. is reduced immediately at calving among cows
Calving in May-June or September-october with sole lesions. However, observational
was associated with a 1.4-fold increased in the studies probably cannot clarify this cause and
odds of SF. These periods are when heifers are effect sequence. The high FCM plus high BW
tumed out and brought in from the pasture, group could have been allocated more concen-
respectively. Also,heifers calving in September trate despite the applied flat rate feeding princi-
to October will usually be brought into the cow ple, because farm workers commonly give pref-
herd directly from the pasture. Such abrupt erence to high yielding cows. Because of the
changes in the environment may be important higher social rank of heavy cows, they may
risk factors (3, 29). In addition, the roughage also have ingested more than their share of
ration is more likely to be low in fiber and high concentrates.
in protein content during these periods. The Heel erosion in the current lactation was
latter observation is in accordance with trim- associated with rn exponentially increasing risk
ming in May to August being associated with a of SF and, consequently, was the only variable
higher risk of SF. The process of adapting to that justified an analysis as an untransformed
different environments and rations is a promis- continuous variable. However, the ordinality
ing area for future studies because these factors assumption of the regression procedure was
have a large potential for manipulation. An- probably not ~31stified, since the logit cumula-
other interesting view of this finding is that tive probability curves clearly converged with
cows calving in May to September had a lower increasing degrees of heel erosion especially
mi& production (9). above degree 2. For this reason and because of
As expected, stage of lactation at trimming the low number of observations above degree 2,
was very strongly associated with the risk of the present effect estimates probably are not
SF. Plots of the combined data (not shown) valid above degree 2 of horn degradation. As-
Journal of Dairy Science Vol. 74, No. 4, 1991
1290 EN'EVOLDSEN ET AL.

sociations between sole ulcer and heel erosion Sole Ulcer in More Than One
have been reported previously (2, 14). Claws Foot in First Lactation
softened by sole ulcers may be more suscepti-
ble to heel erosion (6, 29) or the erosion may The final model of MF in the fiist lactation
reduce the weight-bearing surface, thus increas- included the terms season of trimming, season
ing the pressure on the remaining sole (28). of calving, stage of lactation, FCM-BW, horn
Previous analyses of these data (27) have erosion, and disease. In addition, the interaction
shown that the overall prevalence of severe heel terms season of trimming x season of calving,
erosion increased almost linearly from first season of trimming x horn erosion, season of
calving to the end of lactation 2, and the overall calving x disease, stage of lactation x disease,
sole ulcer prevalence fluctuated during the and disease x FCM-BW were included in the
same period. Such a pattern indicates that heel model. Sole ulcers in more than one foot of the
erosion probably is not the most important risk degrees 1 to 2, 3, and 4 to 5 occurred among
factor in individual cows. As described, howev- 11.2, 17.3, and 12.9% of cows, respectively. To
er, the associations between diseases and sole facilitate interpretation of the effect estimates,
ulcer show that the same group of cows have cows calving in November to April and all the
heel erosion, sole ulcers, and disease, i.c., these other cows were analyzed in two separate sta-
conditions share common risk factors. Experi- tistical models (Tables 2 and 3). In the first step
mental studies could be useful to clarify further of the data analysis (before including interac-
the relationship between sole ulcer and heel tion terms), calving in May to October was
erosion. associated with a 1.3 times higher risk of sole

TABLE 2. Final logistic regression model of sole ulcer in more than one foot in lactation 1. Calvings were in
November to April. Sole ulcer of degrees 1 to 2, 3, and 4 to 5 occnmd among 7.7, 15.0, and 11.9% of the 866 COWS.
~ ~ ~~

Percentage Odds 95%


Description of variables' of n ratio CI
Month of tbmiqd and heel crosion
Trimmiq~M a y to Aug and
Heel erosion degrees 2 to 4 .9 16.8 3.9 to 71
Heel erosion degree 1 4.3 8.1 3.7 to 18
No heel erosion 17.6 3.7 2.3 to 6.0
Trimmiog Sep to Apr and
Heel erosion degrees 2 to 4 4.8 4.5 2.1 to 9.6
Heel erosion degree 1 12.1 3.6 2.7 to 6.0
No heel erosion 60.3 1.o ...
Discase' and K u - B W 3 and stage of lactation
Disease and
FCM 4 9 . 6 kg or BW <490 kg
Trimming 229 DIM 45 9.4 3.9 to 23
No disease and
FCM 219.6 kg and BW 2490 kg (High PCM
+ €€ishBW) and
Trimminga9dinmilk 6.9 1.3 .5 to 2.1
Trimming229dinmilk 13.4 6.4 3.3 to 12
FCM 4 9 . 6 kg or BW <490 kg and
Trimminga9dinmilk 21.6 1.o ...
TrimmingZ29dinmilk 51.5 4.6 2.6 to 30
lIn addition. herd-year of calving is included in the model. Three combinations of disease,XM-BW, and stage of
lactation are omitted.
21nclwies limb disorder alone (limb) or in combhtion with otha disease (severe plus limb, limb pills othm, severe
plus limb plus other). see text.
%CM = 4% at fjrst test day after calving. BW = body weight after calving, U = confidence interval.

J o d of Dairy Scimcc VoL 74, No. 4, 1991


EFTDEMOLOGY OF SOLE ULCERS 1291
ulcer (95% CI: 1.1 to 1.7). This effect estimate The disease factor, in contrast, affected few
was similar to the finding in the model of SP in cows, but had a very strong relative effect (OR
Table 1 and probably can be explained similar- 2 to 139). The logit cumulative probability
1Y* curves converged to a minor extent, making the
The effect estimates for cows calving in ordinality assumption less valid. However, dis-
November to April are presented in Table 2. ease clearly was strongly associated with MF in
Among cows without heel erosion, the cows early lactation. The effect of disease on sole
trimmed in May to August were 3.7 times more ulcer is fresuently mentioned in the literature
likely to contract sole ulcer compared with (6, 12, 15, 16), but as noted by Weaver (29),
other cows. The corresponding effect on SF the statistical evidence is sparse and seemingly
(Table 1) was 1.5, but these estimates cannot be based on qualitative evaluations of clinical
compared directly. However, feeding and cases without establishing proper comparison
stress, which can be expected to act systemical- groups. Metabolic and digestive disorders and
ly, probably are more important risk factors for metritis usually are regarded as the most impor-
MF than for SF. Heel erosion occurred less tant disease risk factors. In this analysis, they
frequently among cows calving in May to Oc- had an effect only when combined with other
tober (69.9%) than in April to November diseases. In contrast, limb disorders had an
(77.9%). The effect of degree 1 heel erosion effect by themselves. This could have been due
differed in the two trimming periods, but the to a lack of statistical power or the possibility
very small number of cows with high degrees that the animals with severe disease had died or
of heel erosion make inferences difficult. In had been culled, whereas those animals
contrast to the model of SF (Table l), the responding to treatment benefited from associ-
ordinality assumption of the regression proce- ated changes in dia and environment. This
dure seemed to be reasonably satisfied, but the hypothesis was supported by the finding that
numbers of heel erosion degrees 3 to 4 were severe must be associated with limb or other to
small. However, heel erosion evidently was increase the risk of MF. Diseases in category
strongly associated with MF. The association other may have been sequelae to severe cases
was stronger than with SF, supporting the hy- that were extremely severe. Herd mates may
pothesis that soft horn characteristic of claws also have had untreated (subclinical) long-last-
with sole ulcers promotes the formation of heel ing cases of the same diseases causing some
erosion. cases of MP, thus decreasing the relative effect
Table 2 summarizes the estimated effects of of the treated cases that had observed clinical
belonging to one of the eight possible combma- disease. The practicing veterinarians in the
tions of the dichotomized variables stage of herds had access to approximately 200 different
lactation, FCM-BW, and disease. In this model, diagnostic codes. These were used differently
disease was defined as belonging to either limb, in various herds, which made distinguishing
severe plus limb, severe plus other, limb plus between severe and nonsevere cases of disease
other, or severe plus limb plus other. The risk difficult. Misclassifications which decrease the
of MF increased markedly near 29 DIM for magnitude of the effect estimates, therefore
cows without disease. For cows without dis- probably occurred. This was an argument for
ease, the increased risk after 29 DIM was most pooling diagnoses.
pronounced for cows belonging to the high The effect estimates for calving in May-
FCM plus high BW group, supporting the hy- October are presented in Table 3. Among cows
potheses that the stress of a relatively high mi& without heel erosion, there was no increased
production and the increased pressure on the risk associated with trimming in May to Au-
horn producing tissues caused by a high BW gust, which contrasts to the estimate in Table 2.
increase the susceptibility to sole ulcer, The Explanations could be that the horn quality of
estimated OR of high FCM plus high BW this group was better or that they were on
range from 1.3 to 8.9, depending on stage of pasture longer prior to calving. Housing condi-
lactation and disease. Because this factor exerts tions also might have been less crowded during
its effect on a relatively large proportion of May to August. The stronger association to
cows, the total effect on the population can be heel erosion in this period supports these hy-
substantial. potheses. The estimated effects of stage of lac-
J d of Dajxy Science Vol. 74, No. 4, 1991
1292 ENEVOLDSEN ET AL.

tation and FCM-BW were similar to the esti- effect of heel erosion, which occurred more
mates in Table 2. frequently in lactations 2 to 9 compared with
lactation 1, was comparable to the effect esti-
Sole Ulcer In One Foot In mated for SF among cows in lactation 1. But as
Lactatlons 2 to 9 for SF model, the ordinality assumption may
not be completely valid.
The frnal model of SF in lactations 2 to 9 Table 4 provides separate estimates of the
included the following terms: season of trim- effectsof different degrees of SF and MF at the
ming, stage of lactation, days between trim- preceding trimming. Although Mp had an ef-
mings, heel erosion, sole ulcer previous trim- fect, a dose-response relationship was lacking,
ming, disease, stage of lactation x disease, days maybe because the numbers were rather small.
between trimmings x disease, and sole ulcer Severe cases in the previous lactation might
previous trimming x disease. Sole ulcer of have been culled more frequently, leading to a
degrees 1 to 2, 3, and 4 to 5 occurred among selection bias or the cows may have been
16.3, 8.6, and 6.4% of cows, respectively. To offered special attention in the current lactation,
facilitate interpretation of the effect estimates, e.g., earlier trimming in lactation. In contrast,
cows less than 67 DIM and all others were SF exhibited a dose-response relationship with
analyzed in two separate statistical models. In SF at previous trimming. This finding supPoas
the first step of the data analysis (before includ- the hypothesis SF and h4F being two different
ing interaction terms), 67 DIM or greater was claw disorders. The variable sole ulcer at previ-
associated with a 2.0 times higher risk of sole O U S trimming was included in the analysis due
ulcer (95% CI: 1.4 to 2.9). Hots (not shown) to the high heritability of sole ulcers and re-
indicated that the effect of stage of lactation search repom stating that laminitis recurs in the
clearly occurred later in lactations 2 to 9 com- same animals in successive lactations (16).
pared with lactation 1, and the effect estimates Consequently, this variable may be very impor-
also were smaller although an exact comparison tant in making management decisions concem-
was not possible. ing individual cows. This analysis confirmed
The model selected for cows less than 67 that sole ulcer is a highly repeatable disorder.
DIM (T.able 4) included only the variables heel The estimated effects for cows 67 DIM and
erosion and sole ulcer previous trimming. The greater are presented in Table 5. Although the

TABLE 3. Pinsl logistic regression model of sole ulcer in more than one foot (MFj in lactation 1. Calvin@ were in May to
October. Sole ulcer of degrees 1 to 2. 3, and 4 to 5 OCcllITdd among 6.4, 19.5, and 13.8% of the 897 cows.
perwtagt odds 95%
Dcscriution of variables' of n ratio a*
Month of trimming and heel erosion
Trimming May to Aug iuhd
Heel aosion degrees 2 to 4 15 22.3 5.3 to 93
Heel erosion degree 1 4.3 2.7 1.3 to 5.5
No hecl erosion 16.4 12 .8 to 1.9
Trimming Sep to Apr and
Heel erosion degrees 2 to 4 7.8 2.9 1.6 to 5.2
Heel erosion degree 1 165 1.7 1.1 to 2.5
No heel erosion 535 1.o ...
Stage of lactation
TrimminE; 229 d in milk 71.9 45 3.0 to 6.8
Trimming a 9 d in milk 28.1 1.o ...
-
4% FCM test d 1 (FCW and BW at cahrina
PCM 219.6 kg and BW 2490 kg 21.4 1.4 1.0 to 2.1
PCM 4 9 . 6 kg or BW 490 kg 78.6 1.o ...
1In addition. hcrd-ycar of calving is included in the model.
k
I = Confidcnct interval.
Journal of Dairy Science Vol. 74. No. 4, 1991
EPIDEMIOLOGY OF SOJA ULCERS 1293
TABLE 4. Final logistic regression model of sole ulcer in single foot (Sp)in lactations 2 to 9. Sole ulcer of degrees 1 to 2,
3, and 4 to 5 o c c ~ e damong 11.9, 8.1, and 55% of the 471 COWS. Cows were trimmed less than 67 d after calving.
Pcrccntage Odds 95%
Description of variables' of n ratio cI2
Heel m i o n
Heel erosion degrees 2 to 4 17.8 2.6 1.3 to 5.1
Heel erosion degree 1 255 1.9 1.1 to 3.5
No heel erosion 56.7 1.o ...
Sole ulcer at previous trimming
Sole ulcer in mom than one digit 0
Degrees 4 to 5 2.6 2.9 .7 to 12
Degree 3 2.8 J .1 to 2.4
DegreesltoZ 2.6 3.9 1.0 to 16
Sole ulcer in one digit (Sp)
Degrees 4 to 5 2.6 11.1 2.6 to 49
hP 3 4.0 2.8 1.0 to 7.5
Degreeslto2 9.6 1.4 .7 to 3.1
No sole ulcer 75.8 1.o ...
lIn addition, herd-year of calving is included in the model.
%=IConfidence intmal.

ordinality assumption was slightly violated, easily as discussed above. The steady increase
heel erosion was clearly associated with SF. in prevalence with age (population) is in agree-
However, the lack of a dose-response effect ment with this finding with individual cows.
contradicted the hypothesis of heel erosion as a The combined disease classes limb, severe
direct cause of SF. More likely, certain claws plus other, severe plus limb, limb plus other,
or cows were susceptible to both disorders or and severe plus limb plus other were associated
the claws with sole ulcers were degraded more with a 2.9 to 9.8 times higher risk of SF,which

TABLE 5. F d logistic regression model of sole u l w in single foot (SF)in lactations 2 to 9. COWStrimmed 67 d or later
after calving. Sole ulcer of degrees 1 to 2. 3. and 4 to 5 OCcMed among 21.9, 9.3, and 7.5% of the 375 cows.
Pnccntage Odds 95%
Description of variables' of n d 0 cI2
Heel erosion
Heel erosion degrees 2 to 4 205 1.4 .7 to 2.8
Heel erosion degree 1 29.6 25 1.4 to 4.6
No heel erosion 49.9 1.o ...
oiseast3 and trim interval4 and sole ulcer previous
Disease and trim interval A 5.3 9.8 2.8 to 33
No diswse and trim intmals A and
Sole ulcer previous degrees 1 to 5 75 3.6 1.1 to 12
No sole ulcer previous 45.1 12 5 to 2.9
No disease and trim inteavats B and
Sole ulcer previous degrees 1 to 5 11.1 1.o ...
No sole ulcca urcvims 28.3 1.1 5 to 2.8
'In addition, herd-year of cahriog is included in the model. Disease combined with trim intend B omitted due to
imprecisiOlL
% =I Confidence interval.
h l u d e s disease classes limb, severe plus other, severe plus limb, limb plus other, and severe plus limb plus other. See
text.
%rim interval is number of days between current and preceding trimmiag. A 56 to 188 d and 204 to 258 d. B 189 to
203 d and more than 258 d.

Jonmal of Dairy Science Vol. 74, No. 4, 1991


1294 ENEVOLDSEN ET AL..

was largely similar to the effects on MF in separately in a later analysis to elucidate this
lactation 1. The effect differed according to the question. The trimming interval is a factor that
interval between p'w.Rding trimming (which should be considered when interpreting record-
occurred in the previous lactation) and the cur- ings of claw health. This intuitively reasonable
rent one. Similarly, the effect of sole ulcer at hypothesis is supported by experimental data
previous trimming differed among trimming in- showing that trimming immediately prior to the
tervals. These complex relationships are M i - second calving affects claw health positively
cult to explain satisfactorily. At trimming, ab- (16).
normal horn is removed but symptoms may
exist for some time, especially in cases of se Sole Ulcer In More Than One
vere sole ulcers. However, with very long inter- Foot In Lactations 2 Through 9
vals, the risk of new incidents is likely to The estimated effects on MF in lactations 2
increase due to increased burdening of the to 9 are presented in Table 6 and in Figures 1
pododerm caused by excessive sole horn. B e and 2. Trimming in July to October was associ-
cause trimming is performed simultaneously ated with a 2.2 times higher risk of MF com-
with the recording of claw health, trimming pared with other months. The seasonal effect
will automatically interfere with the subsequent was similar in magnitude to lactation 1, but
measurements. The pattern of plots of the risk occurred approximately 2 mo later. The expla-
cstimates for different trimming intervals nation may be that a higher proportion of sole
pointed to the presence of two different popula- ulcers among heifers were laminitis cases. The
tions. In population 1, the risk decreased stead- factors causing sole ulcers in heifers seemed to
ily from approximately 2 to 7 mo. In popula- act before calving or to act on a relatively more
tion 2, the risk decreased from approximately 7 susceptible newly calved animal. Excess pro-
mo and on. In addition, the pattern of sole ulcer tein supply and adaptational problems may pro-
degrees 1 to 2 differed from the more severe vide some explanation for this pattern.
cases. If cows were treated differently accord- A m o n g cows calving in September to Octo-
ing to their status at second trimming in the ber, MF occurred 5.4 times more frequently if
previous lactation or they were only trimmed the cows were less than 52 DIM, i.e., MF
once, such patterns might be the result. The occurzed earlier in lactation. However, the ordi-
findings at second trimming will be analyzed nal@ assumption appeared slightly violated.

TABLE 6. Final logistic regression model of sole ulcer in more than one foot at fmt trinOming in lactations 2 to 9. Sole
ulcer of degrees 1 to 2, 3, and 4 to 5 occurred among 7.3 125, and 7.3% of the 859 cows.
Percentage Odds 95%
Description of variables' of n ratio a2
Month of trimminj
Trimming Jul to Oct 27.7 2.2 1.4 to 3.3
Trimming Nov to June 72.3 1.o ...
Month of calving and stage of lactation
Calving Sep to Oct (rimming 252 d in milk 10.6 7.2 3.1 to 17
Calving Sep to Oct trhmming 4 2 d in milk 9.9 5.4 2.3 to 12
Calving Nov to Aug trimming 252 d in milk 48.0 5.2 3.2 to 8.3
Calving Nov to Aug himming 4 2 d in miJk 315 1.o ...
Disease in classes limb, severe plus limb, severe plus other,
Limb plus ob=, and severe plus limb plus other 7.3 2.1 1 2 to 3.9
No disease (remaining classes, see text) 92.7 1.o ...
Trim interval: days between current and preceding
56 to 178 d and 189 to 251 d 73.1 2.7 1.7 to 4 2
179 to 188 d and more than 251 d 26.9 1.o ...
'In addition, herd-year of calving is included in the model.
%=I
Confidence intaval.

Journal of Dairy Science Vol. 74, No. 4, 1991


EPIDEMIOLOGY OF SOLE UJXERS 1295
The instability in feeding (e.g., turning in, a m - same patterns and had an effect on MF as
mencement of feeding with sugar beets) during described in models of SF and poses the same
this period could be one explanation of the interpretational difficulties.
association. The work load in the herds usually For cows without sole ulcer at previous
was very high h m the middle of March until trimming, FCM-BW had no effect (Figure 1).
the middle of June and again from the middle For cows belonging to the low FCM-high BW
of August until the beginning of November. In group, the effect of sole ulcer at previous trim-
such periods, less attention obviously was paid ming was approximately 3 (8.1/2.6) times
to individual animals, thus possibly increasing higher than that of cows not belonging to the
the risk for an animal to have a low intake of low FCM-high BW group. The OR of sole
roughage for a longer period and thereby ulcer previous trimming was 6.8 (8.U1.2) in the
changing the roughage to concentrate ratio sig- low FCMnigh B W p u p versus 2.6 among the
nificantly. remainder. However, the cause and effect se-
The combined disease classes limb, severe quence is unclear. The milk yield may have
plus limb, severe plus other, limb plus other, been reduced among cows with poor claw
and severe plus limb plus other were associated health. These may have had a longer calving
with a 2.1 times higher risk of MF compared interval prior to the current lactation due to a
with the remaining health classes. This effect possible influence of lameness on repduction.
was smaller compared with h4F in lactation 1. Fatness resulting from a long calving intewal
The interval between trimmings exhibited the or other management factors is mentioned as a

Sole Ulcers in Dairy Cows


effects of FCM, BW & previous ulcers
101 I

0
8.7 I
d
d
8

R
a
?t.T;.I...........................................
t
I ...................... 19.0....
0

High FCM or t o w BW Low FCM 8 High BW


FCM at First Test & BW at Calving
Previous Trimming
-NO sole Ulcer Ulcer degrees 1-5
Wgure 1. Effects of milk yield, body weight at calving, arad occumnce of sole ulcer@) at the previous claw trimming
on ~JE odds ratios of sole ulcer in lactations 2 to 9. The percentage of dismBution of rhc obsQvations is presented ovec the
bars.

Journal of Dairy Science Vol. 74, No. 4. I991


1296 ENEVOLDSEN ET AL.

risk factor for sole ulcer (28). Due to a reduced farmers for individual cases of lameness.
intake of roughage early postpartum, fatness Therefore, the farmer decides what becomes an
may have caused a reduced FCM. For cows incident. Inferences about the nature of a long-
without heel erosion, MF occurzed approxi- lasting disease when the symptoms do not ac-
mately three times more frequently in lactations cur suddenly (like sole ulcers) are very diflicult
4 to 9 compared with lactations 2 and 3 (Figure to make unless some measure of the severity of
2). This finding is in agreement with the litera- that disease is available. Without such mea-
ture.Except for heel erosion degrees 2 to 4 in sures, the epidemiology of the factors that trig-
parity 3, heel erosion had a similar effect in ger treatment and not the epidemiology of the
lactations 2 to 9. A doseresponse effect was disease will be studied. In these herds the treat-
obvious in lactation 3 only. This mixed pattern ment frequencies were very different in herds
does not support the hypothesis of heel erosion with similar prevalences (25). Weaver (29) ar-
as a direct cause of sole ulcer. gues similarly. An explanation for older cows
The effect of parity was markedly smaller being at higher risk to sole ulcers could be the
than reported in studies of clinical claw disor- increase in claw size associated with both age
ders. An explanation could be the high culling and sole ulcer (2, 14).
rate (-35%) in these herds (26). Another expla- Initial analyses revealed that year of calving
nation could be that most studies of the epide and herd had systematic effects and that the
miology of sole ulcers are based upon observa- proportions of the combined degrees 1 to 2 of
tions made by veterinarians called by the sole ulcer increased during the study, indicating

Sole Ulcers in Dairy Cows


effects of parity & heel erosion

I L I P
..........................................
0
d
d ..........................................
8

R
a ...................
t
i
0

Lactation 2 Lactation 3 Lactations 4-9


Parity at Claw Trimming
Condition of Heels
No Eroslon Erosion degree 1 Erosion degrees 2-4

Pigure 2. Effects of parity and heel erosion on the odds ratios of sole ulcer. 'Ihe percentage of distribution of the
observations is presented over the bars.

Journal of Dairy Scimcc VoL 74, No. 4, 1991


EPIDEMIOLOGY OF SOLE ULCERS 1297

a possible shift in the recording procedure. ACKNOWLEDGMENTS


Consequently, herd-year of calving was forced Computations supporting this research were
into all models to account for some of the performed on the cornell Production Super-
possible systematic Merences in the skills of computer Facility, which is supported in part
claw trimmers, genetic characteristics of the by the National Science Foundation, New York
herd, quality of floors and stalls, type and State, and the IBM Corporation.
amount of bedding, type of glazing areas (wet,
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Journal of Dairy Science Vol. 74, No. 4, 1991

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