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Sole haemorrhages in dairy heifers managed under different underfoot and environmental conditions
Br. vet..[. (1996). 151, 57
SOI~
HAEMORRHAGES IN DAIRY I~ERS MANAGED UNDER DIFFERENT UNDERFOOT AND ENVIRONMENTAL CONDITIONS
J . J . VERMUNT* and P. R. G R E E N O U G H
Department of Veterinary Anesthesiology, Radiology and Surgery, Western Collegeof Veterinary Medicine, University of Saskatchewan, Saskatoon, Saskatchewan, Canada S7N OWO
SUMMARY Sole haemorrhages associated with laminitis were studied in 30 Holstein heifers in one herd housed either indoors on concrete or out of doors on a dry lot. Examinations were at 4-week intervals during a 15-month period from approximately 13 months of age to 2 months after calving. At 13 months of age, sole haemorrhages were present in 77% of the heifers. Five heifers, affected by clinical laminitis shortly after calving, developed early sole ulcers. Indoor-housed heifers had a greater n u m b e r of and more severe haemorrhages than heifers managed in dry lots (P<0.001). In both groups, hind claws were more .affected than front claws (P<0.001). Lateral claws were more affected in hind limbs (P<0.001), whereas medial claws had more sole haemorrhages in front limbs (P<0.01). Heifers managed in dry lots had more sole h a e m o r r h a g e s i n right claws than in left claws (P< 0.01). The n u m b e r and severity of haemorrhages differed among the six zones of the sole (P<0.001). Overall, the abaxial white zone (zone 2) had the greatest n u m b e r of haemorrhages, followed by the white zone at the toe (zone 0), the bulb (zone 5) and the sole-bulb junction (zone 4), respectively. Few haemorrhages occurred in the apex of the sole (zone 1) and the axial groove (zone 3). Zone 0 was more severely affected in heifers managed in dry lots (P<0.001), whereas zones 2, 4 and 5 h a d greater numbers of haemorrhages in heifers housed indoors (P<0.01). Time had no effect on total haemorrhages scores, but the effect of m a n a g e m e n t was significant for zones 0 and 5. Total h a e m o r r h a g e scores for zone 0 were greater in heifers managed in dry lots (P<0.05), whereas zone 5 was m o r e affected in indoor-housed heifers (P<0.01). This study shows that sole haemorrhages do occur in the claws of dairy heifers managed either
*To whom correspondence should be addressed at: 12 Park Road, Palmerston North, New Zealand. 0007-1935/96/010057-17/$12.00/0
© 1996 Ballli~re Tindal
BRITISH VETERINARY.]OURN,M.. 152. I
58
indoors or in dry lots, and permanent damage to the claws of these young cattle may already have occurred before they reach maturity. I~..~wom~s: Sole haemorrlaages: laminitis; heifers; management.
INTRODUCTION
In dairying countries worldwide, lameness in cattle is now recognised as a major economic and welfare problem. There is little doubt that (subclinical) laminitis, by affecting horn quality, is a major predisposing factor in the aetiolo~' of lameness caused by claw lesions such as white line (white zone) disease and sole ulcer (Bradley et aL, 1989; Greenough & Vermtmt, 1991). However, the Factors that are important in the aetiology of iaminitis are much less certain. It has been suggested that changes in the micl'o-circulation of the corium (dermis) of the claw contril> ute to the development of laminitis, with arterio-venous anastomoses (AVAs) playing a crucial role (Vermunt, 1999; Vermunt & Leach, 1992). The main factors that are considered to predispose cattle to laminitis have been reviewed recenth' (Vermunt & Greenougla, 1994) and include systemic disease, nutrition, age, growth, housing, bedding, exercise, calving, behaviour and conformation. The predominalat features of laminitis are haemorrhages in the sole and ahnormal horn production (Bradley et aL, 1989; Greenough et al., 1990; Greenough & Vermunt, 1991 ). Most earh' studies on bovine lalninitis and associated lesions have been carried out on adult cattle and slaughterhouse material and, until recently, claw lesions of imnmture dairy cattle received little attention. However, Bradley et al. (1989) and Vermunt (1990) reported sole haemorrhages in the claws of 5-and 6-month-old heifer calves, respectively; Frankena et aL (1992) reported that sole haemorrhages were present in calves as young as 10 weeks of age and found a positive correlation between sole haemorrhages and age. Bargai et al. (1999) reported outbreaks of laminitis and associated sole haentorrhages in cah'es aged 4-6 months. Therefore, there is increasing evidence that damage to the claws of young dairy cattle may already occur before the}' reach maturi W. The aim of the present study was to describe the distribution of sole haemorrhages in dail T heifers between the ages of 13 and 24 months, managed under different underfoot and environmental conditions.
MATERIALS AND METHODS
The study was carried out from January 1989 to April 1990. Heifers were examined every 4 weeks with, in general, claw examinations starting when the animals were approximately 13-months old and finishing 2 months after calving. Some heifers had not yet, or had only recently calved at the end of the study and, therefore, their records were incomplete. Animals
Thirty Holstein heifers, replacements for the dairy herd on the campus of the
SOI.E HAEMORRHAGES IN DAIRY HEIFERS
59
University of Saskatchewan, were used for this study. All animals were raised on the farm.
Management and nutrition Replacement heifers were moved to a breeding group at 12-13 months of age. This group was maintained out of doors on a dry lot with access to a well-bedded shelter. Heifers were artificially inseminated when they reached a body weight of 340 kg or at 15 months of age; they were not bred under 13 months of age. In the breeding group, heifers received 2 kg of a growing heifer concentrate (67% total digestible nutrients (TDN) or 10.21 MJ kg -~, and 14% crude protein (CP) on an 'as fed' basis). Good quality alfalfa hay (90% dry matter, 52% TDN or 9.62 MJ kg-n and 14% CP) was available ad libitum.
7:reatment groups and experimental design Actual treatments were imposed when heifers were diagnosed pregnant (generally 42 days after conception) and continued until 2 weeks prior to their expected calving date. Heifers were randomly allocated to one of two groups a., they became available until a total of 15 animals had been allotted to each group.
Heifers housed indoors. These heifers joined the adult cows in the dry group, housed in a separate area of the free-stall (cubicle) barn. The animals had acces., to cubicles bedded with rubber mats plus a limited a m o u n t of cut straw during the winter months. Approximately two-thirds of the floor area of the alleyways alon8 the cubicles was slatted; the remainder of the floor was solid concrete. Animals in the dry group were fed 1 kg of a dry cow concentrate (fed as a carrier of minerak, and vitamins) and 4 kg chopped, good quality alfalfa hay per day plus barley silag~ to meet their daily energy requirements. The ration was provided as a complet~ mixed diet with an average particle length of 2.5 cm. There was always sufficien~ cubicle and feeding space for all cattle to rest and feed together. Heifers managed in d~), lots. These heifers stayed out of doors for the remainde] of their pregnancy. No mature, dry cows were present in this group and the animals were confined on an earth and gravel-surfaced corral. Straw was used a~ bedding in the shelter. For 4-5 months of the year, the ground surface was frozen often snow-covered or icy, and rather rough. Heifers in this group received the same nutrition on a per head basis as the indoor-housed animals and there wa~ always adequate bunk space. All animals, whether indoor-housed or dry lot, had free access to a commercia 1:1 mineral mix (19% calcium:19% phosphorus) with trace minerals and vitamin: A, D and E. Good quality water was available from drinking bowls at all times. Approximately 14 days prior to their expected calving date, heifers from bott groups were transferred to individual, indoor box-stalls, which were bedded with thick layer of straw. The a m o u n t of concentrate fed was increased by dail' increments so that animals were consuming 2 kg dairy concentrate (71% TDN o: 10.8MJkg-', and 19% CP) plus 2 k g fresh cow concentrate (71% TDN o: 10.8 MJ kg-~, and 18% CP) by the time they calved. After calving, dairy concen trate was increased by 0.5 kg per day and heifers were moved to flae lactating here in the free-stall barn when they were consuming a total of 8 kg dairy concentrat4
60
BRITISH VETERINARY .JOURNAL., 152, I
per day. Forage (barley silage and alfalfa hay) was fed at a rate of 1.7% of the average body weight on a dry matter basis. During lactation, cows were offered a semitotal mixed diet and additional concentrate was fed through computerised feeding stalls in order to meet the animals' energy requirement. The dimensions of the cubicles in the free-stall barn were 2.15 m x l . 2 m and the grooved, concrete floor was scraped several times per day.
Evaluation of sole haemorrhages The claws of heifers housed in the free-stall barn were examined using a custom made, hydraulic tilting table. A conventional restraining crush (Superstall II, A.C. Bakx Industries) was used when heifers were housed elsewhere. At each examination, a sliver of horn was pared from the soles of all eight claws to expose fresh horn. Photographs were taken of the trimmed plantar/palmar aspect of the claws and were used for evaluation of haemorrhages in the sole. Haemorrhages were localized as to zone of the sole, n u m b e r e d 0-5 (Greenough & Vermunt, 1990). Zone 0 was a m e n d e d to include the axial white zone at the toe (Fig. 1). The severity of sole haemorrhages was scored by the density and extent of the haemorrhage: no haemorrhage was scored as 0; slight haemorrhage, 1; moderate, 2; marked, 3; severe, 4; exposed corium and associated haemorrhage, 5 (Figs 2-5).
A nimal performance Heifers were weighed at birth, at weekly intervals until weaning at approximately 75 kg of body weight, and once every 4 weeks thereafter. Average daily
Fig. 1. Diagram showing the six zones of the weight-bearing surface ('sole') of the bovine claw. Zone 0, white zone at the toe; zone 1, apex of the sole; zone 2, abaxial white zone including the wall-bulb junction; zone 3, axial groove; zone 4, sole-bulb junction; and zone 5, bulb.
SOLE HAEMORRHAGES IN DAIRY HEIFERS
Fig. 9
Fig. S
Fig. 4
Fig. 5
61
Fig. 2. Moderate (score 2) haemorrhage in zone 0 of the left hind lateral claw and slight (score 1) haemorrhage in zone 4 of the left hind medial claw. Fig. 3.
Marked (score 3) haemorrhage in zone 2 of the left hind lateral claw.
Fig. 4. Severe (score 4) haemorrhage in zone 9, moderate (score 9) haemorrhage in zone 1 and slight (score 1) haemorrhage in zone 4 of the left hind lateral claw. Note the haemorrhage that can be seen only as a blue tinge, deep within the horn in zone 3 of the same claw. Fig. 5. Severe (score 4) haemorrhage at the transition of zone 3 into zone 4 of the right h i n d lateral claw; moderate (score 9) haemorrhage in zones 2 and 5 o f the same claw.
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BRITISH VETERINARY JOURN.AL, 152, 1
weight gain (ADG) from birth .40 breeding, from birth to calving, and from breeding to calving was calculated.
Statistical analysis All data were analyzed using SAS (Statistical Analysis System, SAS Institute Inc.). Eleven heifers in each group had at least one post-calving examination, whereas seven and eight animals from the 'indoors' and 'dry lot' group, respectively, had two examinations after calving.
Descriptive analysis. Differences in the n u m b e r and severity of haemorrhage scores between groups, between left and right, hind and front, and lateral and medial claws, and between the zones of the sole was analyzed using the Chi-square test. This test was also used to compare the prevalence of sole ulceration between the two groups. A non-parametric one-way analysis of variance (ANOVA), the Kruskal-Wallis H test, was used to test for differences between claws for each zone and for differences between zones within each claw. Correlation coefficients between accumulated haemorrhage scores (scores 0-5x8 clawsx6 zones; theoretical range 0 to 240) and weight gains were calculated using Pearson's correlation analysis. Comparative analysis. The data, collected from repeated observations over time on the same experimental units (i.e. heifers), were also analyzed by repeated measures ANOVA. Total haemorrhage scores for each of the six zones of the sole were obtained by summing the scores in all eight claws for each examination (theoretical range of 0 to 40). Means of total haemorrhage scores for the different examinations were separated using the General Linear Models (GLM) procedure of SAS and comparisons among these means were carried out using Scheffe's Sprocedure. Factors of interest were time and treatment (management group), and their effects were analyzed, using the F-statistic, for the actual treatment period, i.e. from entry into the respective group through to calving (examinations - 7 to 0). RESULTS
Haemorrhages in the sole At the first examination at approximately 13 months of age, 77% of the heifers had sole haemorrhages in one or more claws. These haemorrhages were on the surface and could be pared out. Before calving, no haemorrhages with a score greater than 3 were recorded for any of the six zones of the sole and no haemorrhages with a score of 5 were observed during the entire study. Haemorrhage scores ranged from 0-3 for zones 0 and 5, whereas zones 1, 2, 3 and 4 had scores varying from 0 to 4. At the first post-partum examination, sole haemorrhages were present in five heifers affected by clinical laminitis. In some cases, haemorrhage was seen as a blue tinge, deep within the sole horn (Fig. 4). When re-examined at the last examination, approximately 2 months after calving, the condition had worsened. Severe haemorrhage or early sole ulceration had developed at the transition of
SOLE HAEMORRHAGES IN DAIRY HEIFERS
63
INDOORS
~
LFL
LFM
RFM
RFL
LHL
LHM
RHM
RHL
<0.1
[]
0.5
0x 6~ @ 03
I I 06 m 07 D 06
I
I I ,06
0,
LFL, leftfront lateral; LFM, leftfront medial; RFM, right front medial; RFL, right front lateral; LHL, lefthind lateral; LHM, lefthind medial; RHM, right hind medial; RHL, right hind lateral.
Fig. 6. Illustration of mean haemorrhage scores (0-5; n=204) fOl"the six zones of the sole in the frout and hind limb claws of heifers housed indoors.
z o n e 3 into z o n e 4 (Fig. 5) in o n e o r b o t h h i n d lateral claws o f t h r e e heifers f r o m the i n d o o r - h o u s e d g r o u p a n d two heifers f r o m the g r o u p m a n a g e d in dry lots (P>0.05). T o e ulcers were r e c o r d e d for o n e heifer in each group; b o t h animals h a d b e e n affected by clinical laminitis and also had early sole ulcers. Mean h a e m o r r h a g e scores for the two g r o u p s o f heifers are illustrated in Figs 6 a n d 7. Overall, i n d o o r - h o u s e d heifers h a d a g r e a t e r n u m b e r of, a n d m o r e severe, sole h a e m o r r h a g e s than heifers m a n a g e d in dry lots (P<0.001). In h i n d claws, the n u m b e r and severity o f h a e m o r r h a g e s were g r e a t e r in i n d o o r - h o u s e d heifers
64
BRITISH VETERINARY.JOURNAL, 152, I DRY LOT
LFL
LFM
RFM
RFL
LHL
LHM
RHM
RHL
~<0.1
~
R o.~
m o.,
0.2
@ o.~ m o.~
0.5
_____ o.7
~ o., m ~o.,
LFL, leftfront lateral; LFM, leftfront medial; RFM, right front medial; RFL, right front lateral; LHL, lefthind lateral; LHM, lefthind medial; RHM, right hind medial; RI-IL,right hind lateral.
Fig. 7. Illustration of mean haemorrhage scores (0-5; n=199) for the six zones of the sole in the front and hind limb claws of heifers managed in dry lots. (PO.05), but the severity was g r e a t e r in heifers m a n a g e d in dry lots (P<0.01). F r e q u e n c y distributions o f h a e m o r r h a g e scores for the differing claws are pres e n t e d in Tables I a n d II. In b o t h g r o u p s t h e r e were a g r e a t e r n u m b e r a n d m o r e severe h a e m o r r h a g e s in h i n d claws than in f r o n t claws (P<0.001). M o r e h a e m o r rhages o f g r e a t e r severity were r e c o r d e d in f r o n t medial claws t h a n in f r o n t lateral claws (P<0.01). H i n d lateral claws h a d a g r e a t e r n u m b e r of, a n d m o r e severe,
SOLE HAEMORRHAGES IN DAIRY HEIFERS
65
Table I Frequency distribution (%) of sole haemorrhage scores for heifers (n=30) either housed indoors or managed in dry lots (examined from 13 months o f age to 2 months after calving) Indoors (9792 Left Right Front Hind Lateral Medial
Scow 0
Score 1
Score 2
Score 3
Score 4
(I -4) *
%
scores) 39.11 38.34 42.06 35.39 37.17 40.28
8.37 8.86 6.50 10.74 9.63 7.61
2.18 2.35 1.25 3.28 2.66 1.87
0.29 0.44 0.18 0.54 0.49 0.23
0.05 0.01 0.01 0.05 0.05 0.01
10.89 11.66 7.94 a 14.61" 12.83" 9.72"
50 50 50 50 50 50
7.02 8.02 5.79 9.25 8.31 6.73
1.83 2.35 1.61 2.56 2.43 1.75
0.30 0.51 0.36 0.46 0.48 0.34
0.01 0.03 0.00 0.04 0.03 0.01
9.17" 10.91" 7.76" 12.32" 11.25" 8.83"
50 50 50 50 50 50
Dry lot (9552 scores) Left 40.83 Right 39.09 Front 42.24 Hind 37.68 Lateral 38.75 Medial 41.17
*Within this column and hetween claw pairs (left remus right, front versus hind, or lateral versus medial); percentages with identical letters are significantly different; ("P<0.001).
Table II Frequency distribution (%) o f sole haemorrhage scores for front and hind limb claws o f heifers (n=30) housed either indoors or managed in dry lots (examined from 13 months of age to 2 months after calving) F~vnt claws
Hind claws
Score 0
Scores (1-4) *
Score 0
Scores (1-4) *
Indoors (4896 scores) Left Righ t
42.30 41.83
7.70 8.17
35.93 34.84
14.07 15.16
Dry lot (4766 scores) Left Right
43.13 41.35
6.87" 8.65"
38.53 36.83
13.17h
Indoors Lateral Medial
43.12 41.01
6.88" 8.99"
31.23 39.54
18.77" 10.46"
Dry lot Lateral Medial
42.96 41.52
7.04 b 8.48 h
34.53 40.83
15.47;' 9.17"
11.47h
*Within these columns and groups (indoors or dry lot), and between claw pairs (left versus right, fi'ont versus hind, or lateral versus medial); percentages with identical letters are sigqificantly differe,at; ("P<0.001; bP<0.01).
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BRITISH VETERINARY.JOURNAL. 152. I
Table III Frequency distribution (%) o f haemorrhage scores (1-4 combined) for the six zones of the sole in heifers (n=30) housed either indoors or managed in dry lots (examined from 13 months of age to 2 months after calving) All claws
Front claw.~
Hind claws
Zone 0 (3224 scores) Indoors Dry lot
13.52 17.00"
9.68 12.41 h
17.37 21.59"
Zone 1 (3224 scores) Indoors D~y lot
3.41 3.(}7
1.74 2.54
5.09' 3.60
Zone 2 (3224 scores) Indoors Dr}, lot
24.53 22.53
17.99 19.98'
31.08" 24.94
Zone 3 (3224 scores) Indoors Dry lot
1.61 1.40
0.74 1.12
2.48 1.67
Zone 4 (3224 scores) Indoors Dry lot
10. I I" 7.26
4.96h 2.98
15.26 h I 1.54
Zone 5 (3224 scores) Indoors Dry lot
15.29" 8.31
13.09" 6.95
17.49" 9.68
"P<0.001; hP
h a e m o r r h a g e s than h i n d medial claws (P<0.001). Heifers m a n a g e d in dry lots had m o r e h a e m o r r h a g e s in right h i n d claws than in left h i n d claws (P<0.01); the h a e m o r r h a g e s were also m o r e severe (P<0.05). In these heifers, m o r e h a e m o r rhages o f g r e a t e r severity were also r e c o r d e d for right fi'ont claws c o m p a r e d with left f r o n t claws (P<0.001). T h e r e were no differences in the nunaber a n d severity o f h a e m o r r h a g e s between right and left fi'ont claws o f heifers h o u s e d i n d o o r s (P>0.05). H a e m o r r b a g e s r e c o r d e d in right h i n d claws o f these animals were m o r e severe (P<0.05), but not g r e a t e r in n u m b e r (P>0.05), when c o m p a r e d with left h i n d claws. F r e q u e n c y distributions o f h a e m o r r h a g e scores for the six zones o f the sole are p r e s e n t e d in Table III. For all (front a n d hind) claws c o m b i n e d , there were a g r e a t e r n u m b e r of, and m o r e severe, h a e m o r r h a g e s in z o n e 0 in heifers m a n a g e d in dry lots (P<0.001). T h e n u m b e r and severity o f h a e m o r r h a g e s in zones 1, 2 and 3 did not differ between the two g r o u p s (/:'>0.05). I n d o o r - h o u s e d heifers had a g r e a t e r n u m b e r o f h a e m o r r h a g e s in zones 4 a n d 5 (P<0.001). T h e s e heifers also h a d m o r e severe h a e m o r r h a g e s in z o n e 4 (P<0.01) and z o n e 5 (P<0.001). In f r o n t claws, t h e r e were n o differences in n u m b e r a n d severity o f b a e m o r r h a g e s in zones 1 a n d 3. Heifers m a n a g e d in dry lots h a d m o r e h a e m o r r h a g e s o f g r e a t e r severity in z o n e 0 (P<0.01) a n d z o n e 2 (P<0.05). I n d o o r - h o u s e d heifers h a d m o r e h a e m o r rhages o f g r e a t e r severity in zone 4 (P<0.01) a n d z o n e 5 (P<0.001). In h i n d claws,
SOLE HAEMORRHAGES IN DAIRY HEIFERS
67
there were no differences in number and severity of haemorrhages in zone 3. Heifers managed in dry lots had a greater number of, and more severe, haemorrhages in zone 0 (P<0.001). Indoor-housed heifers had more haemorrhages of greater severity in zones 2 and 5 (P<0.001). Also, there were more haemorrhages (P<0.01) of greater severity (P<0.05) in zone 4 in heifers housed indoors. Haemorrhage scores for the six zones of the sole were also compared between left and right, front and hind, lateral and medial, and front and hind lateral and medial claws for each group separately. Indoor-housed heifers had more haemorrhages in zone 4 of right claws compared with left claws (P<0.01). Heifers managed in dry lots had more haemorrhages in zones 0 and 4 of right claws (P<0.001). In both groups, there were more haemorrhages in zones 0, 2, 4 and 5 of hind claws compared with front claws (P<0.001). In indoor-housed heifers, zones 2 and 5 of front medial claws had more haemorrhages compared with front lateral claws (P<0.001). In heifers managed in dry lots, only zone 2 had more haemorrhages in front medial claws (P<0.001). In both groups, all zones had more haemorrhages in hind lateral claws than in hind medial claws; the difference being least significant for zone 0. Relatively few haemorrhages occurred in zones 1 and 3 compared with the other four zones of the sole. Overall, zones 2 and 5 had a peak in total haemorrhage score at the tenth examination before calving. After calving, there was an increase in total haemorrhage scores for most of the six zones (P<0.05), except for zones 3 and 5. The repeated measures ANOVA for examinations -7 to 0 revealed that, for all six zones, time effects were not significant for total haemorrhage scores. However, there were significant treatment (management) effects of total haemorrhage scores in zones 0 and 5. Heifers managed in dry lots had greater total haemorrhage scores for zone 0 (P<0.05); indoor-housed heifers scored higher for zone 5 (P<0.01). There was no significant time by treatment interaction.
Animal performance For both groups, ADG from birth to breeding was 0.78 kg. From breeding to calving, ADG of heifers housed indoors was 0.83 kg and for heifers managed in dry lots ADG was 0.89 kg. Their respective ADG from birth to calving was 0.80 and 0.83 kg. No significant correlations were found between accumulated haemorrhage scores and average daily gains.
DISCUSSION Sole haemorrhages as recorded in the present study have been described in the literature as signs of snbclinical laminitis (Peterse, 1979; Bradley et aL, 1989; Greenough & Vermunt, 1991). The heifers affected by clinical laminitis in the early post-partum period presented a characteristic picture. The severe haemorrhages associated with the laminitic insult only became apparent several weeks later when the horny sole, formed prior to the onset of laminitis, had worn off. The superficial sole haemorrhages found at the first post-calving examination could not account for the clinical signs as they were easily removed by paring without alleviating the animals' lameness. This indicated that there was significant
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BRITISH VETERINARY JOURNAL, 152, I
damage deep within the claw. Some of the other animals might have suffered similar pathological changes within their claws without exhibiting clinical signs of laminitis; the stockmen attributed the animals' uneasiness to discomfort related to increased udder size or parturition. Both sole haemorrhages and sole ulceration result from damage to the corium of the claw and are regarded as two phases of the same disease, i.e. laminitis (Nilsson, 1963). At 2 months after calving, all five laminitic heifers had one or other lesion at the predilection site of sole ulceration (transition of zone 3 into zone 4). Also, two of the laminitic heifers had severe haemorrhages or early ulcers in the dorsal part (apex) of the sole (zone 1). These occurred at the same depth as the plantar lesions and probably originated at the same time. The early ulcers resembled severe haemorrhage with both consisting of abnormal horn with incorporated blood. However, the haemorrhages could be removed by paring whereas the ulcers were contiguous ~vith the corium. In the five heifers affected by early sole ulcers, the corium injury had not healed either because the initial damage was more severe or prolonged, or because the corium was less able to resolve the damage in these animals. Although, the distinction between sole haemorrhages and sole ulcers was clear, the aetiology was probably the same. Lameness due to sole lesions commonly occurs in heifers newly introduced to a loose-housing system and into an established herd. Bazeley and Pinsent (1984) reported that the onset of the condition was associated with calving, especially if changes in management occurred at the same time. Others have reported that the onset of the problem was related to housing rather than calving (David, 1986; Colam-Ainsworth et al., 1989; Singh et aL, 1993; Leonard et al., 1994). In all cases, the development of sole lesions was attributed to a reduction in resting (lying) time, with heifers spending most of their time standing and walking on concrete. In this study, varying degrees of haemorrhage were found in the horn of the weight-bearing surface of one or more claws of all newly calved heifers, 4-8 weeks after introduction into the main herd. Haemorrhage in the sole may be a major risk factor in the subsequent occurrence of ulcers and white zone lesions. The frequency distributions of sole haemorrhages in hind and front, and hind lateral and medial claws, found in the present study are consistent with literature observations. Bergsten (1988) reported that haemorrhage scores were higher for hind claws than for front claws. Close examination of Smart's (1986) data, revealed that hind claws had about twice the number of haemorrhages than front claws. In agreement with Peterse (1980) and Bradley et al. (1989), more haemoro rhages were observed in hind lateral claws than in hind medial claws. The distribution of forces on the bovine claw has long been the foundation of theories on the pathogenesis of sole lesions. Scott (1987) studied the variation in load distribution under the claws of Friesian heifers and found that the peak vertical force, expressed as a function of total force produced by the body weight, was significantly higher on front claws than on hind claws. Hind claws carry less than half of the body weight (Scott, 1987). However, judging by the distribution of haemorrhages in the present study, it appears that the main stress was situated in the hind claws. The apparent disparity in haemorrhage distribution between hind and front claws may be attributed to the fact that hind limbs provide thrust to carry the animal forward. Webb & Clark (1981) and Scott (1987) concluded, after
SOLE HAEMORRHAGES IN DAIRY HEIFERS
69
analyzing the horizontal forces in the direction of travel, that greater forces were applied by hind legs than by front legs. A greater horizontal force may cause friction as the animal propels itself forwards and so contributes to the greater number of haemorrhages observed in hind claws. The overall tendency for involvement of the hind lateral claw in the occurrence of sole haemorrhages and sole ulceration is considered to be due to greater and uneven weight-bearing by this claw as opposed to the hind medial claw (Toussaint Raven, 197Ba). Ossent el al. (1987), using a double force plate apparatus, demonstrated that in heifers before calving, weight-bearing in both front and hind limbs was either equally distributed over the lateral and medial claw or more weight was borne on the medial claw. After calving, however, load on the lateral claw was greater than on the medial claw. These authors also tbund that heifers that developed severe lesions in hind lateral claws'2 months after calving had, on average, loaded these claws to a greater degree prior to calving than heifers with none or only minor sole lesions. Therefore, the lateral shift in load-bearing appears to be initiated in the peri-partum a n d / o r early lactation period and it has been suggested that the development of a large and tight udder is a major predisposing factor (Russell el al., 1982). No comparable data could be found in the literature for the distribution of haemorrhages over front lateral and medial claws. The greater number and severity of haemorrhages in front medial claws found in this study may be explained by the greater load being carried on these claws, as suggested by Webb g= Clark (1981). These authors found that, compared with the front lateral claw, a smaller area of the front medial claw was involved in actual load-bearing, resulting in higher pressures in this claw. However, Ossent et aL (1987) and Mair et al. (1988) reported that there was no difference in weight-bearing between front lateral and medial claws. The greater n u m b e r and severity of sole haemorrhages in right claws than in left claws of heifers managed in dry lots is difficult to explain. Only one study could be found on load distribution between right and left claws of cattle (Ossent et al., 1987), which demonstrated that the total load on hind limbs was equally distributed over left and right claws. Differences in friction forces between right and left claws of the heifers managed in dry lots could have occurred during the present stud),. However, different individuals had pared the left and right claws of these heifers and a difference in trimming technique may be a more logical explanation. The n u m b e r and severity of haemorrhages differed between the six zones of the sole. It can be suggested that haemorrhages will occur in those regions of the weight-bearing surface (sole) where most load is being borne, i.e. where highest pressures occur on impact and during limb loading. Pressure plate studies have shown that, in hind as well as front claws, the impact of load is taken by the bulb and the plantar/palmar part of the abaxial border (Webb & Clark, 1981; Mair et aL, 1988). As the cow pushes forwards, the pressure pattern and the animal's weight move forwards along the abaxial wall towards the toe until just the tip of the toe is in contact. The highest pressures occur along the abaxial wall of the claw towards the mid-phase of the step and, to a lesser extent, in both toes at the end of the step (Webb & Clark, 1981). In the present study, these areas were represented
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BRITISH VETERINARY .JOURNAL, 152, 1
by zones 2 and 0, respectively. Ill both groups of heifers, more haemorrhages were recorded in these two zones than in the others. This finding is not consistent with comparable literature observations where the n u m b e r of sole haelnorrhages was lowest in the white zone (zones 2 and 0) and highest in the sole-bulb junction (zone 4) (Peterse, 1980; Bergsten et al., 1986). These apparently conflicting results may be due to differences in haemorrhage evaluation lnethods and confinement of animals. A relatively large ntmaber of haemorrhages were recorded for the bulb region of the weight-bearing surface (zone 5). However, these haemorrhages were never severe. Bulb horn is soft when compared with tile horn of the sole or the abaxial wall (Manson & Leaver, 1988). Furthermore, the papillae of the corium in this region are long and extend far into the horn (Vermunt & Leach, 1999). Therefore, mechanical injury of blood vessels situated in the corium of the bulb can easily occur, especially if undertbot conditions are unyielding a n d / o r rough. For both groups studied, such conditions were present, i.e. concrete slats and a dry or frozen earthen surthce. Total haemorrhage scores for zone 5 were significantly greater in indoor-housed heifers, probably because the relatively restrictive confinement on slats was more injurious to the soft btdb of the claw. Few haemorrhages were recorded for zones 1 and 3. These regions of the sole are generally not involved in weight-bearing, except for zone 1 in the case of excessive weal" of the sole (Toussaint Raven, 1973b). By and large, laaemorrlaages in these zones were probably the restdt of accidental trauma. The two toe ulcers recorded in zone 1 may have been caused by compression of the corium after rotation of the distal phalanx. Phalangeal rotation has been reported in association with laminitis in young cattle (Maclean, 1970; Greenough et al., 1990). The peak in total laaemorrlaage score for zones 2 and 5 observed at the tenth examination prior to calving requires clarification. The tinle-lag between this examination and calving was the equivalent of approximately 9 months. Considering normal rates of horn gl'owth and wear, it may have taken 1-2 months for haemorrhages, occurring in the corium of the sole, to reach the horn surthce. Therefore, the observed haemorrhages probably originated 10-11 months prior to calving. At that time, the heifers were in the breeding group and sexually active. The act of mounting and being mounted greatly increases loading of the hind limbs and this could explain the increase in haemorrhages found in these areas of the sole. However, the peak in total haemorrhage score for zones 2 and 5 was brought about by haemorrhages occurring in hind as well as front claws. There is no information available on a possible hormonal influence on the occurrence of sole haemorrhages, which would affect all claws equally. Such an influence is not likely to exist as it would regularly occur in heifers after puberty. Another, more probable, explanation is an environmental influence; heifers of breeding age were moved from relatively small, inside or outside pens to a larger corral. The surface of this corral was quite rough when compared with the grass-covered or strawbedded pens and was therefore more conducive to mechanical trauma. The high prevalence of sole haemorrhages in indoor-housed heifers, confined on concrete, was expected and agrees with observations in the literature (Bergsten, 1988; Bradley et aL, 1989; Greenough & Vermunt, 1991; Leonard et al., 1994). However, the relatively high prevalence and severity of sole haemorrhages
SOI.E HAEMORRHA(;ES IN DAIRY HEIFERS
71
in heifers managed in dry lots was not anticipated, but could have been nutritionrelated. Tile feeding of barley silage, as practised in this herd, has been implicated in the occurrence of laminitis in dairy heifers (Little & Kay, 1979). Another, more likely explanation is that tile haemorrhages arose as a result of the combined effects of nutrition and certain conditions specifically related to the environment. During the winter, tile earthen surface of the outside corral was frozen and rough; conditions which predisposed to trauma. In addition, heifers managed in dry lots were standing fbr long periods on ice and snow during the winter months. Cattle are well endowed with digital AVAs (Vermunt & Leach, 1992). One of the prime ftmctions of AVAs in the extremities is to provide for local maintenance of temperatnre (Molyneux & Bryden, 1981), and periodic dilation of AVAs may prevent cold-induced trauma of the sensitive digital tissues. However, repeated or prolonged dilation of AVAs may have occurred during periods of extreme cold temperatures. Increased shunting of blood through AVAs may lead to a rise in local venous pressure, spreading to the capillary bed. The capillaries become congested, which can lead to oedema and focal haemorrhages in the capillary beds of the affected tissues. Such haenaorrhages are then incorporated into the horn. Sole haemorrhages obsela'ed in the majority (77%) of the heifers when 12-13 months old were not severe but nevertheless present. At that age, the heifers were led a high-rouglaage diet. Evidence of a link between rapid growth during rearing and the occurrence of haemorrhages associated with laminitis is scarce. Rapid rearing of dairy heiti~rs, resulting in mean body weight gains exceeding 1.0 kg day -I, has been implicated in the occurrence of laminitis (Little & Kay, 1979). Greenough and Vermunt (1991) suggested that a growth rate greater than 0.8 kg da) ,-* was a predisposing factor of laminitis. High planes of nutrition giving these rapid growth rates must involve a low roughage intake, which has been associated with rumen acidosis and laminitis (Livesey & Fleming, 1984). In the present study, no significant correlation was found between accumulated haemorrhage score and weight gains. Tile ADG from birth to breeding of 0.78 kg was in accordance with the recommendations for dairy heifers (Anon, 1981). In conclusion, differences in the number, severity and distribution of sole haemorrhages were found between the two groups of heifers studied. Nutrition had been intentionally kept tile same for both groups and, although a possible effect of the diet on claw health cannot be discounted, the obselwed differences in sole haenlorrhages could .only have been the result of a difference in management. Haemorrhages in the sole are an historic record of an event that did take place some weeks or months prior to the observation, depending on rates of horn growth and wear. Although sole haemorrhages are not pathognomonic for laminitis, they are, at present, the only readily visible sign of early laminitic damage within the claw of a live animal. Thus, recording of sole haemorrhages in a number of cows can be a reliable method to study the prevalence and severity of laminitis within the herd. In an earlier pilot study (Vermunt & Greenough, 1995), sole haemorrhages were found in calves as young as 6-7 months of age. This observation, combined with the present finding of sole haemorrhages in heifers aged 12-13 months and consistently thereafter, indicates that laminitis of varying degrees was a common condition during the growing period of these yotmg cattle and that damage to their claws occurred before they reached maturity. Whatever
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BRITISH VETERINARYJOURN.AL, 152, 1
the cause, such damage, if severe e n o u g h , is likely to have long-lasting conseq u e n c e s for this class o f animal.
ACKNOWLEDGEMENTS T h e a u t h o r s a p p r e c i a t e the help o f Marlene F e h r and the staff at the University o f Saskatchewan Animal Science Dairy Unit. T h a n k s are d u e to Michael O g u n y e l e for his assistance in data collection a n d Juliane D e u b n e r for the illustrations. Sheila M c C o r m a c and Colin Rousseaux assisted with the analysis o f the data. T h e study was f u n d e d , in part, by the Agriculture D e v e l o p m e n t Fund, the Dairy P r o d u c e r s Co-op Ltd a n d the C a n a d i a n Veterinary Research T r u s t Fund.
REFERENCES ANON (1981). Dairy HudJandry in Cattle. Publication No 1439/E, pp. 89. Ottawa: Communications Branch, Agriculture Canada. BARGAI,U., SHAMIR,I., Lt:BLIN,A. & BOG,N, E. (1992). Winter outbreaks of laminitis in daily calves: aetiology and laboratory, radiological and pathological findings. Vetennary Record 131, 411-14. BAZF.t.F.V,It. & PINSENT,P.J.N. (1984). Preliminary observations on a series of outbreaks of acute laminitis in dairy cattle. VeterinaryRecord 115, 619-22. BERGSTEN,C. (1988). Sole bruising as an indicator of laminitis in cattle. A field study. In Proceedings of the XVth World Buiatnrs Congress, pp. 1072-6. Palma de Mallorca. BERGSTEN,C., ANDERSSON,L. & WJK'roRsSON,L. (1986). Effect of feeding intensity at calving on the prevalence of subclinical laminitis. In P~loreeding~of the Vth International S~,mposium on Disorders oft/u, Ruminant Digit, pp. 33-8. Dublin. B~M~LEV,H. K., SHAnnOn, D. & NFH_~ON,D. R. (1989). Subclinical laminitis in dairy heifers. Veterinary Record 125, 177-9. COmM-AINsWORTH, P., LYNN, G. A., THOMAS,R. C. & EDDy, R. G. (1989). Behaviour of cows in cubicles and its possible relationship with laminitis in replacement daily heifers. Veterinar), Records 125, 573-5. DAVID, G. P. (1986). Cattle behaviour and lameness. In Pivceedings of the Vth International Symposium on Disorda~ of the Ruminant Digit, pp. 79-86. Dublin. FRANKENA,K., VAN KEULEN,K. A. S., NOORDHlqZEN,J. P. et al. (1992). A cross-sectional study into prevalence and risk indicators of digital haemorrhages in female daily calves. Preventive Veterinary Medicine 14, 1-12. GREENOUGH,P. R. & VF.RMUNT,J. J. (1990). Evaluation of subclinical laminitis and associated lesions in dairy cattle. In P~aceedings of the Vlth International Symposium on Diseases of the Ruminant Digit, pp. 11-7. Liverpool. GREENOUGH,P. R. & V~'RMUNT,J.J. (1991). Evaluation of subclinical laminitis in a dairy herd and observations on associated nutritional and management factors. Veterinary Record
128, 11-7. GREENOUGH,P. R., VERMUNT,J. J., McKINNON,J. J., FATHV,F. A., BERG,P. A. & CO'IEN, R. D. H. (1990). Laminitis-like changes in the claws of feedlot cattle. Canadian VeterinmyJournal
31,202-8. LEONARD,N., O'CoNNEt.t.,J. & O'F.MtRVLt.,K. (1994). Effect of different housing conditions on behaviour and foot lesions in Friesian heifers. Veterinary Record 134, 490--4. LlYrt.E, W. & KAy, R. M. (1979). The effects of rapid rearing and early calving on the subsequent performance of dairy heifers. Animal Production 29, 131-42. LJVESEV,C. T. & FLEMINt;,F. L. (1984). Nutritional influences on laminitis, sole ulcer and bruised sole in Friesian cows. Veterinary Record 114, 510-12.
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MA(:I.I"-.~N,C. W. (1970). A post-mortem X-ray study of laminitis in barley beef animals. Veteffnary Recm'd86, 457-62. MAIn, A., SrlEI.,X,AS, C., Dtvnscrn,~c., W., Kg:~L'SSI.ICH,H., Grt,,r, F. & Dts'n., O. (1988). Druckverteihmgsmessungen an der Sohlenfliche yon-Rinderklauen---grundlegende Untersuchungen mit einem neuartigen MeBsystem. Deutsche Tierarztliche Wochenschrifl95, 325-8. M.~,uso,~, F.J. & LL-wER,J. D. (1988). The influence of dietary protein intake and of hoof trimming on lameness in dairy cattle. Animal Production 47, 191-9. MoL~.~:t'x, G. S. & BR~I)~:,~, M. M. (1981). Comparative aspects of arteriovenous anastomoses. In Prog~'ess in Anatmny, ed. R. J. Harrison, vol. I, pp. 207-27. Cambridge: Cambridge University Press. Nn.~s()N, S. A. (1963). Clinical, morphological and experimental studies of laminitis in cattle. Acta Veteffnaria Scandinavica 4 (Suppl.), 9-304. Osst.:xr, P., Pv:,'~:a.s~:, D.J. & ScHaxn-,am)r, H. C. (1987). Distribution of load between the lateral and medial hoof of the bovine hind limb. Journal of Veterinary Medicine A $4, 296-300. PF'rVRS~:,D.J. (1979). Nutrition as a possible factor in the pathogenesis of ulcers of the sole in cattle. 7"l~/dschriflvoor Diergeneeskunde 104, 966-70. Pr'.'rl:.asv., D.J. (1980). De beoordeling van de runderklauw op basis van het optreden van zoollaesies. Ph.D. thesis, Rijksuniversiteit Utrecht. RL'SSI-I.I.,A. M., RoWI),NI~S,G.J., SHAW,S. R. & Wv-w~:r, A. D. (1982). Survey of lameness in British dairy cattle. Vetednat3,Record 111, 155--60. Scxna, G. B. (1987). Variation" in load distribution under the hooves of Friesian heifers. In Cattle Housing ,~,stems, Lameness and Behavimo, ed. H. K. Wierenga & D. J. Peterse, pp. 29-36. Boston: Martinus NijhoffPublishers. Si.xca,, S. S., W.-~aD,W. R., L-XCTI.'.XI~ACH,L., Ht'¢mES,J. W. & Mt'RZ-~; R. D. (1993). Behaviour of first lactation and adult dairy cows while housed and at pasture and its relationship with sole lesions. VeterinaryRecord 133, 469-74. S.~tagr, M. E. (1986). Relationship of sub-clinical laminitis and nutrition in dairy cattle: a Canadian experience. In Proceedings of the Vth International Symposium on Disorders of the Ruminant Digit, pp. 51-62. Dublin. Totsg.xtNr R..wF~, E. (1973a). Determination of weight-bearing by the bovine foot. NetherlandsJou rnal of Veteffna~y Science 5, 99-103. Tot'sx.uxr K-wvy, E. (1973b). Lameness in cattle and footcare. Netherlands Journal of Veterinm~ Science5, 105-11. Vt:.axwyr,J~ J. (199(I). Lesions and structural characteristics of the claws of dairy heifers in two management systems. M.Sc. thesis, University of Saskatchewan. VERXlL'NT,J.J. (1992). "Subclinical" laminitis in dairy cattle. New Zealand Veterina~Journal 401 133-8. VERML'N'r,J.J. & LI--~(:H,D. H. (1992). A scanning electron microscopic study of the vascular system of the bovine hind claw. New Zealand VeterinmyJourna140, 146-54. VI-'RML'NT,J. J. & GaE~:NOt't;H,P. R. (1994). Predisposing factors of laminitis in cattle. British Veterina~ Journa1150, 151-64. VvRx~t,,~v,J.J. & GRr.Er~Ot,¢;H,P. R. (1995). Lesions associated with subclinical laminitis of the claws of dairy calves in two management systems. British VeterinaryJournal 151,391-9. Wen~, N. G. & C~.*RK, M. (1981). Livestock foot-floor interactions measured by force and pressure.plate. Farm BuiMing Progress66, 22-36.
(Acreptedfor publication 15 Febnta~y1995)
SOI~
HAEMORRHAGES IN DAIRY I~ERS MANAGED UNDER DIFFERENT UNDERFOOT AND ENVIRONMENTAL CONDITIONS
J . J . VERMUNT* and P. R. G R E E N O U G H
Department of Veterinary Anesthesiology, Radiology and Surgery, Western Collegeof Veterinary Medicine, University of Saskatchewan, Saskatoon, Saskatchewan, Canada S7N OWO
SUMMARY Sole haemorrhages associated with laminitis were studied in 30 Holstein heifers in one herd housed either indoors on concrete or out of doors on a dry lot. Examinations were at 4-week intervals during a 15-month period from approximately 13 months of age to 2 months after calving. At 13 months of age, sole haemorrhages were present in 77% of the heifers. Five heifers, affected by clinical laminitis shortly after calving, developed early sole ulcers. Indoor-housed heifers had a greater n u m b e r of and more severe haemorrhages than heifers managed in dry lots (P<0.001). In both groups, hind claws were more .affected than front claws (P<0.001). Lateral claws were more affected in hind limbs (P<0.001), whereas medial claws had more sole haemorrhages in front limbs (P<0.01). Heifers managed in dry lots had more sole h a e m o r r h a g e s i n right claws than in left claws (P< 0.01). The n u m b e r and severity of haemorrhages differed among the six zones of the sole (P<0.001). Overall, the abaxial white zone (zone 2) had the greatest n u m b e r of haemorrhages, followed by the white zone at the toe (zone 0), the bulb (zone 5) and the sole-bulb junction (zone 4), respectively. Few haemorrhages occurred in the apex of the sole (zone 1) and the axial groove (zone 3). Zone 0 was more severely affected in heifers managed in dry lots (P<0.001), whereas zones 2, 4 and 5 h a d greater numbers of haemorrhages in heifers housed indoors (P<0.01). Time had no effect on total haemorrhages scores, but the effect of m a n a g e m e n t was significant for zones 0 and 5. Total h a e m o r r h a g e scores for zone 0 were greater in heifers managed in dry lots (P<0.05), whereas zone 5 was m o r e affected in indoor-housed heifers (P<0.01). This study shows that sole haemorrhages do occur in the claws of dairy heifers managed either
*To whom correspondence should be addressed at: 12 Park Road, Palmerston North, New Zealand. 0007-1935/96/010057-17/$12.00/0
© 1996 Ballli~re Tindal
BRITISH VETERINARY.]OURN,M.. 152. I
58
indoors or in dry lots, and permanent damage to the claws of these young cattle may already have occurred before they reach maturity. I~..~wom~s: Sole haemorrlaages: laminitis; heifers; management.
INTRODUCTION
In dairying countries worldwide, lameness in cattle is now recognised as a major economic and welfare problem. There is little doubt that (subclinical) laminitis, by affecting horn quality, is a major predisposing factor in the aetiolo~' of lameness caused by claw lesions such as white line (white zone) disease and sole ulcer (Bradley et aL, 1989; Greenough & Vermtmt, 1991). However, the Factors that are important in the aetiology of iaminitis are much less certain. It has been suggested that changes in the micl'o-circulation of the corium (dermis) of the claw contril> ute to the development of laminitis, with arterio-venous anastomoses (AVAs) playing a crucial role (Vermunt, 1999; Vermunt & Leach, 1992). The main factors that are considered to predispose cattle to laminitis have been reviewed recenth' (Vermunt & Greenougla, 1994) and include systemic disease, nutrition, age, growth, housing, bedding, exercise, calving, behaviour and conformation. The predominalat features of laminitis are haemorrhages in the sole and ahnormal horn production (Bradley et aL, 1989; Greenough et al., 1990; Greenough & Vermunt, 1991 ). Most earh' studies on bovine lalninitis and associated lesions have been carried out on adult cattle and slaughterhouse material and, until recently, claw lesions of imnmture dairy cattle received little attention. However, Bradley et al. (1989) and Vermunt (1990) reported sole haemorrhages in the claws of 5-and 6-month-old heifer calves, respectively; Frankena et aL (1992) reported that sole haemorrhages were present in calves as young as 10 weeks of age and found a positive correlation between sole haemorrhages and age. Bargai et al. (1999) reported outbreaks of laminitis and associated sole haentorrhages in cah'es aged 4-6 months. Therefore, there is increasing evidence that damage to the claws of young dairy cattle may already occur before the}' reach maturi W. The aim of the present study was to describe the distribution of sole haemorrhages in dail T heifers between the ages of 13 and 24 months, managed under different underfoot and environmental conditions.
MATERIALS AND METHODS
The study was carried out from January 1989 to April 1990. Heifers were examined every 4 weeks with, in general, claw examinations starting when the animals were approximately 13-months old and finishing 2 months after calving. Some heifers had not yet, or had only recently calved at the end of the study and, therefore, their records were incomplete. Animals
Thirty Holstein heifers, replacements for the dairy herd on the campus of the
SOI.E HAEMORRHAGES IN DAIRY HEIFERS
59
University of Saskatchewan, were used for this study. All animals were raised on the farm.
Management and nutrition Replacement heifers were moved to a breeding group at 12-13 months of age. This group was maintained out of doors on a dry lot with access to a well-bedded shelter. Heifers were artificially inseminated when they reached a body weight of 340 kg or at 15 months of age; they were not bred under 13 months of age. In the breeding group, heifers received 2 kg of a growing heifer concentrate (67% total digestible nutrients (TDN) or 10.21 MJ kg -~, and 14% crude protein (CP) on an 'as fed' basis). Good quality alfalfa hay (90% dry matter, 52% TDN or 9.62 MJ kg-n and 14% CP) was available ad libitum.
7:reatment groups and experimental design Actual treatments were imposed when heifers were diagnosed pregnant (generally 42 days after conception) and continued until 2 weeks prior to their expected calving date. Heifers were randomly allocated to one of two groups a., they became available until a total of 15 animals had been allotted to each group.
Heifers housed indoors. These heifers joined the adult cows in the dry group, housed in a separate area of the free-stall (cubicle) barn. The animals had acces., to cubicles bedded with rubber mats plus a limited a m o u n t of cut straw during the winter months. Approximately two-thirds of the floor area of the alleyways alon8 the cubicles was slatted; the remainder of the floor was solid concrete. Animals in the dry group were fed 1 kg of a dry cow concentrate (fed as a carrier of minerak, and vitamins) and 4 kg chopped, good quality alfalfa hay per day plus barley silag~ to meet their daily energy requirements. The ration was provided as a complet~ mixed diet with an average particle length of 2.5 cm. There was always sufficien~ cubicle and feeding space for all cattle to rest and feed together. Heifers managed in d~), lots. These heifers stayed out of doors for the remainde] of their pregnancy. No mature, dry cows were present in this group and the animals were confined on an earth and gravel-surfaced corral. Straw was used a~ bedding in the shelter. For 4-5 months of the year, the ground surface was frozen often snow-covered or icy, and rather rough. Heifers in this group received the same nutrition on a per head basis as the indoor-housed animals and there wa~ always adequate bunk space. All animals, whether indoor-housed or dry lot, had free access to a commercia 1:1 mineral mix (19% calcium:19% phosphorus) with trace minerals and vitamin: A, D and E. Good quality water was available from drinking bowls at all times. Approximately 14 days prior to their expected calving date, heifers from bott groups were transferred to individual, indoor box-stalls, which were bedded with thick layer of straw. The a m o u n t of concentrate fed was increased by dail' increments so that animals were consuming 2 kg dairy concentrate (71% TDN o: 10.8MJkg-', and 19% CP) plus 2 k g fresh cow concentrate (71% TDN o: 10.8 MJ kg-~, and 18% CP) by the time they calved. After calving, dairy concen trate was increased by 0.5 kg per day and heifers were moved to flae lactating here in the free-stall barn when they were consuming a total of 8 kg dairy concentrat4
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BRITISH VETERINARY .JOURNAL., 152, I
per day. Forage (barley silage and alfalfa hay) was fed at a rate of 1.7% of the average body weight on a dry matter basis. During lactation, cows were offered a semitotal mixed diet and additional concentrate was fed through computerised feeding stalls in order to meet the animals' energy requirement. The dimensions of the cubicles in the free-stall barn were 2.15 m x l . 2 m and the grooved, concrete floor was scraped several times per day.
Evaluation of sole haemorrhages The claws of heifers housed in the free-stall barn were examined using a custom made, hydraulic tilting table. A conventional restraining crush (Superstall II, A.C. Bakx Industries) was used when heifers were housed elsewhere. At each examination, a sliver of horn was pared from the soles of all eight claws to expose fresh horn. Photographs were taken of the trimmed plantar/palmar aspect of the claws and were used for evaluation of haemorrhages in the sole. Haemorrhages were localized as to zone of the sole, n u m b e r e d 0-5 (Greenough & Vermunt, 1990). Zone 0 was a m e n d e d to include the axial white zone at the toe (Fig. 1). The severity of sole haemorrhages was scored by the density and extent of the haemorrhage: no haemorrhage was scored as 0; slight haemorrhage, 1; moderate, 2; marked, 3; severe, 4; exposed corium and associated haemorrhage, 5 (Figs 2-5).
A nimal performance Heifers were weighed at birth, at weekly intervals until weaning at approximately 75 kg of body weight, and once every 4 weeks thereafter. Average daily
Fig. 1. Diagram showing the six zones of the weight-bearing surface ('sole') of the bovine claw. Zone 0, white zone at the toe; zone 1, apex of the sole; zone 2, abaxial white zone including the wall-bulb junction; zone 3, axial groove; zone 4, sole-bulb junction; and zone 5, bulb.
SOLE HAEMORRHAGES IN DAIRY HEIFERS
Fig. 9
Fig. S
Fig. 4
Fig. 5
61
Fig. 2. Moderate (score 2) haemorrhage in zone 0 of the left hind lateral claw and slight (score 1) haemorrhage in zone 4 of the left hind medial claw. Fig. 3.
Marked (score 3) haemorrhage in zone 2 of the left hind lateral claw.
Fig. 4. Severe (score 4) haemorrhage in zone 9, moderate (score 9) haemorrhage in zone 1 and slight (score 1) haemorrhage in zone 4 of the left hind lateral claw. Note the haemorrhage that can be seen only as a blue tinge, deep within the horn in zone 3 of the same claw. Fig. 5. Severe (score 4) haemorrhage at the transition of zone 3 into zone 4 of the right h i n d lateral claw; moderate (score 9) haemorrhage in zones 2 and 5 o f the same claw.
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weight gain (ADG) from birth .40 breeding, from birth to calving, and from breeding to calving was calculated.
Statistical analysis All data were analyzed using SAS (Statistical Analysis System, SAS Institute Inc.). Eleven heifers in each group had at least one post-calving examination, whereas seven and eight animals from the 'indoors' and 'dry lot' group, respectively, had two examinations after calving.
Descriptive analysis. Differences in the n u m b e r and severity of haemorrhage scores between groups, between left and right, hind and front, and lateral and medial claws, and between the zones of the sole was analyzed using the Chi-square test. This test was also used to compare the prevalence of sole ulceration between the two groups. A non-parametric one-way analysis of variance (ANOVA), the Kruskal-Wallis H test, was used to test for differences between claws for each zone and for differences between zones within each claw. Correlation coefficients between accumulated haemorrhage scores (scores 0-5x8 clawsx6 zones; theoretical range 0 to 240) and weight gains were calculated using Pearson's correlation analysis. Comparative analysis. The data, collected from repeated observations over time on the same experimental units (i.e. heifers), were also analyzed by repeated measures ANOVA. Total haemorrhage scores for each of the six zones of the sole were obtained by summing the scores in all eight claws for each examination (theoretical range of 0 to 40). Means of total haemorrhage scores for the different examinations were separated using the General Linear Models (GLM) procedure of SAS and comparisons among these means were carried out using Scheffe's Sprocedure. Factors of interest were time and treatment (management group), and their effects were analyzed, using the F-statistic, for the actual treatment period, i.e. from entry into the respective group through to calving (examinations - 7 to 0). RESULTS
Haemorrhages in the sole At the first examination at approximately 13 months of age, 77% of the heifers had sole haemorrhages in one or more claws. These haemorrhages were on the surface and could be pared out. Before calving, no haemorrhages with a score greater than 3 were recorded for any of the six zones of the sole and no haemorrhages with a score of 5 were observed during the entire study. Haemorrhage scores ranged from 0-3 for zones 0 and 5, whereas zones 1, 2, 3 and 4 had scores varying from 0 to 4. At the first post-partum examination, sole haemorrhages were present in five heifers affected by clinical laminitis. In some cases, haemorrhage was seen as a blue tinge, deep within the sole horn (Fig. 4). When re-examined at the last examination, approximately 2 months after calving, the condition had worsened. Severe haemorrhage or early sole ulceration had developed at the transition of
SOLE HAEMORRHAGES IN DAIRY HEIFERS
63
INDOORS
~
LFL
LFM
RFM
RFL
LHL
LHM
RHM
RHL
<0.1
[]
0.5
0x 6~ @ 03
I I 06 m 07 D 06
I
I I ,06
0,
LFL, leftfront lateral; LFM, leftfront medial; RFM, right front medial; RFL, right front lateral; LHL, lefthind lateral; LHM, lefthind medial; RHM, right hind medial; RHL, right hind lateral.
Fig. 6. Illustration of mean haemorrhage scores (0-5; n=204) fOl"the six zones of the sole in the frout and hind limb claws of heifers housed indoors.
z o n e 3 into z o n e 4 (Fig. 5) in o n e o r b o t h h i n d lateral claws o f t h r e e heifers f r o m the i n d o o r - h o u s e d g r o u p a n d two heifers f r o m the g r o u p m a n a g e d in dry lots (P>0.05). T o e ulcers were r e c o r d e d for o n e heifer in each group; b o t h animals h a d b e e n affected by clinical laminitis and also had early sole ulcers. Mean h a e m o r r h a g e scores for the two g r o u p s o f heifers are illustrated in Figs 6 a n d 7. Overall, i n d o o r - h o u s e d heifers h a d a g r e a t e r n u m b e r of, a n d m o r e severe, sole h a e m o r r h a g e s than heifers m a n a g e d in dry lots (P<0.001). In h i n d claws, the n u m b e r and severity o f h a e m o r r h a g e s were g r e a t e r in i n d o o r - h o u s e d heifers
64
BRITISH VETERINARY.JOURNAL, 152, I DRY LOT
LFL
LFM
RFM
RFL
LHL
LHM
RHM
RHL
~<0.1
~
R o.~
m o.,
0.2
@ o.~ m o.~
0.5
_____ o.7
~ o., m ~o.,
LFL, leftfront lateral; LFM, leftfront medial; RFM, right front medial; RFL, right front lateral; LHL, lefthind lateral; LHM, lefthind medial; RHM, right hind medial; RI-IL,right hind lateral.
Fig. 7. Illustration of mean haemorrhage scores (0-5; n=199) for the six zones of the sole in the front and hind limb claws of heifers managed in dry lots. (P
SOLE HAEMORRHAGES IN DAIRY HEIFERS
65
Table I Frequency distribution (%) of sole haemorrhage scores for heifers (n=30) either housed indoors or managed in dry lots (examined from 13 months o f age to 2 months after calving) Indoors (9792 Left Right Front Hind Lateral Medial
Scow 0
Score 1
Score 2
Score 3
Score 4
(I -4) *
%
scores) 39.11 38.34 42.06 35.39 37.17 40.28
8.37 8.86 6.50 10.74 9.63 7.61
2.18 2.35 1.25 3.28 2.66 1.87
0.29 0.44 0.18 0.54 0.49 0.23
0.05 0.01 0.01 0.05 0.05 0.01
10.89 11.66 7.94 a 14.61" 12.83" 9.72"
50 50 50 50 50 50
7.02 8.02 5.79 9.25 8.31 6.73
1.83 2.35 1.61 2.56 2.43 1.75
0.30 0.51 0.36 0.46 0.48 0.34
0.01 0.03 0.00 0.04 0.03 0.01
9.17" 10.91" 7.76" 12.32" 11.25" 8.83"
50 50 50 50 50 50
Dry lot (9552 scores) Left 40.83 Right 39.09 Front 42.24 Hind 37.68 Lateral 38.75 Medial 41.17
*Within this column and hetween claw pairs (left remus right, front versus hind, or lateral versus medial); percentages with identical letters are significantly different; ("P<0.001).
Table II Frequency distribution (%) o f sole haemorrhage scores for front and hind limb claws o f heifers (n=30) housed either indoors or managed in dry lots (examined from 13 months of age to 2 months after calving) F~vnt claws
Hind claws
Score 0
Scores (1-4) *
Score 0
Scores (1-4) *
Indoors (4896 scores) Left Righ t
42.30 41.83
7.70 8.17
35.93 34.84
14.07 15.16
Dry lot (4766 scores) Left Right
43.13 41.35
6.87" 8.65"
38.53 36.83
13.17h
Indoors Lateral Medial
43.12 41.01
6.88" 8.99"
31.23 39.54
18.77" 10.46"
Dry lot Lateral Medial
42.96 41.52
7.04 b 8.48 h
34.53 40.83
15.47;' 9.17"
11.47h
*Within these columns and groups (indoors or dry lot), and between claw pairs (left versus right, fi'ont versus hind, or lateral versus medial); percentages with identical letters are sigqificantly differe,at; ("P<0.001; bP<0.01).
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BRITISH VETERINARY.JOURNAL. 152. I
Table III Frequency distribution (%) o f haemorrhage scores (1-4 combined) for the six zones of the sole in heifers (n=30) housed either indoors or managed in dry lots (examined from 13 months of age to 2 months after calving) All claws
Front claw.~
Hind claws
Zone 0 (3224 scores) Indoors Dry lot
13.52 17.00"
9.68 12.41 h
17.37 21.59"
Zone 1 (3224 scores) Indoors D~y lot
3.41 3.(}7
1.74 2.54
5.09' 3.60
Zone 2 (3224 scores) Indoors Dr}, lot
24.53 22.53
17.99 19.98'
31.08" 24.94
Zone 3 (3224 scores) Indoors Dry lot
1.61 1.40
0.74 1.12
2.48 1.67
Zone 4 (3224 scores) Indoors Dry lot
10. I I" 7.26
4.96h 2.98
15.26 h I 1.54
Zone 5 (3224 scores) Indoors Dry lot
15.29" 8.31
13.09" 6.95
17.49" 9.68
"P<0.001; hP
h a e m o r r h a g e s than h i n d medial claws (P<0.001). Heifers m a n a g e d in dry lots had m o r e h a e m o r r h a g e s in right h i n d claws than in left h i n d claws (P<0.01); the h a e m o r r h a g e s were also m o r e severe (P<0.05). In these heifers, m o r e h a e m o r rhages o f g r e a t e r severity were also r e c o r d e d for right fi'ont claws c o m p a r e d with left f r o n t claws (P<0.001). T h e r e were no differences in the nunaber a n d severity o f h a e m o r r h a g e s between right and left fi'ont claws o f heifers h o u s e d i n d o o r s (P>0.05). H a e m o r r b a g e s r e c o r d e d in right h i n d claws o f these animals were m o r e severe (P<0.05), but not g r e a t e r in n u m b e r (P>0.05), when c o m p a r e d with left h i n d claws. F r e q u e n c y distributions o f h a e m o r r h a g e scores for the six zones o f the sole are p r e s e n t e d in Table III. For all (front a n d hind) claws c o m b i n e d , there were a g r e a t e r n u m b e r of, and m o r e severe, h a e m o r r h a g e s in z o n e 0 in heifers m a n a g e d in dry lots (P<0.001). T h e n u m b e r and severity o f h a e m o r r h a g e s in zones 1, 2 and 3 did not differ between the two g r o u p s (/:'>0.05). I n d o o r - h o u s e d heifers had a g r e a t e r n u m b e r o f h a e m o r r h a g e s in zones 4 a n d 5 (P<0.001). T h e s e heifers also h a d m o r e severe h a e m o r r h a g e s in z o n e 4 (P<0.01) and z o n e 5 (P<0.001). In f r o n t claws, t h e r e were n o differences in n u m b e r a n d severity o f b a e m o r r h a g e s in zones 1 a n d 3. Heifers m a n a g e d in dry lots h a d m o r e h a e m o r r h a g e s o f g r e a t e r severity in z o n e 0 (P<0.01) a n d z o n e 2 (P<0.05). I n d o o r - h o u s e d heifers h a d m o r e h a e m o r rhages o f g r e a t e r severity in zone 4 (P<0.01) a n d z o n e 5 (P<0.001). In h i n d claws,
SOLE HAEMORRHAGES IN DAIRY HEIFERS
67
there were no differences in number and severity of haemorrhages in zone 3. Heifers managed in dry lots had a greater number of, and more severe, haemorrhages in zone 0 (P<0.001). Indoor-housed heifers had more haemorrhages of greater severity in zones 2 and 5 (P<0.001). Also, there were more haemorrhages (P<0.01) of greater severity (P<0.05) in zone 4 in heifers housed indoors. Haemorrhage scores for the six zones of the sole were also compared between left and right, front and hind, lateral and medial, and front and hind lateral and medial claws for each group separately. Indoor-housed heifers had more haemorrhages in zone 4 of right claws compared with left claws (P<0.01). Heifers managed in dry lots had more haemorrhages in zones 0 and 4 of right claws (P<0.001). In both groups, there were more haemorrhages in zones 0, 2, 4 and 5 of hind claws compared with front claws (P<0.001). In indoor-housed heifers, zones 2 and 5 of front medial claws had more haemorrhages compared with front lateral claws (P<0.001). In heifers managed in dry lots, only zone 2 had more haemorrhages in front medial claws (P<0.001). In both groups, all zones had more haemorrhages in hind lateral claws than in hind medial claws; the difference being least significant for zone 0. Relatively few haemorrhages occurred in zones 1 and 3 compared with the other four zones of the sole. Overall, zones 2 and 5 had a peak in total haemorrhage score at the tenth examination before calving. After calving, there was an increase in total haemorrhage scores for most of the six zones (P<0.05), except for zones 3 and 5. The repeated measures ANOVA for examinations -7 to 0 revealed that, for all six zones, time effects were not significant for total haemorrhage scores. However, there were significant treatment (management) effects of total haemorrhage scores in zones 0 and 5. Heifers managed in dry lots had greater total haemorrhage scores for zone 0 (P<0.05); indoor-housed heifers scored higher for zone 5 (P<0.01). There was no significant time by treatment interaction.
Animal performance For both groups, ADG from birth to breeding was 0.78 kg. From breeding to calving, ADG of heifers housed indoors was 0.83 kg and for heifers managed in dry lots ADG was 0.89 kg. Their respective ADG from birth to calving was 0.80 and 0.83 kg. No significant correlations were found between accumulated haemorrhage scores and average daily gains.
DISCUSSION Sole haemorrhages as recorded in the present study have been described in the literature as signs of snbclinical laminitis (Peterse, 1979; Bradley et aL, 1989; Greenough & Vermunt, 1991). The heifers affected by clinical laminitis in the early post-partum period presented a characteristic picture. The severe haemorrhages associated with the laminitic insult only became apparent several weeks later when the horny sole, formed prior to the onset of laminitis, had worn off. The superficial sole haemorrhages found at the first post-calving examination could not account for the clinical signs as they were easily removed by paring without alleviating the animals' lameness. This indicated that there was significant
68
BRITISH VETERINARY JOURNAL, 152, I
damage deep within the claw. Some of the other animals might have suffered similar pathological changes within their claws without exhibiting clinical signs of laminitis; the stockmen attributed the animals' uneasiness to discomfort related to increased udder size or parturition. Both sole haemorrhages and sole ulceration result from damage to the corium of the claw and are regarded as two phases of the same disease, i.e. laminitis (Nilsson, 1963). At 2 months after calving, all five laminitic heifers had one or other lesion at the predilection site of sole ulceration (transition of zone 3 into zone 4). Also, two of the laminitic heifers had severe haemorrhages or early ulcers in the dorsal part (apex) of the sole (zone 1). These occurred at the same depth as the plantar lesions and probably originated at the same time. The early ulcers resembled severe haemorrhage with both consisting of abnormal horn with incorporated blood. However, the haemorrhages could be removed by paring whereas the ulcers were contiguous ~vith the corium. In the five heifers affected by early sole ulcers, the corium injury had not healed either because the initial damage was more severe or prolonged, or because the corium was less able to resolve the damage in these animals. Although, the distinction between sole haemorrhages and sole ulcers was clear, the aetiology was probably the same. Lameness due to sole lesions commonly occurs in heifers newly introduced to a loose-housing system and into an established herd. Bazeley and Pinsent (1984) reported that the onset of the condition was associated with calving, especially if changes in management occurred at the same time. Others have reported that the onset of the problem was related to housing rather than calving (David, 1986; Colam-Ainsworth et al., 1989; Singh et aL, 1993; Leonard et al., 1994). In all cases, the development of sole lesions was attributed to a reduction in resting (lying) time, with heifers spending most of their time standing and walking on concrete. In this study, varying degrees of haemorrhage were found in the horn of the weight-bearing surface of one or more claws of all newly calved heifers, 4-8 weeks after introduction into the main herd. Haemorrhage in the sole may be a major risk factor in the subsequent occurrence of ulcers and white zone lesions. The frequency distributions of sole haemorrhages in hind and front, and hind lateral and medial claws, found in the present study are consistent with literature observations. Bergsten (1988) reported that haemorrhage scores were higher for hind claws than for front claws. Close examination of Smart's (1986) data, revealed that hind claws had about twice the number of haemorrhages than front claws. In agreement with Peterse (1980) and Bradley et al. (1989), more haemoro rhages were observed in hind lateral claws than in hind medial claws. The distribution of forces on the bovine claw has long been the foundation of theories on the pathogenesis of sole lesions. Scott (1987) studied the variation in load distribution under the claws of Friesian heifers and found that the peak vertical force, expressed as a function of total force produced by the body weight, was significantly higher on front claws than on hind claws. Hind claws carry less than half of the body weight (Scott, 1987). However, judging by the distribution of haemorrhages in the present study, it appears that the main stress was situated in the hind claws. The apparent disparity in haemorrhage distribution between hind and front claws may be attributed to the fact that hind limbs provide thrust to carry the animal forward. Webb & Clark (1981) and Scott (1987) concluded, after
SOLE HAEMORRHAGES IN DAIRY HEIFERS
69
analyzing the horizontal forces in the direction of travel, that greater forces were applied by hind legs than by front legs. A greater horizontal force may cause friction as the animal propels itself forwards and so contributes to the greater number of haemorrhages observed in hind claws. The overall tendency for involvement of the hind lateral claw in the occurrence of sole haemorrhages and sole ulceration is considered to be due to greater and uneven weight-bearing by this claw as opposed to the hind medial claw (Toussaint Raven, 197Ba). Ossent el al. (1987), using a double force plate apparatus, demonstrated that in heifers before calving, weight-bearing in both front and hind limbs was either equally distributed over the lateral and medial claw or more weight was borne on the medial claw. After calving, however, load on the lateral claw was greater than on the medial claw. These authors also tbund that heifers that developed severe lesions in hind lateral claws'2 months after calving had, on average, loaded these claws to a greater degree prior to calving than heifers with none or only minor sole lesions. Therefore, the lateral shift in load-bearing appears to be initiated in the peri-partum a n d / o r early lactation period and it has been suggested that the development of a large and tight udder is a major predisposing factor (Russell el al., 1982). No comparable data could be found in the literature for the distribution of haemorrhages over front lateral and medial claws. The greater number and severity of haemorrhages in front medial claws found in this study may be explained by the greater load being carried on these claws, as suggested by Webb g= Clark (1981). These authors found that, compared with the front lateral claw, a smaller area of the front medial claw was involved in actual load-bearing, resulting in higher pressures in this claw. However, Ossent et aL (1987) and Mair et al. (1988) reported that there was no difference in weight-bearing between front lateral and medial claws. The greater n u m b e r and severity of sole haemorrhages in right claws than in left claws of heifers managed in dry lots is difficult to explain. Only one study could be found on load distribution between right and left claws of cattle (Ossent et al., 1987), which demonstrated that the total load on hind limbs was equally distributed over left and right claws. Differences in friction forces between right and left claws of the heifers managed in dry lots could have occurred during the present stud),. However, different individuals had pared the left and right claws of these heifers and a difference in trimming technique may be a more logical explanation. The n u m b e r and severity of haemorrhages differed between the six zones of the sole. It can be suggested that haemorrhages will occur in those regions of the weight-bearing surface (sole) where most load is being borne, i.e. where highest pressures occur on impact and during limb loading. Pressure plate studies have shown that, in hind as well as front claws, the impact of load is taken by the bulb and the plantar/palmar part of the abaxial border (Webb & Clark, 1981; Mair et aL, 1988). As the cow pushes forwards, the pressure pattern and the animal's weight move forwards along the abaxial wall towards the toe until just the tip of the toe is in contact. The highest pressures occur along the abaxial wall of the claw towards the mid-phase of the step and, to a lesser extent, in both toes at the end of the step (Webb & Clark, 1981). In the present study, these areas were represented
711
BRITISH VETERINARY .JOURNAL, 152, 1
by zones 2 and 0, respectively. Ill both groups of heifers, more haemorrhages were recorded in these two zones than in the others. This finding is not consistent with comparable literature observations where the n u m b e r of sole haelnorrhages was lowest in the white zone (zones 2 and 0) and highest in the sole-bulb junction (zone 4) (Peterse, 1980; Bergsten et al., 1986). These apparently conflicting results may be due to differences in haemorrhage evaluation lnethods and confinement of animals. A relatively large ntmaber of haemorrhages were recorded for the bulb region of the weight-bearing surface (zone 5). However, these haemorrhages were never severe. Bulb horn is soft when compared with tile horn of the sole or the abaxial wall (Manson & Leaver, 1988). Furthermore, the papillae of the corium in this region are long and extend far into the horn (Vermunt & Leach, 1999). Therefore, mechanical injury of blood vessels situated in the corium of the bulb can easily occur, especially if undertbot conditions are unyielding a n d / o r rough. For both groups studied, such conditions were present, i.e. concrete slats and a dry or frozen earthen surthce. Total haemorrhage scores for zone 5 were significantly greater in indoor-housed heifers, probably because the relatively restrictive confinement on slats was more injurious to the soft btdb of the claw. Few haemorrhages were recorded for zones 1 and 3. These regions of the sole are generally not involved in weight-bearing, except for zone 1 in the case of excessive weal" of the sole (Toussaint Raven, 1973b). By and large, laaemorrlaages in these zones were probably the restdt of accidental trauma. The two toe ulcers recorded in zone 1 may have been caused by compression of the corium after rotation of the distal phalanx. Phalangeal rotation has been reported in association with laminitis in young cattle (Maclean, 1970; Greenough et al., 1990). The peak in total laaemorrlaage score for zones 2 and 5 observed at the tenth examination prior to calving requires clarification. The tinle-lag between this examination and calving was the equivalent of approximately 9 months. Considering normal rates of horn gl'owth and wear, it may have taken 1-2 months for haemorrhages, occurring in the corium of the sole, to reach the horn surthce. Therefore, the observed haemorrhages probably originated 10-11 months prior to calving. At that time, the heifers were in the breeding group and sexually active. The act of mounting and being mounted greatly increases loading of the hind limbs and this could explain the increase in haemorrhages found in these areas of the sole. However, the peak in total haemorrhage score for zones 2 and 5 was brought about by haemorrhages occurring in hind as well as front claws. There is no information available on a possible hormonal influence on the occurrence of sole haemorrhages, which would affect all claws equally. Such an influence is not likely to exist as it would regularly occur in heifers after puberty. Another, more probable, explanation is an environmental influence; heifers of breeding age were moved from relatively small, inside or outside pens to a larger corral. The surface of this corral was quite rough when compared with the grass-covered or strawbedded pens and was therefore more conducive to mechanical trauma. The high prevalence of sole haemorrhages in indoor-housed heifers, confined on concrete, was expected and agrees with observations in the literature (Bergsten, 1988; Bradley et aL, 1989; Greenough & Vermunt, 1991; Leonard et al., 1994). However, the relatively high prevalence and severity of sole haemorrhages
SOI.E HAEMORRHA(;ES IN DAIRY HEIFERS
71
in heifers managed in dry lots was not anticipated, but could have been nutritionrelated. Tile feeding of barley silage, as practised in this herd, has been implicated in the occurrence of laminitis in dairy heifers (Little & Kay, 1979). Another, more likely explanation is that tile haemorrhages arose as a result of the combined effects of nutrition and certain conditions specifically related to the environment. During the winter, tile earthen surface of the outside corral was frozen and rough; conditions which predisposed to trauma. In addition, heifers managed in dry lots were standing fbr long periods on ice and snow during the winter months. Cattle are well endowed with digital AVAs (Vermunt & Leach, 1992). One of the prime ftmctions of AVAs in the extremities is to provide for local maintenance of temperatnre (Molyneux & Bryden, 1981), and periodic dilation of AVAs may prevent cold-induced trauma of the sensitive digital tissues. However, repeated or prolonged dilation of AVAs may have occurred during periods of extreme cold temperatures. Increased shunting of blood through AVAs may lead to a rise in local venous pressure, spreading to the capillary bed. The capillaries become congested, which can lead to oedema and focal haemorrhages in the capillary beds of the affected tissues. Such haenaorrhages are then incorporated into the horn. Sole haemorrhages obsela'ed in the majority (77%) of the heifers when 12-13 months old were not severe but nevertheless present. At that age, the heifers were led a high-rouglaage diet. Evidence of a link between rapid growth during rearing and the occurrence of haemorrhages associated with laminitis is scarce. Rapid rearing of dairy heiti~rs, resulting in mean body weight gains exceeding 1.0 kg day -I, has been implicated in the occurrence of laminitis (Little & Kay, 1979). Greenough and Vermunt (1991) suggested that a growth rate greater than 0.8 kg da) ,-* was a predisposing factor of laminitis. High planes of nutrition giving these rapid growth rates must involve a low roughage intake, which has been associated with rumen acidosis and laminitis (Livesey & Fleming, 1984). In the present study, no significant correlation was found between accumulated haemorrhage score and weight gains. Tile ADG from birth to breeding of 0.78 kg was in accordance with the recommendations for dairy heifers (Anon, 1981). In conclusion, differences in the number, severity and distribution of sole haemorrhages were found between the two groups of heifers studied. Nutrition had been intentionally kept tile same for both groups and, although a possible effect of the diet on claw health cannot be discounted, the obselwed differences in sole haenlorrhages could .only have been the result of a difference in management. Haemorrhages in the sole are an historic record of an event that did take place some weeks or months prior to the observation, depending on rates of horn growth and wear. Although sole haemorrhages are not pathognomonic for laminitis, they are, at present, the only readily visible sign of early laminitic damage within the claw of a live animal. Thus, recording of sole haemorrhages in a number of cows can be a reliable method to study the prevalence and severity of laminitis within the herd. In an earlier pilot study (Vermunt & Greenough, 1995), sole haemorrhages were found in calves as young as 6-7 months of age. This observation, combined with the present finding of sole haemorrhages in heifers aged 12-13 months and consistently thereafter, indicates that laminitis of varying degrees was a common condition during the growing period of these yotmg cattle and that damage to their claws occurred before they reached maturity. Whatever
72
BRITISH VETERINARYJOURN.AL, 152, 1
the cause, such damage, if severe e n o u g h , is likely to have long-lasting conseq u e n c e s for this class o f animal.
ACKNOWLEDGEMENTS T h e a u t h o r s a p p r e c i a t e the help o f Marlene F e h r and the staff at the University o f Saskatchewan Animal Science Dairy Unit. T h a n k s are d u e to Michael O g u n y e l e for his assistance in data collection a n d Juliane D e u b n e r for the illustrations. Sheila M c C o r m a c and Colin Rousseaux assisted with the analysis o f the data. T h e study was f u n d e d , in part, by the Agriculture D e v e l o p m e n t Fund, the Dairy P r o d u c e r s Co-op Ltd a n d the C a n a d i a n Veterinary Research T r u s t Fund.
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(Acreptedfor publication 15 Febnta~y1995)