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Effect of different energy and protein levels on leg weakness and osteochondrosis in pigs
LlIVFiSTOCK pRmErN
ELSEVIER
Livestock Production
Science 41 (1995)
171-181
Effect of different energy and protein levels on leg weakness and osteochondrosis in pigs Bente J@rgensen* National institute of Animal Science, Research Centre Foulum, P.O. Box 39, DK 8830 Tjele, Denmark Accepted 7
June 1994
Abstract The effects of energy level, protein level, and sex on leg weakness and osteochondrosis in slaughter pigs were studied, and correlations between these traits were estimated. The experiment consisted of 300 crossbred castrates and gilts, fed either restricted or ad libitum on three different levels of protein. The pigs were scored for 14 different leg weakness traits and the elbow and stifle joints were scored for osteochondrosis after slaughter. Energy level affected three of the leg weakness traits and the ‘total leg weakness score’ in the same direction: pigs fed ad libitum showed more pronounced problems than pigs in the restricted groups. There was no effect of energy level on osteochondrosis. Protein level and sex did neither affect leg weakness nor osteochondrosis. Osteochondral lesions in the medial humeral condyle were correlated with changes in the proximal radius: proximal edge of radius (I-= 0.17, P < 0.05) and synovial fossa of radius (r= 0.28, P
1. Introduction Leg weakness is one of the major reasons for lameness leading to culling in gilts, sows, and boars. The term leg weakness is used to describe a syndrome characterized by changes in leg position and abnormal locomotion. Genetic predisposition as well as selection for production traits such as high growth rate and meat content are found to cause leg weakness problems (Bereskin, 1979; Webb et al., 1983; Lundeheim, 1987; Rothschild et al., 1988; Jorgensen and Vestergaard, 1990). Furthermore, feeding high energy levels appears to predispose for leg weakness in pigs *Corresponding
author.
0301-6226/95/$09.50 0 1995Blsevier Science B.V. All rights reserved SSDIO301-6226(94)00048-C
(Grondalen, 1974~; Hanssen and Grondalen, 1979; Wilson et al., 1980; Sorensen et al., 1993). The protein level does not seem to affect leg soundness (Grondalen, 1974~; Hanssen and Grondalen, 1979; Reiland, 1978b). The etiology of leg weakness is by many researchers considered to be osteochondrosis, a generalized disturbance of the enchondral ossification as well in the joint cartilage as in the growth plates (Duthie and Lancaster, 1964; Grondalen, 1974a; Reiland, 1978a; Goedegebuure et al., 1980; Lundeheim, 1987; Nakano et al., 1987)) while others do not find a relationship between leg weakness and osteochondrosis (Thurley, 1969; Grondalen, 1974~; Empel, 1980; Goedegebuure et al., 1988).
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B. J@rgensen /Livestock
Production Science 41(1995)
The objective of this study was to evaluate the effect of energy and protein levels on leg weakness symptoms and osteochondrosis in slaughter pigs. Furthermore, the aim was to test for sex differences in these traits and finally to estimate the correlations between leg weakness symptoms and osteochondrosis.
2. Material and methods A total of 300 pigs - from 60 Yorkshire * Danish Landrace litters (30 litters of 5 castrates and 30 litters of 5 gilts) - were allocated to five groups and fed three different energy levels (ad libitum and according to either Norwegian or Danish recommandation (Table 1)) and three levels of protein within the ad libitum regime (Table 2). The experiment consisted of three batches of 100 pigs (ten in each group of each sex), fed from 25-100 kg and housed in individual pens on concrete floor with bedding. The composition of the experimental diets is listed in Table 2. There was 7.0 g Ca and 5.5 g P per kg diet. The pigs were judged clinically for leg weakness problems the week before slaughter. Judgment was done using a scale from 1 (normal) to 4 (very severe changes) (Jorgensen and Vestergaard, 1990). After slaughter, the elbow and stifle joints from the same side were inspected macroscopically for osteochondral and other changes at the intact surface. These were all scored on a scale from 1 (normal) to 5 (osteochondritis dissecans) . The following joint changes were scored: Medial and lateral humeral condyles, medial femoral condyle, and articular surface of the anconeal process of ulna (invaginations, grooves or defects in the joint cartilage, 5 = osteochondritis dissecans) (Fig. 1 and Fig. 3) ; proximal edge of radius (thinning of cartilage and/or bony depression of the crania-medial edge) (Fig. 2) ; synovial fossa of proximal radius (enlarged depression in the articular surface of radius) (Fig. 2). All judgments were made by the author without knowledge of treatment group or sex, and evaluation of joint lesions without knowledge of the results of the clinical examination. The effect of energy level, protein level, and sex on performance, leg weakness traits, and osteochondrosis was tested using the following univariate model: Kjklm = p+ti
+Sj
+6,+Lj,l
+eijklm
(1)
171-181
where Yijumis the observation of leg weakness trait or osteochondrosis of the mth pig on treatment group i of sex j in the kth batch from litter 1; p is the mean; ti is the fixed effect of treatment group (i = 1,2,3,4,5) ; Sj is the fixed effect of sex (j is castrate or gilt); 6, is the fixed effect of batch; Ljkl is the random effect of litter within sex and batch, N(O,Iai;) eijam is the random residual effects, N(O,IU’) . The effect of sex was tested by using litter within sex and batch as the appropriate error term. Preliminary analysis showed no differences in leg weakness and osteochondrosis between the Norwegian and the Danish recommendations, therefore these treatment groups were combined into one (control). Effect of energy level was tested at the same level of protein (standard) as the contrast between treatment group 1 + 5 (control) and 3 (ad libitum) . Effect of protein was tested at the same energy level (ad libitum) as the contrast between treatment groups 2, 3, and 4. Only variables with a total prevalence of scores (2, 3, 4) > 10% were analysed, because of non-normal distribution of the data (Weeb et al., 1983; Jorgensen and Vestergaard, 1990). Interaction terms were found nonsignificant in most analyses and deleted from the model when possible. PROC GLM in SAS was used (SAS Institute Inc., 1988). Due to missing values for some pigs the number of pigs used in the analyses was 257. Correlation coefficients ( ryx) between leg weakness traits (n) and changes in the joints (y) were estimated as follows: Cov(x,y) ‘Y”
=
2 2 (+y (+x
where Cov (xv) =
CLyx
+
Gyx
and U; = crz + uf a2=&+(+2 x
ex*
(&, c&, u&, and ~2~ are the litter and residual variances of trait y and trait x, respectively.) us and as are estimated using Henderson Method 3 (Henderson, 1953). MS(L) and MS(e) are obtained from the GLM procedure (MANOVA) in SAS using model ( 1). The significance levels of r were found by simulating a data set where the Yand X values are calculated using pseudo-random variables with Lju distributed
B. Jergensen /Livestock Production Science 4I (1995) 171-181 Table I Danish and Norwegian
recommendations
Weight (kg) Danish, kg/day Norwegian, kg/day
Table 2 Composition
30 1.5 1.3
of the experimental
173
on net energy for slaughter pigs 40 1.9 1.6
50 2.2 1.9
60 2.5 2.3
70 2.7 2.6
80 2.8 2.9
90 2.8 3.2
100 2.8 3.2
diets, per cent 2060
kg
60-100 kg
Treatment group
1+3+5
2
4
1+3+5
2
4
Soybean meal Barley Wheat Oats Minerals and vitamins FU per kg g digestible crude protein/FE,
25.0 50.6 10.9 10.9 2.6 1.00 153
20.5 53.9 11.5 11.5 2.6 0.99 141
30.0 47.2 10.1 10.1 2.6 1.01 167
18.0 55.6 11.9 11.9 2.6 0.99 134
13.0 59.0 12.7 12.7 2.6 0.98 120
22.5 52.5 11.2 Il.2 2.6 1.00 146
Treatment group I is fed according to the Norwegian rec. at standard protein level. Treatment groups 2, 3, and 4 are fed ad libitum at low, standard, and high protein level. Treatment group 5 is fed according to the Danish rec. at standard protein level.
Fig. 1. Osteochondritis
dissecans
(score 5) in the anconeal process of ulna.
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B. Jergensen /Livestock Production Science 41 (1995) 171-181
Fig. 2. The proximal part of radius and ulna. To the left is the normal appearance (score 1). To the right the crania-medial edge is depressed (score 4) and the synovial fossa of radius is enlarged to a minor extent (score 2).
Fig. 3. Osteochondritis dissecans (score 5) in the medial femoral condyle.
B. &rgensen
/Livestock
Production Science 41(1995)
N(O,l) and eijklmdistributed N (0,l) , accounting for the family structure in the model and assuming that Y and X are uncorrelated. The other effects in model ( 1) were set to zero. From the distribution across samples of the estimates of r the confidence intervals were found to be: 95% CI: - 0.170,O. 170; 99% CT: - 0.223,0.223; 99.9% CI: - 0.285,0.285 (no. of simulations = 1000). Table 3 Performance
I7I-181
175
3. Results The feeding regimes affected the production traits significantly (Table 3). Regarding daily gain there was significant interaction between sex and treatment group (P = 0.0002), while sex and treatment did not interact as to feed conversion and meat percentage. Regarding
data Castrates
Energy level Protein level No. of pigs Daily gain (g ) Feed conversion (FU kg-‘) Meat percentage
Gilts
1
2
3
4
5
1
2
3
4
5
R S 29 740a
AD L 29 925
AD s 29 928
AD H 30 943
R S 29 800
R S 30 748
AD L 30 854
AD S 29 857
AD H 29 850
R S 29 800
2.65” 56.7”
2.92 53.4
2.98 55.0
2.83 55.0
2.75 56.3
2.72 56.9
3.04 55.4
2.98 56.5
3.00 56.4
2.87 56.7
R, restricted; AD, ad libitum; S, standard; L, low; H, high. “Means corrected to mean carcass weight and dressing percentage. bMeans corrected to mean carcass weight. (from Madsen et al., Short Communication no. 753 from The National Institute of Animal Science) Table 4 Prevalence of leg weakness symptoms
(%); no. of pigs = 275
Score” Fore legs Buck-kneed Upright pasterns Weak pasterns Legs turned out Claws uneven Hind legs Standing under Steep hock joints Upright pasterns Weak pasterns Legs turned out Claws uneven Locomotion Stiff in front Stiff in rear Swaying hindquarters Twisting hocks Uncoordinated locomotion Bursitis carpalis Bursitis tarsalis “Score 1 (normal) to 4 (severe changes) bScore I (normal) to 2 (non-normal).
1
2
58.2 97.5 87.3 85.8 82.2
38.5 2.5 7.6 13.8 17.1
85.8 80.2 88.0 96.0 17.8 12.0
9.8 19.8” 9.5 2.2 55.3 47.3
98.9 70.7 52.8 61.5 65.9 95.3 51.3
0.7 13.6 27.1 16.5 34.1b 3.6 33.8
4
3
3.3
Mean
SD
1.45
4.7 0.4 0.7
0.4
1.18 1.15 1.19
0.56 0.16 0.52 0.36 0.41
4.0
0.4
1.19
0.5 1
2.5 1.8 25.8 38.9
1.1 1.8
1.15 1.06 2.10 2.31
0.42 0.30 0.69 0.70
0.4 13.9 18.3 18.7
1.8 1.8 3.3
1.01 1.47 1.69 1.64
0.15 0.80 0.83 0.90
0.4 14.5
0.7 0.4
1.07 1.64
0.34 0.74
1.03
B. J@gensen /Livestock Production Science 41(1995)
176
171-181
Table 5 Prevalence of pathological changes in the joints (%) ; no.of pigs = 279 Score” Elbow Medial condyle Lateral condyle Anconeal process Proximal edge of radius Synovial fossa of radius Stifle Medial condyle
1
2
3
4
5
Mean
SD
82.6 34.3 76.4 61.9 68.4
8.7 31.8 6.5 17.8 21.4
5.1 26.7 4.0 16.7 9.1
2.9 1.2 4.0 3.6 1.1
0.7 9.1
1.30 2.07 1.63 1.62 1.43
0.76 0.95 1.28 0.89 0.70
73.1
22.2
3.6
0.0
1.1
1.34
0.65
“Score 1 (normal) to 5 (osteochondritis dissecans) .
feed conversion significant effects of energy level (P = 0.0001) and sex (P = 0.05) were found, but no effect of protein level was present. For meat percentage the effect of energy and sex was also significant (P = 0.03 and P = 0.006, respectively), and the protein level significantly affects this trait (P < 0.01) , the difference being between low and the other levels. The prevalences of leg weakness and pathological changes in the joints are shown in Table 4 and Table 5,
respectively, and the effects of energy, protein, and sex on leg weakness and osteochondral changes in the joints are stated in Tables 6 and 7. Of 14 different leg weakness traits three showed significant difference between the energy levels: ‘weak pasterns’ and ‘legs turned out’ on fore legs, and ‘upright pasterns’ on hind legs (P < 0.05)) while ‘buck-kneed’ fore legs showed a tendency (P = 0.07) (Table 8). As to the sum of all the traits, the effect of energy level
Table 6 Effect of energy, protein and sex on leg weakness traits Energy
No. of pigs Fore legs Buck-kneed Weak pasterns Legs turned out Claws uneven Hind legs Standing under Steep hock joints Upright pasterns Legs turned out Claws uneven Locomotion Stiff in rear Swaying hindquarters Twisting hocks Uncoordinated lot. Bursitis tarsalis Sum of all traits
Protein
Control
Ad lib.
109
56
1.40” 1.13 1.10 1.13
1.55 1.32 1.24 1.20
1.18 1.45 1.10 2.06 2.22
1.29 1.41 1.24 2.08 2.30
1.58 1.55 1.56 1.56 1.60 20.60
1.60 1.87 1.66 1.74 1.66 22.16
Pb
0.07 * *
*
=
**
Sex
Low
Standard
High
56
56
55
1.46 1.08” 1.09 1.28
1.55 1.32b 1.24 1.20
1.39 1.211.18 1.25
1.17 1.24 1.21 2.18 2.49
1.29 1.41 1.24 2.08 2.30
1.12 1.36 1.08 2.25 2.39
1.37ab 1.88’ 1.69 1.64 1.76” 21.54
1.60” 1.87a 1.66 1.74 1.668b 22.16
1.23b l.5Sb 1.59 1.82 1.49b 20.92
“Least squares means from model ( 1) . Vontrast. P-values. ‘Interaction between treatment group and batch. a,b: figures with different letters are significantly different at P< = 0.05.
Pb
*
* ’
0.08
Castrates
Gilts
137
140
1.49 1.21 1.15 1.25
1.41 1.15 1.15 1.18
1.16 1.34 1.12 2.21 2.42
1.22 1.38 1.19 2.07 2.28
1.45 1.63 1.52 1.63 1.63 21.24
1.43 1.81 1.73 1.76 1.62 21.37
P
0.06
B. J@rgensen /Livestock Production Science 41(1995)
171-181
171
Table 7 Effect of energy, protein and sex on pathological
changes in the joints
Energy
Elbow Medial condyle Lateral condyle Anconeal process Proximal edge of radius Synovial fossa of radius Stifle Medial condyle Sum of all traits
Protein
Control
Ad lib.
1.39 2.10 1.65 1.60 1.41 1.40 9.62
Pb
Sex P”
Castrates
Gilts
1.12 1.84 1.41 1.52 1.41
1.21a 1.91 1.47 1.69 1.31
1.35 2.20 1.78 1.56
1.32 8.68
1.30 8.91
1.36 9.83
Low
Standard
High
1.35 2.16 1.62 1.I3 1.37
1.26 2.12 1.82 1.64 1.37
1.35 2.16 1.62 1.73 1.37
1.21 9.44
1.33 9.52
1.27 9.44
P
1.47 ’ ’
‘Least squares means from model ( 1) Vontrast, P-value. ‘Interaction between treatment group and batch. Table 8 Correlation
coefficients
(r) between leg weakness traits 2
3
4
5
6
8
7
Buck-kneed Weak pasterns - fore Legs turned out - fore Claws uneven - fore Standing under Steep hock joints Upright pasterns - hind Legs turned out - hind Claws uneven - hind Stiff in rear Swaying hindquarters Twisting hocks Uncoordinated lot.
1 0.08 -0.01 0.02 0.04 0.09 -0.04 2 0.03 -0.07 0.04 0.13 0.12 3 0.19* -0.05 0.06 0.08 4 0.07 -0.08 -0.04 5 0.19+ 0.03 6 0.17* 7 8 9 10 I1 12 13
Bursitis tarsalis
14
Table 9 Correlation
coefficients
Medial humeral condyle Lateral humerat condyle Anconeat process Proximal edge of radius Synovial fossa of radius Medial femoral condyle
(r) between osteochondral
I
0.08 0.02 0.06 0.09 0.13 -0.26** 0.04
9
10
0.04 0.09 -0.02 0.02 0.07 0.02 0.27* * 0.00 0.02 0.38*** -0.03 0.14 0.01 0.14 0.16 0.23** 0.01
11
12
13
0.15 0.06 -0.01 -0.06 0.06 0.06 0.05 0.00 0.01 0.07 -0.02 0.09 0.13 0.03 0.06 0.11 0.04 -0.01 -0.02 0.05 0.05 0.10 0.10 0.05 0.08 0.16 0.07 0.14 -0.03 -0.02 0.15 0.14 0.21’
14 0.2lt** -0.08 0.07 0.00 0.04 0.08 -0.07 -0.02 0.02 0.03 0.16 0.05 0.08
changes 2
3
4
5
0.15
0.00 0.07
0.17* 0.05 0.03
0.2tI** 0.08 0.15 0.13
2 3 4 5 6
was highly significant (P < 0.01) . For the above mentioned traits and for most of the other traits the same trend in the results was found: Pigs fed ad libitum
6 - 0.07 0.08 0.09 0.04 - 0.08
showed higher scores (i.e. more pronounced problems) than pigs in the control groups. For ‘swaying hindquarters’ a significant interaction between treat-
B. J@rgensen /Livestock Production Science 41 (1995) 171-181
178 Table 10 Correlation coefficients Osteochondral changes
( r)
between leg weakness traits and osteochondral changes Leg weakness traits” 1
Medial humeral condyle Lateral humeral condyle Anconeal process Proximal edge of radius Synovial fossa of radius Medial femoral condyle
1 0.00 2 -0.17* 3 0.05 4 -0.02 5 0.08 6 -0.02
2
3
0.04 0.04 -0.10 0.03 -0.07 -0.04 0.03 0.04 -0.07 0.00 -0.08 -0.11
4
5
6
7
8
-0.11 0.08 -0.01 -0.01 0.00 -0.08 -0.08 0.00 0.07 -0.04 0.01 0.04 0.01 0.05 0.11 -0.03 -0.12 0.03 -0.04 -0.03 -0.01 -0.04 0.04 0.11 0.06 0.11 0.08 0.04 -0.04 0.04
9 -0.08 -0.07 -0.01 -0.14 -0.04 0.12
10
11
0.02 -0.09 0.04 -0.18* 0.04 0.00 0.10 0.07 0.05 -0.04 0.03 0.06
12
13
14
-0.09 0.00 0.05 -0.04 0.01 0.02 0.00 0.06 -0.01 -0.01 -0.08 -0.15 0.13 0.02 0.01 0.03 -0.01 -0.07
%ee Table 8 for leg weakness traits.
ment group and batch was present: The effect of energy level was only significant in one of the three batches, but the tendency was the same in the other two batches. The level of protein in the feed affected some leg weakness traits, but the results did not show any unambiguous trends (Table 6). There were no differences in treatment groups neither in energy nor in protein level in the prevalences of osteochondral changes in the joints (Table 7). There were no significant differences between castrates and gilts in the prevalences of leg weakness or osteochondrosis (Tables 6 and 7). The correlation coefficients (r) between leg weakness traits were generally not very high, but some were statistically significant (Table 8). The correlation coefficients between joint lesions (Table 9) showed that some changes in the elbow joint were positively correlated, these were: ‘medial humeral condyle’ and ‘proximal edge of radius’, and ‘medial humeral condyle’ and ‘synovial fossa of radius’. However, there were no significant correlations between pathological changes in the elbow and stifle joints. Also, there were no positive correlations between leg weakness traits and osteochondral changes in the joints, however, two correlations were found to be significant in a negative direction that is between ‘buckkneed fore legs’ and ‘lateral humeral condyle’ and between ‘swaying hindquarters’ and ‘lateral humeral condyle’ (Table 10).
4. Discussion The prevalence of leg weakness in this experiment agrees with the prevalence of leg weakness in boars at
Danish pig-breeding test stations (Jorgensen and Vestergaard, 1990) (Table 4). The morphology and sites of the osteochondral lesions are similar to those descriptions by other authors (Grondalen, 1974a; Reiland, 1978b; Goedegebuure et al., 1980; Hani et al., 1983). Only grossly visible defects and abnormalities in the articular cartilage are included in this study. The most frequent occurrence of osteochondritis dissecans was in the anconeal process (9.1%, Table 5)) the medial condyles of humerus and femur having very low prevalences of osteochondritis dissecans (around 1%). In the literature these locations are stated to be predilections sites for osteochondrosis in the joint cartilage (Grondalen, 1974a; Reiland, 1978b; Hani et al., 1983; Nakano et al., 1987). Invaginations and grooves in the joint cartilage in the lateral condyle of humerus were common in this experiment as found by H5ni et al. ( 1983)) but no dissecting lesions were found here. The changes in the joint edge of proximal radius and the enlarged synovial fossa of the proximal radius were rather common here and in other investigations (Doige and Horowitz, 1975; Reiland, 1978b; Hani et al., 1983; Nakano et al., 1984). Feeding different levels of energy to slaughter pigs resulted in different growth rates, feed conversion, and meat percentage (Table 3)) but the protein level only affected the meat percentage. This experiment was one of a series of experiments carried out in the Nordic countries, and the Norwegian recommendation group was included as a control group in all four countries. Ad libitum feeding to slaughter pigs increased leg weakness problems (Table 6). This result agrees with similar experiments in slaughter pigs (Grondalen, 1974~; Wilson et al., 1980). However, Nakano et al.
B. J@gensen /Livestock
Production Science 4/(1995)
( 1979), Calabotta et al. ( 1982), and Piedrafita et al. ( 199 1) found no effect of energy level (ad libitum and restricted) on incidence of leg weakness in pigs. The energy level did not affect the prevalences of osteochondrosis in this experiment (Table 7). This agrees with the results presented by Grondalen ( 1974b) and Nakano et al. ( 1979)) whereas Goedegebuure et al. (1980) found that ad libitum feeding resulted in more lesions in the joints than middle and low energy levels did. Carlson et al. ( 1988) found that in gilts slaughtered at the same weight (110 kg) the restricted group had fewer lesions than the ad libitum group. Lundeheim (1987) has shown that weight gain during the second part of the fattening period can be seriously depressed in animals with severe lesions of osteochondrosis. The protein level affected neither leg weakness nor osteochondrosis in a uniform way (Tables 6 and 7) which is in agreement with findings from Grandalen ( 1974b c) , Reiland ( 1978~) and Hanssen and Grandalen ( 1979). There were no sex differences in the prevalences of leg weakness and osteochondrosis (Tables 6 and 7). Grondalen (1974~) and Empel (1980) found no difference in incidence of leg weakness in boars as compared with gilts, and Grcbndalen and Vangen (1974) found no difference between castrates and gilts. In contrast, Rothschild and Christian ( 1988) reported higher incidences of leg weakness in boars than in gilts, and Grondalen ( 1974b), Nakano et al. ( 1979)) Empel et al. (1980) and Goedegebuure et al. (1988) published higher incidences of joint lesions in boars than in gilts. Van der Wal et al. (1983) and Lundeheim (1987) found higher incidences of osteochondrosis in barrows than in gilts. In this study there were many mutually positive correlations between leg weakness traits (Table 8). All the significant correlation coefficients, except one, were positive - indicating that these are symptoms included in the same syndrome. Some symptoms showed no significant or negative correlations to others, these were: ‘weak pasterns’ on fore legs and ‘swaying hindquarters’, indicating that they are perhaps not part of the leg weakness syndrome. Grondalen (1974~) reported that pigs having weak pasterns on front legs achieved the best gait score, while Jorgensen and Vestergaard ( 1990) found that the phenotypic correlations between leg weakness symptoms were small.
171-181
179
Osteochondral lesions in the medial humeral condyle were correlated with joint changes in the proximal radius (depression of the joint edge with thinning of cartilage and enlarged synovial fossa) (Table 9). The same associations were found by Harti et al. (1983) and Nakano et al. ( 1984)) while Doige and Horowitz (1975) reported that synovial fossae in the joints had histologically normal structures without collapse of underlying bone. There was no correlation between osteochondrosis in the elbow and stifle joints corresponding to results by Grandalen ( 1974b), Grondalen and Vangen ( 1974), and Carlson et al. ( 1988), whereas Olsson and Reiland (1978) state that osteochondrosis is a generalized disorder. Local conditions in the joints may play an important part for the osteochondrosis complex (Grondalen, 1974b). This study did not show any positive correlations (in a mathematics meaning) between leg weakness traits and osteochondral changes in the joints (Table IO). Osteochondrosis has been stated as the primary cause of leg weakness, and the relationship between these traits has been investigated. The relationship was not always possible to demonstrate, however (Thurley, 1969; Grondalen, 1974~; Reiland et al., 1978; Empel, 1980; Goedegebuure et al., 1988), and the explanation might be that only severe joint lesions cause an increase in the clinical signs of leg weakness (Grondalen, 1974~; Bring-Larsson and Sundgren, 1977; Lundeheim, 1987). In the present study the prevalences of severe joint lesions (osteochondritis dissecans) were low compared with the previously mentioned investigations, so this hypothesis could not be examined.
Acknowledgements Dr. E. Jorgensen and Dr. D. Sorensen, National Institute of Animal Science and Dr. S. Andersen, The Federation of Danish Pig Producers and Slaughterhouses have provided helpful comments regarding the statistics. Dr. Ame Madsen has provided valuable comments on the manuscript. They are thanked for their assistance.
References Bereskin, B., 1979. Genetic aspects of feet and legs soundness swine. J. Anim. Sci., 48: 1322-1328.
in
180
B. J@rgensen / Livestock Production Science 41 (1995) 171-181
Bring-Larsson K. and Sundgren P.-E., 1977. Studier over risrelsestijmingar hos svin. Reports Agric. Coll. Sweden, 284.30 pp. Calabotta, D.F., Komegay,E.T., Thomas, H.R., Knight, J.W., Notter, D.R. and Veit, H.P., 1982. Restricted energy intake and elevated calcium and phosphorus intake for gilts during growth. I. Feedlot performance and foot and leg measurements and scores during growth. J. Anim. Sci., 54: 565-575. Carlson, C.S., Hilley, H.D. Meuten, D.J. Hagan, J.M. and Moser, R.L., 1988. Effect of reduced growth rate on the prevalence and severity of osteochondrosis in gilts. Am. J. Vet. Res., 49: 396 402. Doige, C. and Horowitz, A., 1975. A study of articular surfaces and synovial fossae of the pectoral limb of swine. Can. J. Comp. Med., 39: 7-16. Duthie, I.F. and Lancaster, M.C., 1964. Polyarthritis and epiphyseolysis of pigs in England. Vet. Rec., 76: 263-273. Empel, W., 1980. Pathomorphological lesions in the skeleton and incidence of leg weakness syndrome in six month old Norwegian Landrace pigs. Ann. Wars. Agricult. Univ., Vet. Med., 10: 3338. Empel, W., Walach-Janiak, M. and Fandrejewski, H., 1980. Influence of intensity of feeding and protein body content on the incidence of osteochondrosis in six month old pigs. Ann. Wars. Agricult. Univ., Vet. Med., 10: 39-43. Goedegebuure, S.A., Hani, H.J., van der Valk, P.C. and van der Wal, P.G., 1980. Osteochondrosis in six breeds of slaughter pigs. I. A morphological investigation of the status of osteochondrosis in relation to breed and level of feeding. Vet. Q., 2: 2841. Goedegebuure, S.A., Rothschild, M.F., Christian, L.L. and Ross, R.F., 1988. Severity of osteochondrosis in three genetic lines of Duroc swine divergently selected for front leg-weakness. Livest. Prod. Sci., 19: 487-498. Grondalen, T., 1974a. Osteochondrosis and arthrosis in pigs. 1. Incidence in animals up to 120 kg live weight. Acta Vet. Scand., 15: l-25. Grendalen, T., 1974b. Osteochondrosis and arthrosis in pigs. VI. Relationship to feed level and calcium, phosphorus and protein levels in the ration. Acta Vet. Scand., 15: 147-169. Grendalen, T., 1974~. Leg weakness in pigs. I. Incidence and relationship to skeletal lesions, feeding level, protein and mineral supply, exercise and exterior conformation. Acta Vet. Scand., 15: 555-573. Grondalen, T. and Vangen, O., 1974. Osteochondrosis and arthrosis in pigs. V. A comparison of the incidence in three different lines of the Norwegian Landrace breed. Acta Vet. Stand., 15: 61-79. Hanssen, J.T. and Grendalen, T., 1979. The effect of different dietary factors on growth and development in young boars and gilts. Z. Tierphysiol., Tiem&hrg. u. Futtermittelkde., 42: 65-83. Henderson, C.R., 1953. Estimation of variance and covariance components. Biometrics, 9: 226-252. H&ii, H., Troxler, I. und W=ursten, B., 1983. Untersuchungen zum Einfluss der Haltung auf Verbreitung und Schweregrad von Osteochondrosis (OC) bei Mastschweinen. Schweiz. Arch. Tierheilk., 125: 453-475. Jorgensen, B. and Vestergaard, T., 1990. Genetics of leg weakness in boars at the Danish pig breeding stations. Acta Agric. Scand., 40: 59-69.
Lundeheim, N., 1987. Genetic analysis of osteochondrosis and leg weakness in the Swedish pig progeny testing scheme. Acta Agric. Scand., 37: 159-173. Nakano, T., Aheme, F.X. and Thompson, J.R., 1979. Effects of feed restriction, sex and diethylstilbestrol on the occurence of joint lesions with some histological and biochemical studies of the articular cartilage of growing-finishing swine. Can. I. Anim. Sci., 59: 491-502. Nakano, T., Aheme, F.X. Brennan, J.J. and Thompson, J.R., 1984. Effect of growth rate on the incidence of osteochondrosis in growing swine. Can. J. Anim. Sci., 64: 139-146. Nakano, T., Brennan, J.J. and Aheme, F.X., 1987. Leg weakness and osteochondrosis in swine: A review. Can. J. Anim. Sci., 67: 883901. Olsson, S-E and Reiland, S., 1978. The nature of osteochondrosis in animals. Summary and conclusions with comparative aspects on osteochondritis dissecans in man. ActaRadiol. Suppl., 358: 299306. Piedratita, J., Rothschild, M.F. and Christian L.L., 1991. Differential response to restricted feeding in two divergent lines of Duroc swine selected for front-leg structure. J. Anim. Breed. Genet., 108: 139-146. Reiland, S., 1978a. Pathology of so-called leg weakness in the pig. Acta Radiol. Suppl., 358: 23-14. Reiland, S., 1978b. Morphology of osteochondrosis and sequelae in pigs. Acta Radiol. Suppl., 358: 45-90. Reiland, S., 1978~. Effects of vitamin D and A, Ca, P, and protein on frequency of osteochondrosis in pigs. An experimental investigation. Acta Radiol. Suppl., 358: 91-106. Reiland, S., Ordell, N., Lundeheim, N. and Olsson, S.-E., 1978. Heredity of osteochondrosis, body constitution and leg weakness in the pig. Acta Radiol. Suppl., 358: 123-137. Rothschild, M.F. and Christian, L.L., 1988. Genetic control of frontleg weakness in Duroc swine. I. Direct response to five generations of divergent selection. Livest. Prod. Sci., 19: 459-471. Rothschild, M.F., Christian, L.L. and Jung, Y.-C., 1988. Genetic control of front-leg weakness in Duroc swine. II. Correlated responses in growth rate, backfat and reproduction from five generations of divergent selection. Livest. Prod. Sci., 19: 473485. SAS Institute Inc., 1988. SAS/STATTMUser’s Guide, Release 6.03 Edition. Gary, N.C: SAS Institute Inc., 1028 pp. Serensen, M.T., Jergensen, B. and Danielsen, V., 1993. Different feeding intensity of young gilts: Effect on growth, milk yield, reproduction, leg soundness, and longevity. Report No. 14 from National Institute of Animal Science, Denmark, 20 pp. (in Danish with English abstract and subtitles). Thurley, D.C., 1969.Changes in the epiphyseal cartilage of immature pigs without clinical lameness. Path. Vet., 6: 217-226. Wal, P.G. van der, Valk, P.C. van der, Goedegebuure, S.A. and Essen, G. van, 1983. Do gilts and barrows react similarly with respect to leg weakness and osteochondrosis? Vet. Q., 5: 175177. Webb, A.J., Russel, W.S. and Sales, D.I., 1983. Genetics of leg weakness in performance-tested boars. Anim. Prod., 36: 117130.
B. J@gensen /Livestock Production Science 41 (1995) 171-181 Wilson, R.D., Christian, L.L. and Schneider, J.F., 1980. The effects of sire soundness classification and feed restriction on perform-
181
ante and leg scores of pigs. J. Anim. Sci., 5 1, Suppl. 1: 132. (Abstr.)
R&urn6 Jorgensen, B., 1995. Effets de differents niveaux d’apports d’energie et de proteines sur la faiblesse des pattes et l’osteochondrose LiI;esr. Prod.Sci.,41: 171-181.
chez le port.
Les effets des apports d’energie, de proteines et du sexe sur la faiblesse des panes et l’osteochondrose ont et6 etudies sur le port charcutier. et les correlations entre ces caracteres ont et6 estimees. L’exp&ience portait sur 300 ports croises males c&r& et femelles, recevant des regimes a trois taux de proteines en alimentation ration&e ou ad libitum. Les ports Btaient notes sur 14 caracteres de faiblesse des pattes different% et une note d’osteochondrose &it attribuQ au coude et a l’articulation du carpe apms l’abattage. Les apports d’energie affectaient dans le meme sens trois des caracters de faiblesse des pattes et la “note globale de faiblesse des pattes”: les ports nourris ad libitum avaient des prob&mes plus prononces que ceux qui etaient ration&. I1 n’y avait pas d’effet du niveau d’energie sur l’osttochondrose. Les apports de proteines et le sexe n’affectaient ni la faiblesse des pattes, ni l’osteochondrose. Les lesions osteochondrales du condyle hum&al median Btaient corr&es avec les changements du radius proximal: a&e proximale du radius ( r = 0.17, P < 0.05) et fosse synoviale du radius ( r = 0.28, P < 0.0 1) Cependant, il n’y avait pas de correlation significative entre les changements au coude et a l’articulation du carpe. 11n’y avait pas de correlation entre les caracteres de faiblesse des pattes et l’osteochondrose, ce qui pourrait &tre dfl au fait que la prevalence de lesions severes des articulations (osteochondritis dissecans) etait t&s faible.
Kurzfassung Jorgensen, B., 1995. Die Wirkung verschiedener Prod. Sci.,41: 171-181 (aufenglisch).
Energie- und Proteinniveaus
auf Beinschwkhe
und Osteochondrosis
bei Schweinen.
Lioesl.
Die Wirkung des Energie- und Proteinniveaus, sowie des Geschlechts auf Beinschwache und Osteochondrosis bei Schlachtschweinen wurde untersucht und die Korrelationen zwischen diesen Merkmalen wurden beurteilt. Der Versuch bestand aus 300 gekreuzten Kastraten und Jungsauen, die entweder restriktiv oder ad libitum auf drei verschiedenen Proteinniveaus gefiittert wurden. Nach dem Schlachten wurden die Ellbogen und die Kniegelenke auf Osteochondrosis beurteilt. Das Energieniveau beeinflusste drei der BeinschwEheeigenschaften und die ‘gesamte Beinschwachebeurteilung’ in derselben Richtung: die ad libitum gefthterten Schweine zeigten ausgepragtere Probleme als die Schweine der restriktiven Gruppe. Das Energieniveau ermittelte keine Wirkung auf Osteochondrosis. Weder das Geschlecht noch das Proteinniveau hatten eine Wirkung auf das Vorkommen von Beinschwache oder Osteochondrosis. Osteochondrosale LIsionen im medialen humemlen Condylus waren mit einigen Gelenkveriinderungen im proximalen Radius korreliert: proximale Rand des Radius (r= 0.17, P < 0,05) und Synovialgrube des Radius (r= 0.28, P
ELSEVIER
Livestock Production
Science 41 (1995)
171-181
Effect of different energy and protein levels on leg weakness and osteochondrosis in pigs Bente J@rgensen* National institute of Animal Science, Research Centre Foulum, P.O. Box 39, DK 8830 Tjele, Denmark Accepted 7
June 1994
Abstract The effects of energy level, protein level, and sex on leg weakness and osteochondrosis in slaughter pigs were studied, and correlations between these traits were estimated. The experiment consisted of 300 crossbred castrates and gilts, fed either restricted or ad libitum on three different levels of protein. The pigs were scored for 14 different leg weakness traits and the elbow and stifle joints were scored for osteochondrosis after slaughter. Energy level affected three of the leg weakness traits and the ‘total leg weakness score’ in the same direction: pigs fed ad libitum showed more pronounced problems than pigs in the restricted groups. There was no effect of energy level on osteochondrosis. Protein level and sex did neither affect leg weakness nor osteochondrosis. Osteochondral lesions in the medial humeral condyle were correlated with changes in the proximal radius: proximal edge of radius (I-= 0.17, P < 0.05) and synovial fossa of radius (r= 0.28, P
1. Introduction Leg weakness is one of the major reasons for lameness leading to culling in gilts, sows, and boars. The term leg weakness is used to describe a syndrome characterized by changes in leg position and abnormal locomotion. Genetic predisposition as well as selection for production traits such as high growth rate and meat content are found to cause leg weakness problems (Bereskin, 1979; Webb et al., 1983; Lundeheim, 1987; Rothschild et al., 1988; Jorgensen and Vestergaard, 1990). Furthermore, feeding high energy levels appears to predispose for leg weakness in pigs *Corresponding
author.
0301-6226/95/$09.50 0 1995Blsevier Science B.V. All rights reserved SSDIO301-6226(94)00048-C
(Grondalen, 1974~; Hanssen and Grondalen, 1979; Wilson et al., 1980; Sorensen et al., 1993). The protein level does not seem to affect leg soundness (Grondalen, 1974~; Hanssen and Grondalen, 1979; Reiland, 1978b). The etiology of leg weakness is by many researchers considered to be osteochondrosis, a generalized disturbance of the enchondral ossification as well in the joint cartilage as in the growth plates (Duthie and Lancaster, 1964; Grondalen, 1974a; Reiland, 1978a; Goedegebuure et al., 1980; Lundeheim, 1987; Nakano et al., 1987)) while others do not find a relationship between leg weakness and osteochondrosis (Thurley, 1969; Grondalen, 1974~; Empel, 1980; Goedegebuure et al., 1988).
172
B. J@rgensen /Livestock
Production Science 41(1995)
The objective of this study was to evaluate the effect of energy and protein levels on leg weakness symptoms and osteochondrosis in slaughter pigs. Furthermore, the aim was to test for sex differences in these traits and finally to estimate the correlations between leg weakness symptoms and osteochondrosis.
2. Material and methods A total of 300 pigs - from 60 Yorkshire * Danish Landrace litters (30 litters of 5 castrates and 30 litters of 5 gilts) - were allocated to five groups and fed three different energy levels (ad libitum and according to either Norwegian or Danish recommandation (Table 1)) and three levels of protein within the ad libitum regime (Table 2). The experiment consisted of three batches of 100 pigs (ten in each group of each sex), fed from 25-100 kg and housed in individual pens on concrete floor with bedding. The composition of the experimental diets is listed in Table 2. There was 7.0 g Ca and 5.5 g P per kg diet. The pigs were judged clinically for leg weakness problems the week before slaughter. Judgment was done using a scale from 1 (normal) to 4 (very severe changes) (Jorgensen and Vestergaard, 1990). After slaughter, the elbow and stifle joints from the same side were inspected macroscopically for osteochondral and other changes at the intact surface. These were all scored on a scale from 1 (normal) to 5 (osteochondritis dissecans) . The following joint changes were scored: Medial and lateral humeral condyles, medial femoral condyle, and articular surface of the anconeal process of ulna (invaginations, grooves or defects in the joint cartilage, 5 = osteochondritis dissecans) (Fig. 1 and Fig. 3) ; proximal edge of radius (thinning of cartilage and/or bony depression of the crania-medial edge) (Fig. 2) ; synovial fossa of proximal radius (enlarged depression in the articular surface of radius) (Fig. 2). All judgments were made by the author without knowledge of treatment group or sex, and evaluation of joint lesions without knowledge of the results of the clinical examination. The effect of energy level, protein level, and sex on performance, leg weakness traits, and osteochondrosis was tested using the following univariate model: Kjklm = p+ti
+Sj
+6,+Lj,l
+eijklm
(1)
171-181
where Yijumis the observation of leg weakness trait or osteochondrosis of the mth pig on treatment group i of sex j in the kth batch from litter 1; p is the mean; ti is the fixed effect of treatment group (i = 1,2,3,4,5) ; Sj is the fixed effect of sex (j is castrate or gilt); 6, is the fixed effect of batch; Ljkl is the random effect of litter within sex and batch, N(O,Iai;) eijam is the random residual effects, N(O,IU’) . The effect of sex was tested by using litter within sex and batch as the appropriate error term. Preliminary analysis showed no differences in leg weakness and osteochondrosis between the Norwegian and the Danish recommendations, therefore these treatment groups were combined into one (control). Effect of energy level was tested at the same level of protein (standard) as the contrast between treatment group 1 + 5 (control) and 3 (ad libitum) . Effect of protein was tested at the same energy level (ad libitum) as the contrast between treatment groups 2, 3, and 4. Only variables with a total prevalence of scores (2, 3, 4) > 10% were analysed, because of non-normal distribution of the data (Weeb et al., 1983; Jorgensen and Vestergaard, 1990). Interaction terms were found nonsignificant in most analyses and deleted from the model when possible. PROC GLM in SAS was used (SAS Institute Inc., 1988). Due to missing values for some pigs the number of pigs used in the analyses was 257. Correlation coefficients ( ryx) between leg weakness traits (n) and changes in the joints (y) were estimated as follows: Cov(x,y) ‘Y”
=
2 2 (+y (+x
where Cov (xv) =
CLyx
+
Gyx
and U; = crz + uf a2=&+(+2 x
ex*
(&, c&, u&, and ~2~ are the litter and residual variances of trait y and trait x, respectively.) us and as are estimated using Henderson Method 3 (Henderson, 1953). MS(L) and MS(e) are obtained from the GLM procedure (MANOVA) in SAS using model ( 1). The significance levels of r were found by simulating a data set where the Yand X values are calculated using pseudo-random variables with Lju distributed
B. Jergensen /Livestock Production Science 4I (1995) 171-181 Table I Danish and Norwegian
recommendations
Weight (kg) Danish, kg/day Norwegian, kg/day
Table 2 Composition
30 1.5 1.3
of the experimental
173
on net energy for slaughter pigs 40 1.9 1.6
50 2.2 1.9
60 2.5 2.3
70 2.7 2.6
80 2.8 2.9
90 2.8 3.2
100 2.8 3.2
diets, per cent 2060
kg
60-100 kg
Treatment group
1+3+5
2
4
1+3+5
2
4
Soybean meal Barley Wheat Oats Minerals and vitamins FU per kg g digestible crude protein/FE,
25.0 50.6 10.9 10.9 2.6 1.00 153
20.5 53.9 11.5 11.5 2.6 0.99 141
30.0 47.2 10.1 10.1 2.6 1.01 167
18.0 55.6 11.9 11.9 2.6 0.99 134
13.0 59.0 12.7 12.7 2.6 0.98 120
22.5 52.5 11.2 Il.2 2.6 1.00 146
Treatment group I is fed according to the Norwegian rec. at standard protein level. Treatment groups 2, 3, and 4 are fed ad libitum at low, standard, and high protein level. Treatment group 5 is fed according to the Danish rec. at standard protein level.
Fig. 1. Osteochondritis
dissecans
(score 5) in the anconeal process of ulna.
174
B. Jergensen /Livestock Production Science 41 (1995) 171-181
Fig. 2. The proximal part of radius and ulna. To the left is the normal appearance (score 1). To the right the crania-medial edge is depressed (score 4) and the synovial fossa of radius is enlarged to a minor extent (score 2).
Fig. 3. Osteochondritis dissecans (score 5) in the medial femoral condyle.
B. &rgensen
/Livestock
Production Science 41(1995)
N(O,l) and eijklmdistributed N (0,l) , accounting for the family structure in the model and assuming that Y and X are uncorrelated. The other effects in model ( 1) were set to zero. From the distribution across samples of the estimates of r the confidence intervals were found to be: 95% CI: - 0.170,O. 170; 99% CT: - 0.223,0.223; 99.9% CI: - 0.285,0.285 (no. of simulations = 1000). Table 3 Performance
I7I-181
175
3. Results The feeding regimes affected the production traits significantly (Table 3). Regarding daily gain there was significant interaction between sex and treatment group (P = 0.0002), while sex and treatment did not interact as to feed conversion and meat percentage. Regarding
data Castrates
Energy level Protein level No. of pigs Daily gain (g ) Feed conversion (FU kg-‘) Meat percentage
Gilts
1
2
3
4
5
1
2
3
4
5
R S 29 740a
AD L 29 925
AD s 29 928
AD H 30 943
R S 29 800
R S 30 748
AD L 30 854
AD S 29 857
AD H 29 850
R S 29 800
2.65” 56.7”
2.92 53.4
2.98 55.0
2.83 55.0
2.75 56.3
2.72 56.9
3.04 55.4
2.98 56.5
3.00 56.4
2.87 56.7
R, restricted; AD, ad libitum; S, standard; L, low; H, high. “Means corrected to mean carcass weight and dressing percentage. bMeans corrected to mean carcass weight. (from Madsen et al., Short Communication no. 753 from The National Institute of Animal Science) Table 4 Prevalence of leg weakness symptoms
(%); no. of pigs = 275
Score” Fore legs Buck-kneed Upright pasterns Weak pasterns Legs turned out Claws uneven Hind legs Standing under Steep hock joints Upright pasterns Weak pasterns Legs turned out Claws uneven Locomotion Stiff in front Stiff in rear Swaying hindquarters Twisting hocks Uncoordinated locomotion Bursitis carpalis Bursitis tarsalis “Score 1 (normal) to 4 (severe changes) bScore I (normal) to 2 (non-normal).
1
2
58.2 97.5 87.3 85.8 82.2
38.5 2.5 7.6 13.8 17.1
85.8 80.2 88.0 96.0 17.8 12.0
9.8 19.8” 9.5 2.2 55.3 47.3
98.9 70.7 52.8 61.5 65.9 95.3 51.3
0.7 13.6 27.1 16.5 34.1b 3.6 33.8
4
3
3.3
Mean
SD
1.45
4.7 0.4 0.7
0.4
1.18 1.15 1.19
0.56 0.16 0.52 0.36 0.41
4.0
0.4
1.19
0.5 1
2.5 1.8 25.8 38.9
1.1 1.8
1.15 1.06 2.10 2.31
0.42 0.30 0.69 0.70
0.4 13.9 18.3 18.7
1.8 1.8 3.3
1.01 1.47 1.69 1.64
0.15 0.80 0.83 0.90
0.4 14.5
0.7 0.4
1.07 1.64
0.34 0.74
1.03
B. J@gensen /Livestock Production Science 41(1995)
176
171-181
Table 5 Prevalence of pathological changes in the joints (%) ; no.of pigs = 279 Score” Elbow Medial condyle Lateral condyle Anconeal process Proximal edge of radius Synovial fossa of radius Stifle Medial condyle
1
2
3
4
5
Mean
SD
82.6 34.3 76.4 61.9 68.4
8.7 31.8 6.5 17.8 21.4
5.1 26.7 4.0 16.7 9.1
2.9 1.2 4.0 3.6 1.1
0.7 9.1
1.30 2.07 1.63 1.62 1.43
0.76 0.95 1.28 0.89 0.70
73.1
22.2
3.6
0.0
1.1
1.34
0.65
“Score 1 (normal) to 5 (osteochondritis dissecans) .
feed conversion significant effects of energy level (P = 0.0001) and sex (P = 0.05) were found, but no effect of protein level was present. For meat percentage the effect of energy and sex was also significant (P = 0.03 and P = 0.006, respectively), and the protein level significantly affects this trait (P < 0.01) , the difference being between low and the other levels. The prevalences of leg weakness and pathological changes in the joints are shown in Table 4 and Table 5,
respectively, and the effects of energy, protein, and sex on leg weakness and osteochondral changes in the joints are stated in Tables 6 and 7. Of 14 different leg weakness traits three showed significant difference between the energy levels: ‘weak pasterns’ and ‘legs turned out’ on fore legs, and ‘upright pasterns’ on hind legs (P < 0.05)) while ‘buck-kneed’ fore legs showed a tendency (P = 0.07) (Table 8). As to the sum of all the traits, the effect of energy level
Table 6 Effect of energy, protein and sex on leg weakness traits Energy
No. of pigs Fore legs Buck-kneed Weak pasterns Legs turned out Claws uneven Hind legs Standing under Steep hock joints Upright pasterns Legs turned out Claws uneven Locomotion Stiff in rear Swaying hindquarters Twisting hocks Uncoordinated lot. Bursitis tarsalis Sum of all traits
Protein
Control
Ad lib.
109
56
1.40” 1.13 1.10 1.13
1.55 1.32 1.24 1.20
1.18 1.45 1.10 2.06 2.22
1.29 1.41 1.24 2.08 2.30
1.58 1.55 1.56 1.56 1.60 20.60
1.60 1.87 1.66 1.74 1.66 22.16
Pb
0.07 * *
*
=
**
Sex
Low
Standard
High
56
56
55
1.46 1.08” 1.09 1.28
1.55 1.32b 1.24 1.20
1.39 1.211.18 1.25
1.17 1.24 1.21 2.18 2.49
1.29 1.41 1.24 2.08 2.30
1.12 1.36 1.08 2.25 2.39
1.37ab 1.88’ 1.69 1.64 1.76” 21.54
1.60” 1.87a 1.66 1.74 1.668b 22.16
1.23b l.5Sb 1.59 1.82 1.49b 20.92
“Least squares means from model ( 1) . Vontrast. P-values. ‘Interaction between treatment group and batch. a,b: figures with different letters are significantly different at P< = 0.05.
Pb
*
* ’
0.08
Castrates
Gilts
137
140
1.49 1.21 1.15 1.25
1.41 1.15 1.15 1.18
1.16 1.34 1.12 2.21 2.42
1.22 1.38 1.19 2.07 2.28
1.45 1.63 1.52 1.63 1.63 21.24
1.43 1.81 1.73 1.76 1.62 21.37
P
0.06
B. J@rgensen /Livestock Production Science 41(1995)
171-181
171
Table 7 Effect of energy, protein and sex on pathological
changes in the joints
Energy
Elbow Medial condyle Lateral condyle Anconeal process Proximal edge of radius Synovial fossa of radius Stifle Medial condyle Sum of all traits
Protein
Control
Ad lib.
1.39 2.10 1.65 1.60 1.41 1.40 9.62
Pb
Sex P”
Castrates
Gilts
1.12 1.84 1.41 1.52 1.41
1.21a 1.91 1.47 1.69 1.31
1.35 2.20 1.78 1.56
1.32 8.68
1.30 8.91
1.36 9.83
Low
Standard
High
1.35 2.16 1.62 1.I3 1.37
1.26 2.12 1.82 1.64 1.37
1.35 2.16 1.62 1.73 1.37
1.21 9.44
1.33 9.52
1.27 9.44
P
1.47 ’ ’
‘Least squares means from model ( 1) Vontrast, P-value. ‘Interaction between treatment group and batch. Table 8 Correlation
coefficients
(r) between leg weakness traits 2
3
4
5
6
8
7
Buck-kneed Weak pasterns - fore Legs turned out - fore Claws uneven - fore Standing under Steep hock joints Upright pasterns - hind Legs turned out - hind Claws uneven - hind Stiff in rear Swaying hindquarters Twisting hocks Uncoordinated lot.
1 0.08 -0.01 0.02 0.04 0.09 -0.04 2 0.03 -0.07 0.04 0.13 0.12 3 0.19* -0.05 0.06 0.08 4 0.07 -0.08 -0.04 5 0.19+ 0.03 6 0.17* 7 8 9 10 I1 12 13
Bursitis tarsalis
14
Table 9 Correlation
coefficients
Medial humeral condyle Lateral humerat condyle Anconeat process Proximal edge of radius Synovial fossa of radius Medial femoral condyle
(r) between osteochondral
I
0.08 0.02 0.06 0.09 0.13 -0.26** 0.04
9
10
0.04 0.09 -0.02 0.02 0.07 0.02 0.27* * 0.00 0.02 0.38*** -0.03 0.14 0.01 0.14 0.16 0.23** 0.01
11
12
13
0.15 0.06 -0.01 -0.06 0.06 0.06 0.05 0.00 0.01 0.07 -0.02 0.09 0.13 0.03 0.06 0.11 0.04 -0.01 -0.02 0.05 0.05 0.10 0.10 0.05 0.08 0.16 0.07 0.14 -0.03 -0.02 0.15 0.14 0.21’
14 0.2lt** -0.08 0.07 0.00 0.04 0.08 -0.07 -0.02 0.02 0.03 0.16 0.05 0.08
changes 2
3
4
5
0.15
0.00 0.07
0.17* 0.05 0.03
0.2tI** 0.08 0.15 0.13
2 3 4 5 6
was highly significant (P < 0.01) . For the above mentioned traits and for most of the other traits the same trend in the results was found: Pigs fed ad libitum
6 - 0.07 0.08 0.09 0.04 - 0.08
showed higher scores (i.e. more pronounced problems) than pigs in the control groups. For ‘swaying hindquarters’ a significant interaction between treat-
B. J@rgensen /Livestock Production Science 41 (1995) 171-181
178 Table 10 Correlation coefficients Osteochondral changes
( r)
between leg weakness traits and osteochondral changes Leg weakness traits” 1
Medial humeral condyle Lateral humeral condyle Anconeal process Proximal edge of radius Synovial fossa of radius Medial femoral condyle
1 0.00 2 -0.17* 3 0.05 4 -0.02 5 0.08 6 -0.02
2
3
0.04 0.04 -0.10 0.03 -0.07 -0.04 0.03 0.04 -0.07 0.00 -0.08 -0.11
4
5
6
7
8
-0.11 0.08 -0.01 -0.01 0.00 -0.08 -0.08 0.00 0.07 -0.04 0.01 0.04 0.01 0.05 0.11 -0.03 -0.12 0.03 -0.04 -0.03 -0.01 -0.04 0.04 0.11 0.06 0.11 0.08 0.04 -0.04 0.04
9 -0.08 -0.07 -0.01 -0.14 -0.04 0.12
10
11
0.02 -0.09 0.04 -0.18* 0.04 0.00 0.10 0.07 0.05 -0.04 0.03 0.06
12
13
14
-0.09 0.00 0.05 -0.04 0.01 0.02 0.00 0.06 -0.01 -0.01 -0.08 -0.15 0.13 0.02 0.01 0.03 -0.01 -0.07
%ee Table 8 for leg weakness traits.
ment group and batch was present: The effect of energy level was only significant in one of the three batches, but the tendency was the same in the other two batches. The level of protein in the feed affected some leg weakness traits, but the results did not show any unambiguous trends (Table 6). There were no differences in treatment groups neither in energy nor in protein level in the prevalences of osteochondral changes in the joints (Table 7). There were no significant differences between castrates and gilts in the prevalences of leg weakness or osteochondrosis (Tables 6 and 7). The correlation coefficients (r) between leg weakness traits were generally not very high, but some were statistically significant (Table 8). The correlation coefficients between joint lesions (Table 9) showed that some changes in the elbow joint were positively correlated, these were: ‘medial humeral condyle’ and ‘proximal edge of radius’, and ‘medial humeral condyle’ and ‘synovial fossa of radius’. However, there were no significant correlations between pathological changes in the elbow and stifle joints. Also, there were no positive correlations between leg weakness traits and osteochondral changes in the joints, however, two correlations were found to be significant in a negative direction that is between ‘buckkneed fore legs’ and ‘lateral humeral condyle’ and between ‘swaying hindquarters’ and ‘lateral humeral condyle’ (Table 10).
4. Discussion The prevalence of leg weakness in this experiment agrees with the prevalence of leg weakness in boars at
Danish pig-breeding test stations (Jorgensen and Vestergaard, 1990) (Table 4). The morphology and sites of the osteochondral lesions are similar to those descriptions by other authors (Grondalen, 1974a; Reiland, 1978b; Goedegebuure et al., 1980; Hani et al., 1983). Only grossly visible defects and abnormalities in the articular cartilage are included in this study. The most frequent occurrence of osteochondritis dissecans was in the anconeal process (9.1%, Table 5)) the medial condyles of humerus and femur having very low prevalences of osteochondritis dissecans (around 1%). In the literature these locations are stated to be predilections sites for osteochondrosis in the joint cartilage (Grondalen, 1974a; Reiland, 1978b; Hani et al., 1983; Nakano et al., 1987). Invaginations and grooves in the joint cartilage in the lateral condyle of humerus were common in this experiment as found by H5ni et al. ( 1983)) but no dissecting lesions were found here. The changes in the joint edge of proximal radius and the enlarged synovial fossa of the proximal radius were rather common here and in other investigations (Doige and Horowitz, 1975; Reiland, 1978b; Hani et al., 1983; Nakano et al., 1984). Feeding different levels of energy to slaughter pigs resulted in different growth rates, feed conversion, and meat percentage (Table 3)) but the protein level only affected the meat percentage. This experiment was one of a series of experiments carried out in the Nordic countries, and the Norwegian recommendation group was included as a control group in all four countries. Ad libitum feeding to slaughter pigs increased leg weakness problems (Table 6). This result agrees with similar experiments in slaughter pigs (Grondalen, 1974~; Wilson et al., 1980). However, Nakano et al.
B. J@gensen /Livestock
Production Science 4/(1995)
( 1979), Calabotta et al. ( 1982), and Piedrafita et al. ( 199 1) found no effect of energy level (ad libitum and restricted) on incidence of leg weakness in pigs. The energy level did not affect the prevalences of osteochondrosis in this experiment (Table 7). This agrees with the results presented by Grondalen ( 1974b) and Nakano et al. ( 1979)) whereas Goedegebuure et al. (1980) found that ad libitum feeding resulted in more lesions in the joints than middle and low energy levels did. Carlson et al. ( 1988) found that in gilts slaughtered at the same weight (110 kg) the restricted group had fewer lesions than the ad libitum group. Lundeheim (1987) has shown that weight gain during the second part of the fattening period can be seriously depressed in animals with severe lesions of osteochondrosis. The protein level affected neither leg weakness nor osteochondrosis in a uniform way (Tables 6 and 7) which is in agreement with findings from Grandalen ( 1974b c) , Reiland ( 1978~) and Hanssen and Grandalen ( 1979). There were no sex differences in the prevalences of leg weakness and osteochondrosis (Tables 6 and 7). Grondalen (1974~) and Empel (1980) found no difference in incidence of leg weakness in boars as compared with gilts, and Grcbndalen and Vangen (1974) found no difference between castrates and gilts. In contrast, Rothschild and Christian ( 1988) reported higher incidences of leg weakness in boars than in gilts, and Grondalen ( 1974b), Nakano et al. ( 1979)) Empel et al. (1980) and Goedegebuure et al. (1988) published higher incidences of joint lesions in boars than in gilts. Van der Wal et al. (1983) and Lundeheim (1987) found higher incidences of osteochondrosis in barrows than in gilts. In this study there were many mutually positive correlations between leg weakness traits (Table 8). All the significant correlation coefficients, except one, were positive - indicating that these are symptoms included in the same syndrome. Some symptoms showed no significant or negative correlations to others, these were: ‘weak pasterns’ on fore legs and ‘swaying hindquarters’, indicating that they are perhaps not part of the leg weakness syndrome. Grondalen (1974~) reported that pigs having weak pasterns on front legs achieved the best gait score, while Jorgensen and Vestergaard ( 1990) found that the phenotypic correlations between leg weakness symptoms were small.
171-181
179
Osteochondral lesions in the medial humeral condyle were correlated with joint changes in the proximal radius (depression of the joint edge with thinning of cartilage and enlarged synovial fossa) (Table 9). The same associations were found by Harti et al. (1983) and Nakano et al. ( 1984)) while Doige and Horowitz (1975) reported that synovial fossae in the joints had histologically normal structures without collapse of underlying bone. There was no correlation between osteochondrosis in the elbow and stifle joints corresponding to results by Grandalen ( 1974b), Grondalen and Vangen ( 1974), and Carlson et al. ( 1988), whereas Olsson and Reiland (1978) state that osteochondrosis is a generalized disorder. Local conditions in the joints may play an important part for the osteochondrosis complex (Grondalen, 1974b). This study did not show any positive correlations (in a mathematics meaning) between leg weakness traits and osteochondral changes in the joints (Table IO). Osteochondrosis has been stated as the primary cause of leg weakness, and the relationship between these traits has been investigated. The relationship was not always possible to demonstrate, however (Thurley, 1969; Grondalen, 1974~; Reiland et al., 1978; Empel, 1980; Goedegebuure et al., 1988), and the explanation might be that only severe joint lesions cause an increase in the clinical signs of leg weakness (Grondalen, 1974~; Bring-Larsson and Sundgren, 1977; Lundeheim, 1987). In the present study the prevalences of severe joint lesions (osteochondritis dissecans) were low compared with the previously mentioned investigations, so this hypothesis could not be examined.
Acknowledgements Dr. E. Jorgensen and Dr. D. Sorensen, National Institute of Animal Science and Dr. S. Andersen, The Federation of Danish Pig Producers and Slaughterhouses have provided helpful comments regarding the statistics. Dr. Ame Madsen has provided valuable comments on the manuscript. They are thanked for their assistance.
References Bereskin, B., 1979. Genetic aspects of feet and legs soundness swine. J. Anim. Sci., 48: 1322-1328.
in
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Bring-Larsson K. and Sundgren P.-E., 1977. Studier over risrelsestijmingar hos svin. Reports Agric. Coll. Sweden, 284.30 pp. Calabotta, D.F., Komegay,E.T., Thomas, H.R., Knight, J.W., Notter, D.R. and Veit, H.P., 1982. Restricted energy intake and elevated calcium and phosphorus intake for gilts during growth. I. Feedlot performance and foot and leg measurements and scores during growth. J. Anim. Sci., 54: 565-575. Carlson, C.S., Hilley, H.D. Meuten, D.J. Hagan, J.M. and Moser, R.L., 1988. Effect of reduced growth rate on the prevalence and severity of osteochondrosis in gilts. Am. J. Vet. Res., 49: 396 402. Doige, C. and Horowitz, A., 1975. A study of articular surfaces and synovial fossae of the pectoral limb of swine. Can. J. Comp. Med., 39: 7-16. Duthie, I.F. and Lancaster, M.C., 1964. Polyarthritis and epiphyseolysis of pigs in England. Vet. Rec., 76: 263-273. Empel, W., 1980. Pathomorphological lesions in the skeleton and incidence of leg weakness syndrome in six month old Norwegian Landrace pigs. Ann. Wars. Agricult. Univ., Vet. Med., 10: 3338. Empel, W., Walach-Janiak, M. and Fandrejewski, H., 1980. Influence of intensity of feeding and protein body content on the incidence of osteochondrosis in six month old pigs. Ann. Wars. Agricult. Univ., Vet. Med., 10: 39-43. Goedegebuure, S.A., Hani, H.J., van der Valk, P.C. and van der Wal, P.G., 1980. Osteochondrosis in six breeds of slaughter pigs. I. A morphological investigation of the status of osteochondrosis in relation to breed and level of feeding. Vet. Q., 2: 2841. Goedegebuure, S.A., Rothschild, M.F., Christian, L.L. and Ross, R.F., 1988. Severity of osteochondrosis in three genetic lines of Duroc swine divergently selected for front leg-weakness. Livest. Prod. Sci., 19: 487-498. Grondalen, T., 1974a. Osteochondrosis and arthrosis in pigs. 1. Incidence in animals up to 120 kg live weight. Acta Vet. Scand., 15: l-25. Grendalen, T., 1974b. Osteochondrosis and arthrosis in pigs. VI. Relationship to feed level and calcium, phosphorus and protein levels in the ration. Acta Vet. Scand., 15: 147-169. Grendalen, T., 1974~. Leg weakness in pigs. I. Incidence and relationship to skeletal lesions, feeding level, protein and mineral supply, exercise and exterior conformation. Acta Vet. Scand., 15: 555-573. Grondalen, T. and Vangen, O., 1974. Osteochondrosis and arthrosis in pigs. V. A comparison of the incidence in three different lines of the Norwegian Landrace breed. Acta Vet. Stand., 15: 61-79. Hanssen, J.T. and Grendalen, T., 1979. The effect of different dietary factors on growth and development in young boars and gilts. Z. Tierphysiol., Tiem&hrg. u. Futtermittelkde., 42: 65-83. Henderson, C.R., 1953. Estimation of variance and covariance components. Biometrics, 9: 226-252. H&ii, H., Troxler, I. und W=ursten, B., 1983. Untersuchungen zum Einfluss der Haltung auf Verbreitung und Schweregrad von Osteochondrosis (OC) bei Mastschweinen. Schweiz. Arch. Tierheilk., 125: 453-475. Jorgensen, B. and Vestergaard, T., 1990. Genetics of leg weakness in boars at the Danish pig breeding stations. Acta Agric. Scand., 40: 59-69.
Lundeheim, N., 1987. Genetic analysis of osteochondrosis and leg weakness in the Swedish pig progeny testing scheme. Acta Agric. Scand., 37: 159-173. Nakano, T., Aheme, F.X. and Thompson, J.R., 1979. Effects of feed restriction, sex and diethylstilbestrol on the occurence of joint lesions with some histological and biochemical studies of the articular cartilage of growing-finishing swine. Can. I. Anim. Sci., 59: 491-502. Nakano, T., Aheme, F.X. Brennan, J.J. and Thompson, J.R., 1984. Effect of growth rate on the incidence of osteochondrosis in growing swine. Can. J. Anim. Sci., 64: 139-146. Nakano, T., Brennan, J.J. and Aheme, F.X., 1987. Leg weakness and osteochondrosis in swine: A review. Can. J. Anim. Sci., 67: 883901. Olsson, S-E and Reiland, S., 1978. The nature of osteochondrosis in animals. Summary and conclusions with comparative aspects on osteochondritis dissecans in man. ActaRadiol. Suppl., 358: 299306. Piedratita, J., Rothschild, M.F. and Christian L.L., 1991. Differential response to restricted feeding in two divergent lines of Duroc swine selected for front-leg structure. J. Anim. Breed. Genet., 108: 139-146. Reiland, S., 1978a. Pathology of so-called leg weakness in the pig. Acta Radiol. Suppl., 358: 23-14. Reiland, S., 1978b. Morphology of osteochondrosis and sequelae in pigs. Acta Radiol. Suppl., 358: 45-90. Reiland, S., 1978~. Effects of vitamin D and A, Ca, P, and protein on frequency of osteochondrosis in pigs. An experimental investigation. Acta Radiol. Suppl., 358: 91-106. Reiland, S., Ordell, N., Lundeheim, N. and Olsson, S.-E., 1978. Heredity of osteochondrosis, body constitution and leg weakness in the pig. Acta Radiol. Suppl., 358: 123-137. Rothschild, M.F. and Christian, L.L., 1988. Genetic control of frontleg weakness in Duroc swine. I. Direct response to five generations of divergent selection. Livest. Prod. Sci., 19: 459-471. Rothschild, M.F., Christian, L.L. and Jung, Y.-C., 1988. Genetic control of front-leg weakness in Duroc swine. II. Correlated responses in growth rate, backfat and reproduction from five generations of divergent selection. Livest. Prod. Sci., 19: 473485. SAS Institute Inc., 1988. SAS/STATTMUser’s Guide, Release 6.03 Edition. Gary, N.C: SAS Institute Inc., 1028 pp. Serensen, M.T., Jergensen, B. and Danielsen, V., 1993. Different feeding intensity of young gilts: Effect on growth, milk yield, reproduction, leg soundness, and longevity. Report No. 14 from National Institute of Animal Science, Denmark, 20 pp. (in Danish with English abstract and subtitles). Thurley, D.C., 1969.Changes in the epiphyseal cartilage of immature pigs without clinical lameness. Path. Vet., 6: 217-226. Wal, P.G. van der, Valk, P.C. van der, Goedegebuure, S.A. and Essen, G. van, 1983. Do gilts and barrows react similarly with respect to leg weakness and osteochondrosis? Vet. Q., 5: 175177. Webb, A.J., Russel, W.S. and Sales, D.I., 1983. Genetics of leg weakness in performance-tested boars. Anim. Prod., 36: 117130.
B. J@gensen /Livestock Production Science 41 (1995) 171-181 Wilson, R.D., Christian, L.L. and Schneider, J.F., 1980. The effects of sire soundness classification and feed restriction on perform-
181
ante and leg scores of pigs. J. Anim. Sci., 5 1, Suppl. 1: 132. (Abstr.)
R&urn6 Jorgensen, B., 1995. Effets de differents niveaux d’apports d’energie et de proteines sur la faiblesse des pattes et l’osteochondrose LiI;esr. Prod.Sci.,41: 171-181.
chez le port.
Les effets des apports d’energie, de proteines et du sexe sur la faiblesse des panes et l’osteochondrose ont et6 etudies sur le port charcutier. et les correlations entre ces caracteres ont et6 estimees. L’exp&ience portait sur 300 ports croises males c&r& et femelles, recevant des regimes a trois taux de proteines en alimentation ration&e ou ad libitum. Les ports Btaient notes sur 14 caracteres de faiblesse des pattes different% et une note d’osteochondrose &it attribuQ au coude et a l’articulation du carpe apms l’abattage. Les apports d’energie affectaient dans le meme sens trois des caracters de faiblesse des pattes et la “note globale de faiblesse des pattes”: les ports nourris ad libitum avaient des prob&mes plus prononces que ceux qui etaient ration&. I1 n’y avait pas d’effet du niveau d’energie sur l’osttochondrose. Les apports de proteines et le sexe n’affectaient ni la faiblesse des pattes, ni l’osteochondrose. Les lesions osteochondrales du condyle hum&al median Btaient corr&es avec les changements du radius proximal: a&e proximale du radius ( r = 0.17, P < 0.05) et fosse synoviale du radius ( r = 0.28, P < 0.0 1) Cependant, il n’y avait pas de correlation significative entre les changements au coude et a l’articulation du carpe. 11n’y avait pas de correlation entre les caracteres de faiblesse des pattes et l’osteochondrose, ce qui pourrait &tre dfl au fait que la prevalence de lesions severes des articulations (osteochondritis dissecans) etait t&s faible.
Kurzfassung Jorgensen, B., 1995. Die Wirkung verschiedener Prod. Sci.,41: 171-181 (aufenglisch).
Energie- und Proteinniveaus
auf Beinschwkhe
und Osteochondrosis
bei Schweinen.
Lioesl.
Die Wirkung des Energie- und Proteinniveaus, sowie des Geschlechts auf Beinschwache und Osteochondrosis bei Schlachtschweinen wurde untersucht und die Korrelationen zwischen diesen Merkmalen wurden beurteilt. Der Versuch bestand aus 300 gekreuzten Kastraten und Jungsauen, die entweder restriktiv oder ad libitum auf drei verschiedenen Proteinniveaus gefiittert wurden. Nach dem Schlachten wurden die Ellbogen und die Kniegelenke auf Osteochondrosis beurteilt. Das Energieniveau beeinflusste drei der BeinschwEheeigenschaften und die ‘gesamte Beinschwachebeurteilung’ in derselben Richtung: die ad libitum gefthterten Schweine zeigten ausgepragtere Probleme als die Schweine der restriktiven Gruppe. Das Energieniveau ermittelte keine Wirkung auf Osteochondrosis. Weder das Geschlecht noch das Proteinniveau hatten eine Wirkung auf das Vorkommen von Beinschwache oder Osteochondrosis. Osteochondrosale LIsionen im medialen humemlen Condylus waren mit einigen Gelenkveriinderungen im proximalen Radius korreliert: proximale Rand des Radius (r= 0.17, P < 0,05) und Synovialgrube des Radius (r= 0.28, P