Lameness and fertility of sows and gilts in randomly selected loose-housed herds in Finland

Lameness and fertility of sows and gilts in randomly selected loose-housed herds in Finland M. Heinonen, J Oravainen, T. Orro, L. Seppä-Lassila, E. Ala-Kurikka, J. Virolainen, A. Tast, O. A. T. Peltoniemi The prevalence of lameness among 646 sows and gilts in 21 selected herds was determined; 8 8 per cent of the animals were lame and the most common clinical diagnoses were osteochondrosis, infected skin lesions and claw lesions. The lame animals had higher serum concentrations of haptoglobin and C-reactive protein than the sound animals. Animals housed on slatted floors had twice the odds of being lame and 3 7 times the odds of being severely lame than animals housed on solid floors. Yorkshire pigs had 2 7 times the odds of being lame than Landrace or crossbred animals. Higher parity and the use of roughage decreased the odds of the sows not becoming pregnant; however, lameness was not a risk factor for non-pregnancy. Veterinary Record (2006) 159, 383-387 M. Heinonen, DVM, PhD, DipECVPH, J. Oravainen, DVM, T. Orro, DVM, L. Seppä-Lassila, BVetMed, E. Ala-Kurikka, DVM, J. Virolainen, DVM, MVetSci, PhD, A. Tast, DVM, MVetSci, PhD, O. A. T. Peltoniemi, DVM, MVetSci, PhD, DipECAR, Faculty of Veterinary Medicine, University of Helsinki, Saari Unit, Pohjoinen pikatie 800, 04920 Saarentaus, Finland LAMENESS is a very common problem among sows and one of the most common reasons for culling them; although it is not considered among the main reasons for mortality of sows (Chagnon and others 1991), lameness adversely affects their welfare. Lameness has been claimed to be associated with reduced fertility (Penny 1980), but the association has not been established scientifically in pigs. In cattle, lameness was associated with a decrease in conception rate and an increase in the median number of days open (Lee and others 1989). However, it is well known among practising veterinarians that lameness is a common problem in pig herds, and causes considerable economic losses. Various conditions resulting in lameness have been examined (Dewey 1999). However, changes in housing systems during recent years, from individual crates to group housing, are likely to have changed the situation. More information is needed on the risk factors for lameness and its prevalence, before its possible economic effects on sow herds, and potential preventive measures, can be evaluated. The acute phase response is the non-specific early response to infection and inflammation, during which the hepatic production of the so-called acute phase proteins, for example, haptoglobin and C-reactive protein, is increased. It has been suggested that measurements of acute phase proteins may be useful as diagnostic and prognostic aids and for monitoring the health of pigs (Heegaard and others 1998, Petersen and others 2004). Research has so far been focused mainly on young pigs; lame finishing pigs have high serum concentrations of haptoglobin (Petersen and others 2002a, b). Very little information is available on the use of acute phase proteins in sows. This paper describes a study designed to determine, first, the prevalence of lame animals of near-breeding status in herds with loose-housed dry sows and gilts. Measurements of haptoglobin and C-reactive protein were used as an indication of an acute phase reaction in lame animals under field conditions. The second aim was to identify the risk factors for lameness, severe lameness and non-pregnancy. MATERIALS AND METHODS Inclusion criteria The original study population included 151 sow herds with loose-housed dry sows and gilts that were participating in the Finnish National Litter Recording scheme run by the Finnish Animal Breeding Association and were within 150 km of the university clinic in southern Finland. In a pilot study, comparable with this study, 5 7 per cent of the animals were lame (Heinonen and others 2002). On the basis of the results of this pilot study and a maximal tolerable error of 0 1, it was calculated that 21 herds would be needed to estimate the prevalence of lameness (DiGiacomo and Koepsell 1986). Twenty-one of the 151 herds were therefore selected randomly for herd visits. The owners of four of these 21 herds were not willing to participate in the study; these herds were replaced with an equal number of randomly selected herds. Investigations The 21 herds were each visited once, and all the animals of near-breeding status gilts selected for breeding, sows and gilts up to 30 days after mating, lactating sows more than five days postpartum, and sows between weaning and mating were clinically examined. The herds had a median of 84 sows, with a range from 27 to 130. The housing system for the dry sows in each herd was recorded and the mean area available to each animal was measured. The farmer was interviewed on the use of roughage (straw or hay), and whether the animals were confined in stalls after mating, and if so, for how long. Information on the parity and breed of the animals and their reproductive status was also obtained. The body condition score of each animal was estimated on a scale of 1 (very thin) to 5 (very fat) (Ritter and others 1999). Each animal was assessed as sound, slightly lame or severely lame while it walked on a hard surface for at least 10 m. Animals that were housed on a soft surface with bedding were moved to passages between the pens and examined there. Lame animals were defined as those with one or more slightly or severely lame limbs. The diagnosis for the lame limbs was made clinically by a thorough inspection and palpation of the whole limb, including the claws. The animals were diagnosed with the following disorders: arthritis (painful, warm and swollen joint); osteochondrosis/osteoarthrosis (Hill 1990), that is, lameness with no obvious swelling of joints, but a shortened strike and walking on the tips of the hooves; an infected skin wound, with redness and swelling of the area surrounding the wound; a clearly visible lesion in the claw with no signs of infection, or an infected claw lesion (Gjein and Larssen 1995b) (swelling, necrosis or ulceration on the claw or on the coronary band); overgrown claws that clearly caused difficulty in walking properly; and nervous signs (ataxia of the hind part of the body). Acute phase proteins On each farm a clinically healthy control animal, matched by parity, reproductive status and breed, was selected for each lame animal, and a blood sample was taken from the

tail vein or saphenous vein of each lame and control animal. The samples were transferred in a cool box within four hours to the laboratory, where they were stored in the refrigerator until centrifuged the next day. The serum was stored at 18 C until analysed. C-reactive protein was measured with a commercial solid-phase sandwich immunosassay kit for pigs (Tridelta). Haptoglobin was measured by using the haemoglobinbinding assay for cattle (Makimura and Suzuki 1982) with slight modifications, in which tetramethylbenzidine (0 06 mg/ml) was used as a substrate (Alsemgeest and others 1994) and it was adapted for use with a microtitration plate. The assays were calibrated by using a reference porcine acute phase serum sample provided by the European Commission Directorate General Research Concerted Action Group (project number QLK5-CT-1999-0153) (Skinner 2001). All the samples were tested in duplicate by the same person, who had no information about the health status of each pig. Haemolysis of the samples was estimated visually, and haemolysed samples were excluded from the analyses for haptoglobin and grossly haemolysed samples from the analyses for C-reactive protein. Production data Information about mating or artificial insemination (AI), farrowing and culling was obtained from the central databank. For the statistical analyses the animals were classified as either pregnant (animals that farrowed after mating or AI at about the time of the herd visit) or non-pregnant (animals that did not farrow). Statistical methods A descriptive statistical analysis was performed. Each potential risk factor for the animal being lame or severely lame was screened. A univariate analysis was applied and associations between lameness and possible risk factors were tested with the chi-squared test. Variables with a P value less than 0 15 were retained in the multivariable analysis after testing the variables for correlation. The same procedure was used for non-pregnancy. There was no significant correlation between any of the variables. Biologically plausible interactions were sought. For lameness, the following interactions were investigated: AREA (area per animal) x CAGE (confinement in cage after mating), AREA x SLATTED (slatted floors), CAGE x SLATTED and SLATTED x ROUGHAGE (use of roughage). Similarly, the following interaction terms were investigated in the statistical analysis of non-pregnancy: AREA x SLATTED, CAGE x ROUGHAGE, CAGE x LAMENESS, LAMENESS x SLATTED, CAGE x SLATTED, AREA x CAGE and ROUGHAGE x SLATTED. The multivariate analysis was carried out by logistic regression with random effects, in which the herd was set as the random effect (STATA version 8.1). A backward stepwise elimination procedure with a cut-off level of P=0 05 was used. The acute phase protein results of the lame and sound control animals were compared by using the Wilcoxon signed rank test (Statistics; NetWare version 1). RESULTS TABLE 1: Clinical diagnoses, numbers of lame animals, degree of lameness and the affected limb, among 646 sows and gilts in 21 loose-housed herds Number of Degree of lameness Affected limb Clinical diagnosis animals Slight Severe Front Hind OC/OA 28 19 9 16 13 Infected skin wound 8 4 4 3 5 Arthritis 5 2 3 0 5 Claw lesions 6 4 2 2 4 Infected claw lesions 4 2 2 0 4 Overgrown claws 4 4 0 1 3 Nervous signs 2 0 2 0 2 Total 57 35 (61%) 22 (39%) 21 (37%) 36 (63%) OC/OA Osteochondrosis/osteoarthrosis Four of the herds used deep straw bedding, five used composting sawdust bedding, one used concrete floors with scant bedding, eight used partially slatted concrete floors and three used fully slatted floors. For the statistical analyses, the information on the housing systems was combined into two groups, one to include the 11 herds with slatted floors and the other the 10 without slatted floors. The mean (sd) area available to each pig was 3 0 (0 5) m 2. Eighteen herdsmen provided roughage for the animals, a median of 0 5 kg (range 0 1 to 1 5 kg) per animal per day, and three did not. In 15 of the herds the animals were not confined in stalls after mating, in two herds they were confined for a month and in four herds they were confined for several days. For the statistical analyses the herds were combined into two groups, one to include the 15 herds that did not confine the sows in stalls after mating or AI, and the other the six that confined them for between one and 30 days. A total of 667 animals were examined, but 21 had to be excluded from the study; information on the pregnancy status of 17 of them was not available from the central databank and the other four could not be moved out of their pens to estimate their lameness. The remaining 646 animals constituted a median of 45 2 per cent (range 25 0 to 61 4 per cent) of the animals in the herds. They had farrowed a median of 1 5 (0 to 12) times. Four of the animals had a body condition score of 1, 55 of 2, 329 of 3, 255 of 4 and three of 5. For statistical analysis the animals were combined into two groups: the 59 with scores of 1 or 2, and the 587 with scores of 3, 4 or 5. Fifty-seven (8 8 per cent) of the animals were lame, and of these, 22 (3 4 per cent of the total) were severely lame. A median of 7 0 per cent (range 0 to 27 3 per cent) of the animals in each herd were lame. Table 1 shows the clinical diagnoses, the severity of lameness and the limb affected. The levels of acute phase proteins were higher in the lame animals, especially the severely lame animals, than in the controls (Table 2). Table 2 also shows the acute phase protein results in relation to the diagnoses. A total of 119 animals (18 4 per cent) were culled before the next farrowing. Of 57 lame animals, 13 (22 8 per cent) TABLE 2: Median (range) of concentrations of haptoglobin (Hp) (g/l) and C-reactive protein (CRP) (mg/l) in lame and sound control sows and gilts and in sows and gilts with different diagnoses; one clinically healthy control animal matched by parity, reproductive status and breed was selected on each farm for each lame animal Lame animals Sound control animals P Lame (n=57) Hp (n=45) 2 2 (0 3-4 3) 1 8 (0 9-3 9) 0 09 CRP (n=51) 60 8 (0 5-341 1) 26 3 (2 5-201 5) 0 006 Severely lame (n=22) Hp (n=18) 2 5 (0 5-4 0) 1 8 (1 2-2 8) 0 02 CRP (n=21) 116 2 (13 5-250 0) 33 6 (3 7-162 8) 0 0004 OC/OA (n=28) Hp (n=23) 2 3 (0 3-3 4) 1 9 (1 1-3 9) 0 8 CRP (n=24) 64 4 (0 5-250 0) 41 8 (3 8-201 5) 0 2 Arthritis or skin infection (n=13) Hp (n=10) 2 3 (1 8-4 3) 1 6 (1 2-3 1) 0 05 CRP (n=12) 105 2 (20 5-341 1) 25 9 (3 7-200 1) 0 05 Claw disorders (n=14) Hp (n=10) 1 7 (1 1-3 0) 1 7 (0 9-2 8) 0 5 CRP (n=13) 16 9 (5 0-162 0) 16 6 (2 5-113 9) 0 3 Nervous signs (n=2) Hp (n=2) 2 5 (2 5, 2 6) 2 3 (2 2, 2 4) * CRP (n=2) 143 0 (121 2, 164 7) 42 1 (14 3, 69 9) * * Too few animals for statistical analysis OC/OA Osteochondrosis/osteoarthrosis

TABLE 3: Univariate analysis of the risk factors for lameness and severe lameness in 21 randomly selected loose-housed herds of sows and gilts Number Lame Severely lame Variable Characteristic of herd of animals animals (%) P animals (%) P Herd size <84 sows 344 10 2 3 5 84 sows 302 7 3 0 20 3 6 0 9 Breed Landrace 292 6 8 3 1 Yorkshire 78 16 7 3 8 Crossbred 273 8 4 0 02* 4 0 0 8 Parity Gilts 192 9 9 3 6 Primiparous 130 10 0 4 6 Multiparous 322 7 4 0 50 3 1 0 7 Body condition score 1 and 2 (thin) 59 6 8 6 8 3, 4 and 5 (moderate to fat) 587 9 0 0 70 3 2 0 3 Type of loose housing No slats 279 6 1 1 4 Slatted floor 367 10 9 0 05* 5 2 0 02 Area per animal Less than 2 m 2 29 10 3 3 4 2-3 m 2 194 9 3 5 1 More than 3 m 2 423 8 5 0 90 2 8 0 3 Animals confined in stalls after mating No 415 9 4 3 6 Yes, 1-30 days after mating 231 7 8 0 50 3 4 0 9 Usage of roughage No 122 9 8 5 7 Yes 524 8 6 0 70 3 0 0 15 Interaction term AREA x CAGE 0 03* 0 08 * Variables included in the logistic regression model for lameness Variables included in the logistic regression model for severe lameness Interaction term: area per animal x confinement in cage 0 to 30 days after mating were culled, four (7 0 per cent) for lameness, three (5 3 per cent) for other conditions and six (10 5 per cent) for fertility problems. Similarly, of 589 sound animals 106 (18 0 per cent) were culled, 17 (2 9 per cent) for lameness, 24 (4 1 per cent) for other conditions, 50 (8 5 per cent) for fertility problems and 15 (2 5 per cent) for managemental reasons. The following factors were included in the multivariable logistic regression model for lameness, with herd as a random effect (Table 3, univariate analysis): breed, type of loose housing (with or without slatted floors) and the interaction term AREA x CAGE. The final multivariate model is shown in Table 4. Similarly, the type of loose housing, the use of roughage and the interaction term AREA x CAGE were included in the model for severe lameness (univariate analysis, Table 3), but only the type of housing remained a significant factor in the final model (Table 4). Of the 646 animals, 68 3 per cent became pregnant at about the time of the herd visit. More than half of the variables that were associated with not becoming pregnant (P 0 15) in the univariate analysis (Table 5) were not retained in the final multivariate model, including parity and the use of roughage (Table 6). DISCUSSION The results show that the availability of roughage, the type of loose housing and the parity and breed of the sows had TABLE 4: Final multivariate logistic regression models with farm as a random effect for the animal being lame and severely lame in 21 randomly selected loose-housed herds Variable Parameter b (se) P OR (95% CI) Model for Constant 3 03 (0 31) <0 001 being lame Breed Landrace Yorkshire 0 99 (0 38) 0 01 2 7 (1 3-5 8) Crossbred 0 16 (0 32) 0 6 1 2 (0 6-2 2) Housing No slatted floors Slatted floors 0 70 (0 31) 0 02 2 0 (1 1-3 7) Model for Constant 4 23 (0 50) <0 001 being severely Housing No slatted floors lame Slatted floors 1 32 (0 55) 0 02 3 7 (1 3-11 2) OR Odds ratio, CI Confidence interval, b Coefficient significant effects on their fertility and the prevalence of lameness. Lameness is always a severe problem in sow herds, and the measurements of acute phase proteins appeared to be useful in evaluating the inflammatory process in these lame pigs under field conditions. The prevalence of lame sows was quite high; almost 10 per cent of the animals were diagnosed as lame, but their owners had not observed or reacted to their condition. Similar findings were observed in a study of sows in late pregnancy, among which the mean prevalence of lameness was 9 6 per cent (range 0 8 to 20 1 per cent) (Holmgren and others 2000). In herds of dry sows loose-housed on partly slatted floors, the mean prevalence of hindleg lameness was 13 1 per cent (Gjein and Larssen 1995b). In an epidemiological study by Lingaas and Ronningen (1991), the incidence of hoof or joint diseases was only 0 37 to 1 71 per farrowing, suggesting that the disease may not be common or may not be treated. However, lameness can cause severe discomfort or pain, and lame animals should not be left untreated. There has been much research concerning the reasons for culling sows, but little on the prevalence of lameness under field conditions. Lameness has been reported as a significant cause of culling or mortality; for example, the mean yearly culling rate for lameness was 11 per cent in sows and 13 per cent in gilts, but in many herds it may be much higher (Dewey 1992), in agreement with the present results. The most common causes of lameness in breeding-age animals are osteochondrosis/osteoarthrosis, infectious arthritis and foot lesions (Dewey and others 1993); osteochondrosis is especially prevalent in young breeding animals, but in animals more than one to one-and-a-half years of age the condition has been reported to be less common or may have resolved (Grondalen 1974); it may have been common in the present study because the animals were young. In a study by Flesjå and Ulvesaeter (1979), the diagnosis arthritis or polyarthritis was recorded in about 2 6 per cent of apparently healthy sows at the slaughterhouse; however, these conditions were recorded in a similar proportion of baconers, and no attempt was made to differentiate between osteochondrosis and arthritis, a distinction that would have provided valuable information on which to base preventive measures. In the present study, foot lesions were a common cause of lameness, especially in the hindlegs. In studies by Gjein and Larssen

(1995a, b) the mean herd prevalence of claw lesions in herds loose-housed on partially slatted floors was about twice as high as in herds with individual housing, and claw infections were also more prevalent in herds with dirty floors and with little space per animal. The results of the present study agree well with the results of earlier studies, even though the diagnoses were only clinical. Making these diagnoses was difficult, and the cases were therefore divided into rough groups of diagnoses. The diagnosis of osteochondrosis/osteoarthrosis is particularly difficult, if not impossible, to make in a living animal. The levels of acute phase proteins were higher in the severely lame adult animals than in the sound controls, in agreement with the results obtained with lame finishing pigs by Petersen and others (2002a, b). However, in the control (sound) adult animals in the present study, the overall level of haptoglobin was higher than the levels of adult animals studied by Richter (1974), and higher than the level in young animals (Heegaard and others 1998). In a recent study by Hiss and Sauerwein (2003), the levels of haptoglobin in twomonth-old piglets were comparable with the present results. Other factors such as herd, reproductive status, diet and milk yield may also influence the levels of acute phase proteins. In the present study, the variations between herds (Petersen and others 2002b) were eliminated by selecting the control animals from the same herd. In agreement with the results of Petersen and others (2004), there was a larger response in C-reactive protein than in haptoglobin. The levels of acute phase proteins are associated with the timing of the sampling; after experimental actinobacillosis, maximum levels were reached after two to five days, with C-reactive protein reacting more rapidly than haptoglobin (Heegaard and others 1998). The response is detectable for days but is affected by the extent of tissue damage (Petersen and others 2004). In chronic conditions such as arthritis, consecutive series of inflammatory stimuli occur and increased concentrations of acute phase proteins can be detected (Petersen and others 2004). The effects of chronic and recurrent infections, which are commonly encountered in practice, need further investigation (Heegaard and others 1998). In the present study, a small number of animals had conditions causing severe tissue damage, such as arthritis and skin infections, these animals had significantly increased levels of acute phase protein. The changes in acute phase proteins are non-specific and therefore cannot be used to establish a definitive diagnosis, but they can provide objective information about inflammatory processes (Petersen and others 2004) and may help in the follow-up of treatments for different conditions causing lameness. Housing and management influence the incidence of lameness and foot lesions indirectly by affecting the number and type of movements the pigs can make (Kroneman and others 1993b). Under natural conditions, the ground is usually soft and damp; when pigs are kept indoors, the flooring should be non-slippery, non-abrasive and provide a sound footing. The finding that slatted floors were a risk factor for lameness agrees with the findings of earlier work. There were fewer hoof lesions among the sows on straw bedding than among those on solid concrete floors and partly slatted floors (Ehlorsson and others 2002). In group-housed sows there was a higher prevalence of claw and leg injuries among sows kept in concrete pens than among sows with straw bedding (Holmgren and others 2000). Mouttotou and others (1999) studied the effect of floor type on the foot lesions of finishing pigs; they found that pigs kept on soft floors had a lower prevalence of sole erosions, heel erosions and heel flaps, but a higher prevalence of white line lesions, false sand cracks, wall separations and toe erosions than pigs kept on solid TABLE 5: Univariate analysis of the risk factors for sows or gilts not to become pregnant in 21 randomly selected loose-housed herds Non-pregnant Number of Variable Characteristic of herd (%) animals P Herd size <84 sows 28 8 344 84 sows 31 1 302 0 1* Breed Landrace 34 2 292 Yorkshire 34 6 78 Crossbred 28 2 273 0 3 Parity Gilts 41 7 192 Primiparous 30 8 130 Multiparous 26 3 322 0 001* Body condition score 1 and 2 (thin) 32 2 59 3, 4 and 5 (moderate to fat) 31 9 587 0 9 Lameness Sound 31 8 589 Slightly or severely lame 31 6 57 0 9 Severe lameness Sound or slightly lame 31 1 623 Severely lame 47 8 23 0 1* Type of loose housing No slats 29 8 279 Slatted floors 33 3 367 0 4 Area per animal Less than 2 m 2 27 6 29 2-3 m 2 28 9 194 More than 3 m 2 33 3 423 0 5 Animals confined in stall No 31 3 415 after mating Yes, 1 to 30 days after mating 32 5 231 0 8 Use of roughage No 49 9 122 Yes 27 7 524 0 0001* Interaction term AREA x SLATTED 0 02* * Variables included in the logistic regression model for becoming pregnant Interaction term: area per animal x use of slatted floors concrete floors. Mild claw lesions were not associated with lameness, but the risk of lameness increased as the severity of the lesions increased and if they became infected (Gjein and Larssen 1995b). However, Kroneman and others (1993a) observed no significant differences between the frequency of claw lesions in lame and non-lame limbs. In addition to the type of floor, its slipperiness, abrasiveness, surface profile and cleanliness, and the ability of the animals to move about and thus avoid fighting, play a role in the development of lesions and the prevalence of lameness (Kroneman and others 1993b). The results did not support the hypothesis that lame animals would be less likely to become pregnant. In the univariate analysis, severe lameness appeared to be associated with lower fertility, but this association disappeared in the multivariable analysis. In cows, lameness after calving was associated with significantly increased intervals from calving to conception (Collick and others 1989). No association could be found between lameness in sows during the last month of pregnancy and the numbers of piglets born alive, stillborn piglets or their birthweights (Kroneman and others 1993a), but the animals were not followed up until the next mating. The fact that the provision of roughage was associated with the proportion of sows becoming pregnant was not surprising; similar results were found in a study of 1298 herds by Peltoniemi and others (1999b). The use of relatively young sows in the present study may have amplified TABLE 6: Final multivariate logistic regression model with farm as a random effect for risk factors for sows or gilts not to become pregnant in 21 randomly selected loose-housed herds Variable Parameter b (se) P OR (95% CI) Constant 0 43 (0 22) 0 06 Parity Gilt Primiparous 0 54 (0 24) 0 03 0 6 (0 4-0 9) Multiparous 0 71 (0 20) <0 001 0 5 (0 3-0 7) Use of No roughage Yes 0 95 (0 21) <0 001 0 4 (0 3-0 6) OR Odds ratio, CI Confidence interval, b Coefficient

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