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Quantifying the impact of lameness on welfare and profitability of finisher pigs using expert opinions
Livestock Science 149 (2012) 209–214
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Livestock Science journal homepage: www.elsevier.com/locate/livsci
Quantifying the impact of lameness on welfare and profitability of finisher pigs using expert opinions T.B. Jensen n, H.H. Kristensen, N. Toft Department of Large Animal Sciences, Faculty of Life Sciences, University of Copenhagen, Grønneg˚ ardsvej 2, DK-1870 Frederiksberg C, Denmark
a r t i c l e i n f o
abstract
Article history: Received 2 January 2012 Received in revised form 9 July 2012 Accepted 16 July 2012
Lameness in finisher pigs affects both animal welfare and farmers’ profitability. However, information about the severity of pain and profit losses associated with individual causes of lameness is lacking. This study quantified and compared the pain and economic impact of nine different causes of lameness (e.g., infectious arthritis, claw lesions and osteochondrosis) using expert opinion. Six researchers working on animal behaviour and welfare and eight Danish pig veterinarians answered questionnaires regarding animal welfare and production, respectively. The probability of euthanasia, treatment with antibiotics and analgesics, and the changes in daily weight gain and feed conversion ratio were used to calculate the resulting profit loss for a pig suffering from each of the nine causes. To accommodate the uncertainty associated with the expert assessments, simulations were performed using probability distributions based on the minimum, median and maximum values. According to the experts, bone fractures caused the highest severity of pain and the largest reduction in profitability. Lesions to the claw wall and lesions to the volar area of the foot caused the lowest severity of pain. Arthritis due to Mycoplasma hyosynoviae and lesions to the volar area of the feet caused the smallest reduction in profitability. Considering the consequences of animal welfare and profitability concomitantly provides a transparent evaluation of the overall impact of lameness in finisher pigs. & 2012 Elsevier B.V. All rights reserved.
Keywords: Animal welfare Expert opinion Lameness Pig Profitability
1. Introduction The increased focus on animal welfare in society today emphasises the need to obtain quantitative information in order to investigate the economic consequences of improving or not improving animal welfare. Though several studies have focused on quantifying the effects of endemic and epidemic animal diseases (e.g., Bennett, 2003; Boklund et al., 2009) only limited efforts have been made to determine the effects of animal welfare in an economic context. n Corresponding author at: Present address: Danish Veterinary and Food Administration, Stationsparken 31-33, DK-2600 Glostrup, Denmark. E-mail address: [email protected] (T.B. Jensen).
1871-1413/$ - see front matter & 2012 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.livsci.2012.07.013
A common disease complex affecting the welfare of finisher pigs are leg disorders causing clinical signs of lameness (Busch et al., 2003). Clinical signs of lameness are most often caused by infectious arthritis, physical injuries or osteochondrosis (Jensen and Toft, 2009). Lameness is a sign that movement may be associated with pain (Busch et al., 2003). Besides affecting animal welfare negatively, clinical signs of lameness also have a negative impact on productivity and hence, economy (Jensen et al., 2007). Lameness in growing-finisher pigs has been found to be the third most common reason for antibiotic treatment in finisher herds (Christensen et al., 1994). Moreover, pigs with clinical signs of lameness have an increased risk of being euthanized (Engblom et al., 2008). As lameness in finishers affects both the animals and the farmers, there is a need to measure and compare the
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consequences of lameness on both animal welfare and profitability. Assessing the consequences of different causes of lameness may be a demanding task, partly due the limited information of effects of lameness on production in individual pigs, and partly due to the multidimensional nature of animal welfare. This challenges the assessment of the impact of lameness on the welfare of individual pigs. However, expert opinion has previously been found to be valuable in order to obtain inaccessible information in regard to both leg disorders (Jensen et al., 2009) and animal welfare (Rodenburg et al., 2008). Animal welfare is a multidimensional concept that can be based on the five freedoms (FAWC, 1992): (1) freedom from thirst and hunger, (2) freedom from discomfort, (3) freedom from pain, injury and disease, (4) freedom to express normal behaviour and (5) freedom from fear and distress. Pain may have a large effect on the welfare and behaviour of individual animals (Phillips, 2007). Hence, the pain involved in lameness may influence all five freedoms (Anil et al., 2009). In this study, we therefore used the level of pain as a proxy for the overall welfare of individual animals. The overall objective of this study was, through the use of expert information, to quantify the impact of different causes of lameness on pain and productivity in order to investigate the relationship between animal welfare and profitability in individual finisher pigs. This will be the first step in aggregating the consequences of lameness to the herd level. 2. Materials and methods This study deals with nine specific causes of leg disorders in finisher pigs (90–100 kg) that may cause clinical signs of lameness. The nine causes were selected as they are the commonest causes of lameness in finisher pigs (Jensen and Toft, 2009). The specific causes are infectious arthritis caused by (1) Mycoplasma hyosynoviae (M. hyosynoviae) (Nielsen et al., 2001), (2) Erysipelothrix rhusiopathiae (E. rhusiopathiae) (Buttenschøn et al., 1995), (3) Haemophilus parasuis (H. parasuis) (Nedbalcova et al., 2006) and (4) Streptococcus suis (S. suis) (Clifton-Hadley et al., 1986), physical injuries such as (5) bone fractures of the leg(s), (6) lesions to the claw wall (which includes white line lesions and wall lesions) (Penny et al., 1963) and (7) lesions to the volar area of the feet (which includes sole, toe and heel erosions) (Penny et al., 1963). Additionally, two different manifestations of osteochondrosis are considered: (8) osteochondrosis manifesta (OCM), where a thickened and uneven cartilage is observed and (9) osteochondrosis dissecans (OCD), where lesions of fissured articular cartilage are observed (Ytrehus, 2004). 2.1. Expert questionnaires Two questionnaires were conducted in May 2010 focusing on the consequences of the nine causes of lameness on animal welfare and production. The questionnaire focusing on animal welfare was sent by e-mail to eight scientists from four different countries (Finland,
Sweden, UK and Denmark) with expertise in animal behaviour and welfare. The welfare experts were selected on the basis of their previous work on lameness, pain and welfare as well as their likely knowledge of the nine diagnoses of leg disorders. Likewise, the questionnaire dealing with production consequences was sent by e-mail to 10 Danish veterinarians with several years of experience in pig health and production. The production experts were selected based on their specialisation and working experience as pig veterinarians as well as interest in pig leg health. The welfare and production experts were selected from different criteria, and only three experts participated in both welfare and production questionnaires. The severity of pain was used as a proxy for the level of animal welfare for each cause of lameness. Hence, for each cause of lameness, the welfare experts were asked to evaluate on an arbitrary scale from 0 to 100, the severity of pain that a lame pig would experience (pain index scale). On the pain index scale 100 was equivalent to insufferable pain, 75 was severe pain, 50 was equal to moderate pain, 25 equalled mild pain and 0 equalled no pain (modified from Morton and Griffiths. (1985)). For each of the different lameness causes, the 10 production experts were asked about the probability of a pig being euthanized (0–100%), and the probability of a pig being treated with antibiotics and analgesics (0–100%). Moreover, the experts evaluated the likely change in the average daily weight gain (ADG) from 100 g/day to þ100 g/day, and feed conversion ratio (FCR) from þ0.3 feed units per kilogram weight gain (FU/kg) to 0.3 FU/kg for a pig suffering from each of the nine specific causes of lameness. 2.2. Simulation of the loss in profitability The expert information regarding the consequences of each of the nine causes was used to form probability ¨ et al., distributions, using the BetaPert distribution (Stark 2000; Vose, 2008), which expresses the uncertainty about a parameter using the minimum, maximum and most likely value. This distribution is commonly used to represent expert opinion in a wide range of fields. For this study, we used the median response from the experts as the most likely value, and the maximum and minimum individual response as minimum and maximum values to the BetaPert distribution. Prices in the study reflected the price level in 2010. As presented in Eq. 1, the profit margin of a pig is the difference between the total revenue and the variable costs. Profit margin ¼ V s C F C M C PIGLET
ð1Þ
where, VS is the slaughter value of a pig, CF is the feed cost of a pig during the entire finishing period, CM is the cost of medicine (antibiotics and analgesics) and CPIGLET corresponds to the cost of a piglet at 30 kg (assumed to be 325 DKK in this study). The formula for the slaughter value (VS) is given in Eq. 2. V S ¼ W i þðADG þ DADGÞ*D*Ratio*Pr s *ð1Peu Þ
ð2Þ
T.B. Jensen et al. / Livestock Science 149 (2012) 209–214
where, Wi is the initial weight of a pig in the finisher unit (30 kg). ADG is the average daily weight gain of a finisher pig without lameness, which in this study is set to be 0.85 kg/day, and DADG is the change in the ADG due to the cause of lameness. D is the time (in days) a pig on average will spend in the finisher unit. We assume a pig ideally will be sent to slaughter at 100 kg, and the ADG is 0.85 kg/ day, the total time equals 82 day. Ratio represents the conversion ratio between live weight and carcass weight, which in this study is set to 0.76 (Udesen, 1997). Prs is the price of one kilogram carcass meat (8.5 DKK/kg in this study) and Peu is the probability of euthanisation of a pig with a specific cause of lameness. The formula for the feed cost (CF) is given in Eq. 3. C F ¼ ðDPeu *D=2Þ*ðADGþ DADGÞ*ðFCRþ DFCRÞ*Pr F
ð3Þ
where FCR is the average feed conversion ratio (FCR), which in this study is set to be 2.8 FU/kg, and DFCR is the change in FCR due to the cause of lameness. PrF is the price of one feed unit (in this study 1.1 DKK/FU). In Eq. 3, time of euthanasia is assumed to be in the middle of the period a pig is placed in the finisher unit. Finally, the formula for the medicine cost (CM) is given in Eq. 4. C M ¼ P AB *C AB þP AN *C AN
ð4Þ
where PAB is the probability of a pig being treated with antibiotics and CAB is the cost of a commonly practised three day treatment with antibiotics (20 DKK). Likewise, PAN is the probability of a pig being treated with analgesics and CAN is the price of a three day treatment with analgesics (180 DKK). Using Eqs. (1–4), a pig that does not suffer from any cause of lameness has a profit margin of 104 DKK. The loss in profitability of a pig experiencing a particular cause of lameness was calculated in the interval from 30 kg until slaughter by subtracting the profit margin of a pig without lameness (104 DKK) from the profit margin of a pig with a particular cause of lameness (Eqs. 1–4).
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3. Results 3.1. Impact on pain Out of eight researchers in animal behaviour and welfare, six replied back corresponding to a response rate of 75%. Based on the median values of the expert opinions, bone fractures was the cause of lameness associated with the highest severity of pain (median value ¼90 on the arbitrary scale) (Table 1). This was followed by osteochondrosis dissecans (median value¼67.5) and infectious arthritis caused by S. suis (median value¼65). However, the variation in the expert opinions was considerably higher for these last two causes then for bone fractures. The lowest severity of pain was associated with lesions to the claw wall (median value¼45) and lesions to the volar area of the feet (median value ¼45), however the minimum and maximum values showed a large variation in the answers given by the experts (Table 1).
3.2. Loss in profitability Eight out of 10 Danish veterinarians returned the production questionnaire. This corresponded to a response percentage of 80%. From the experts’ opinions, pigs suffering from bone fractures had 90% (median value) risk of being euthanized (Table 2). The probabilities of euthanasia when a pig suffered from lameness due to other causes than bone fractures were lower (median value r40%). However, these probabilities varied considerably compared to that of bone fractures. Pigs suffering from one of the four infectious pathogens causing arthritis or bone fractures had the highest probability of being treated with antibiotics (median values¼80–90%). On the other hand, lesions to the claw wall and lesions to the volar area of the feet had the lowest probability of being treated with antibiotics (median value¼10%). With a minimum value of 0% and a maximum value of 100%, there were large variations in the answers from the experts. With regard to the probability of
2.3. Simulation of the impact on pain Using the experts’ responses from the welfare questionnaire, the animal welfare consequences (i.e., pain) for each cause of lameness was simulated as a BetaPertdistribution using the median, minimum and maximum values reported by the experts as most likely, minimum and maximum values. 2.4. Modelling The simulation models for loss in profitability and impact on pain were both implemented in R (version 2.9.1) (R Development Core Team, 2006). For each cause 10,000 samples of consequences were simulated from the relevant distributions and used to calculate the profit loss and the impact on pain. The resulting loss in profitability and impact on pain were summarized using median, minimum and maximum values, as well as graphical illustrations of the central 95% probability mass for the combination of pain index and profit loss for each cause.
Table 1 Median, minimum and maximum values of six experts opinions regarding the severity of pain due to the nine causes of lameness. Cause of lameness
Median value
Fracture 90 Lesions to the claw wall 45 Lesions to the volar area of 45 the feet M. hyosynoviaea 57.5 E. rhusiopathiaeb 60 H. parasuisc 57.5 S. suisd 65 OCMe 55 f OCD 67.5 a
Mycoplasma hyosynoviae. Erysipelothrix rhusiopathiae. c Haemophilus parasuis. d Streptococcus suis. e Osteochondrosis manifesta. f Osteochondrosis dissecans. b
Minimum value
Maximum value
75 15 15
95 65 50
20 35 30 30 20 35
70 80 75 70 65 80
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Table 2 Median, minimum and maximum values (in parenthesis) of eight expert opinions regarding the production effects of the nine causes of lameness. Cause of
Consequences
lameness
Euthani-sation (%)
Treatment: antibiotic (%)
Treatment: analgesic (%)
DADGa (g/day)
Fracture Lesions to the claw wall Lesions to the volar area of the feet M. hyosynoviac E. rhusio-pathiaed H. parasuise S. suisf OCMg OCDh
90 (80, 90) 15 (0, 50) 10 (0, 30)
80 (50, 90) 10 (0, 100) 15 (0, 100)
10 (10, 70) 10 (0, 20) 10 (0, 30)
100 ( 100, 75) 0.25 (0,15, 0.30) 25 ( 100, 0) 0.1 (0, 0.30) 25 ( 100, 0) 0.075 (0, 0.30)
0 40 20 20 40 30
90 80 80 80 40 50
20( 0, 80) 20 (10, 70) 20 (10, 70) 20 (10, 50) 15 (0, 50) 20 (10, 50)
(0, 20) (10, 80) (10, 50) (10, 50) (0, 80) (10, 50)
(50, 100) (50, 100) (60, 100) (60, 100) (0, 100) (30, 100)
25 50 25 50 25 25
( 75, 0) ( 75, 25) ( 75, 25) ( 75, 25) ( 100, 0) ( 100, 0)
DFCRb (FU/kg)
0.05 0.15 0.1 0.15 0.1 0.05
(0, 0,15) (0.05, 0.30) (0.05, 0.25) (0.05, 0.25) (0, 0.30) (0, 0.30)
a
Average daily weight gain. Feed conversion ratio. c Mycoplasma hyosynoviae. d Erysipelothrix rhusiopathiae. e Haemophilus parasuis. f Streptococcus suis. g Osteochondrosis manifesta. h Osteochondrosis dissecans. b
treating with analgesics, the median values of the expert opinions for all nine causes were between 10 and 20%. The largest variations in the answers were seen among the causes: bone fractures and the four infectious pathogens. Answers in regard to the ADG and FCR also varied according to the experts. Yet, the experts agreed that pigs with a bone fractures had the highest reduction in ADG (median value¼ 100 g/day) and highest increase in the FCR (median value¼0.25 FU/kg) (Table 2). The highest reduction in profit margin based on production estimates was in pigs with bone fractures (median value¼ 409.9 DKK) (Table 3). Leg disorders caused by E. rhusiopathiae caused the second highest reduction (median value¼ 185 DKK); however, the variation was much larger than for bone fractures. The lowest reduction in the profit margin was associated with M. hyosynoviae arthritis (median value¼21 DKK) and lesions to the volar area of the feet (median value¼5.7 DKK) (Table 3). 3.3. The relationship between profit loss and pain impact The relationship between the impact on pain and the loss in profitability of an individual pig is illustrated in Fig. 1. Bone fractures had the greatest impact on both pain and profitability. The lowest impact on both profit and pain was seen for lesions to the claw wall and lesions to the volar area of the feet (Fig. 1). 4. Discussion Our study shows that of the nine causes of leg disorders, bone fractures had the highest impact on welfare as it caused the most pain and had the highest impact on profitability. Reducing the occurrence of bone fractures in finisher pigs has a large positive effect for both the individual animals as well as the farmer, and therefore, it is important to be able to distinguish bone
Table 3 Simulated median, minimum and maximum values of the loss in profitability (DKK) based on expert information regarding the nine causes of lameness. Cause of lameness
Median value (DKK)
Fracture 514 Lesions to the claw wall 131 Lesions to the volar area of 99 the feet M. hyosynoviaea 86 E. rhusiopathiaeb 290 c H. parasuis 191 S. suisd 190 OCMe 259 OCDf 214
Minimum value (DKK)
Maximum value (DKK)
466 27 15
597 295 198
17 112 101 102 39 99
197 523 344 321 488 346
a
Mycoplasma hyosynoviae. Erysipelothrix rhusiopathiae. c Haemophilus parasuis. d Streptococcus suis. e Osteochondrosis manifesta. f Osteochondrosis dissecans. b
fractures from other causes of lameness. In a study of 130 sows from one Swedish herd, 43% of the sows diagnosed with arthritis post mortem was expected to have a bone fracture based on a previous clinical examination (Engblom et al., 2008). Hence, diagnosing a bone fracture based on clinical examination of individual pigs can be uncertain as they may be confused with other causes of lameness. Correct distinction between bone fractures and arthritis in finisher pigs would potentially reduce the profit loss. Among the four infectious pathogens, infectious arthritis caused by E. rhusiopathiae had the highest economic impact and a large effect on animal welfare according to the experts. The reason for the high effect on profitability
T.B. Jensen et al. / Livestock Science 149 (2012) 209–214
Fig. 1. The relationship between median loss in profitability (DKK) and median pain (pain index) for an individual finisher pig. The bars indicate the minimum and maximum values for pain index and profit loss for each of the nine causes of lameness.
can be explained by the high probability of euthanasia compared with the other infectious pathogens. Pigs infected with E. rhusiopathiae have usually been infected at an early stage of life, and may suffer from bacteraemia and show clinical signs of a generalized infection. Their feet are often placed under the center of the body and their limbs are painful and swollen (Wood and Henderson, 2006). The fact that E. rhusiopathiae can cause severe arthritis in pigs, explains the higher probability of euthanasia and the large negative effect on both profitability and animal pain. On the other hand, M. hyosynoviae had the lowest impact on profitability and caused only mild pain. Infectious arthritis caused by M. hyosnoviae is considered to be less severe, and pigs with clinical signs of lameness usually recover spontaneously within one to two weeks (Friis, 1987). This may explain the low impact of arthritis caused by M. hyosynoviae seen in this study. Claw lesions had the lowest effect on animal pain, and also only a minor effect on profitability. Lesions to the claw are common findings among finisher pigs (Mouttotou et al., 1997). In a study of 15 Norwegian sow herds, only severe claw lesions and claw infections were associated with clinical signs of lameness in sows (Gjein and Larssen, 1995). In our study, lesions to the volar area of the feet and lesions to the claw wall were clinical expressions aggregating a number of specific clinical manifestations. A number of these clinical manifestations (e.g., sole and heel erosions) often do not penetrate the sensitive corium, and hence do not cause pain to the pig. This may explain the reduced effect of claw lesions on pain as well as production as evaluated by the experts. Pain was considered a simple and valid indicator of the overall welfare of individual pigs in this study (Phillips, 2007; Anil et al., 2009). The Welfare Quality Research project focused on developing an objective and operational
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way to assess animal welfare (Botreau et al., 2009). In the future, when more standardised methods are developed for measuring and aggregating different aspects of animal welfare into one numeric value, our knowledge of the relationship between animal welfare and production may be validated. A number of studies in animal welfare research have used expert opinion for the evaluation of the welfare of animals (Bracke et al., 2008; Rodenburg et al., 2008). The experts in our study were selected as highly specialised in pig welfare and production both in Denmark and internationally, and we used the median value as well as the maximum and minimum values to illustrate the variation in the answers given by experts. However, other methods of handling expert opinion are also used in the literature. In a study by Van der Fels-Klerx et al. (2002), a heterogeneous expert panel was used for the quantification of a continuous variable. The individual experts were weighted according to their expertise in that study. In our study equal weight was given for each expert in both animal welfare and production as they had been carefully selected beforehand. However, we cannot rule out that some experts did not have the same level of knowledge for all nine causes of lameness, and therefore, assigned higher scores to causes of which they had more specific knowledge. Results from our study are presented as the consequences for individual pigs. In modern pig production the effect of disease (e.g., lameness) on profitability is generally of interest at the herd level, and it is necessary to know the specific causes of lameness and their prevalence. However, the prevalence of the nine causes differs widely in a herd (Jensen et al., 2009). The prevalence of pigs with bone fractures in a herd is often low (o0.1%) (Baumann and Bilkei, 2002), whereas the prevalence of pigs with at least one claw lesion has been reported to be as high as 94% (Mouttotou et al., 1997). Knowing the specific cause and prevalence of lameness, it is possible to aggregate the production effects of individual pigs to the herd level, when taking into account specific herd information like herd size and production type (i.e., such as all in all out or continuous production). However, aggregating the animal welfare effects of individual pigs to the herd level is indeed more challenging as the animal welfare implications of different scenarios need to be evaluated and compared (e.g., one pig with a bone fracture compared to 10 pigs with claw lesions). Therefore, more research on aggregating the consequences of lameness to the herd level is needed. In conclusion, according to the welfare experts, bone fracture was the most painful leg disorder, with lesions to the claw wall and volar area of the feet being the least painful leg disorders in finisher pigs. The production experts also asserted a fractured limb as having the highest impact on profitability, and M. hyosynoviae and lesions to the volar area of the feet as having the lowest impact on profitability. By combining quantitative information of welfare and production aspects, it is possible to rank the overall consequences of different disorders. This not only highlights areas in need of attention, but also provides incentives to farmers for improving animal welfare in the future.
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Conflict of interest statement To Livestock Science, I hereby confirm that there is no conflict of interest in regard to the manuscript: ‘‘Quantifying the impact of lameness on the pain and profitability of finisher pigs using expert opinions’’. On behalf of the authors of the manuscript, Tina Birk Jensen.
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Livestock Science journal homepage: www.elsevier.com/locate/livsci
Quantifying the impact of lameness on welfare and profitability of finisher pigs using expert opinions T.B. Jensen n, H.H. Kristensen, N. Toft Department of Large Animal Sciences, Faculty of Life Sciences, University of Copenhagen, Grønneg˚ ardsvej 2, DK-1870 Frederiksberg C, Denmark
a r t i c l e i n f o
abstract
Article history: Received 2 January 2012 Received in revised form 9 July 2012 Accepted 16 July 2012
Lameness in finisher pigs affects both animal welfare and farmers’ profitability. However, information about the severity of pain and profit losses associated with individual causes of lameness is lacking. This study quantified and compared the pain and economic impact of nine different causes of lameness (e.g., infectious arthritis, claw lesions and osteochondrosis) using expert opinion. Six researchers working on animal behaviour and welfare and eight Danish pig veterinarians answered questionnaires regarding animal welfare and production, respectively. The probability of euthanasia, treatment with antibiotics and analgesics, and the changes in daily weight gain and feed conversion ratio were used to calculate the resulting profit loss for a pig suffering from each of the nine causes. To accommodate the uncertainty associated with the expert assessments, simulations were performed using probability distributions based on the minimum, median and maximum values. According to the experts, bone fractures caused the highest severity of pain and the largest reduction in profitability. Lesions to the claw wall and lesions to the volar area of the foot caused the lowest severity of pain. Arthritis due to Mycoplasma hyosynoviae and lesions to the volar area of the feet caused the smallest reduction in profitability. Considering the consequences of animal welfare and profitability concomitantly provides a transparent evaluation of the overall impact of lameness in finisher pigs. & 2012 Elsevier B.V. All rights reserved.
Keywords: Animal welfare Expert opinion Lameness Pig Profitability
1. Introduction The increased focus on animal welfare in society today emphasises the need to obtain quantitative information in order to investigate the economic consequences of improving or not improving animal welfare. Though several studies have focused on quantifying the effects of endemic and epidemic animal diseases (e.g., Bennett, 2003; Boklund et al., 2009) only limited efforts have been made to determine the effects of animal welfare in an economic context. n Corresponding author at: Present address: Danish Veterinary and Food Administration, Stationsparken 31-33, DK-2600 Glostrup, Denmark. E-mail address: [email protected] (T.B. Jensen).
1871-1413/$ - see front matter & 2012 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.livsci.2012.07.013
A common disease complex affecting the welfare of finisher pigs are leg disorders causing clinical signs of lameness (Busch et al., 2003). Clinical signs of lameness are most often caused by infectious arthritis, physical injuries or osteochondrosis (Jensen and Toft, 2009). Lameness is a sign that movement may be associated with pain (Busch et al., 2003). Besides affecting animal welfare negatively, clinical signs of lameness also have a negative impact on productivity and hence, economy (Jensen et al., 2007). Lameness in growing-finisher pigs has been found to be the third most common reason for antibiotic treatment in finisher herds (Christensen et al., 1994). Moreover, pigs with clinical signs of lameness have an increased risk of being euthanized (Engblom et al., 2008). As lameness in finishers affects both the animals and the farmers, there is a need to measure and compare the
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consequences of lameness on both animal welfare and profitability. Assessing the consequences of different causes of lameness may be a demanding task, partly due the limited information of effects of lameness on production in individual pigs, and partly due to the multidimensional nature of animal welfare. This challenges the assessment of the impact of lameness on the welfare of individual pigs. However, expert opinion has previously been found to be valuable in order to obtain inaccessible information in regard to both leg disorders (Jensen et al., 2009) and animal welfare (Rodenburg et al., 2008). Animal welfare is a multidimensional concept that can be based on the five freedoms (FAWC, 1992): (1) freedom from thirst and hunger, (2) freedom from discomfort, (3) freedom from pain, injury and disease, (4) freedom to express normal behaviour and (5) freedom from fear and distress. Pain may have a large effect on the welfare and behaviour of individual animals (Phillips, 2007). Hence, the pain involved in lameness may influence all five freedoms (Anil et al., 2009). In this study, we therefore used the level of pain as a proxy for the overall welfare of individual animals. The overall objective of this study was, through the use of expert information, to quantify the impact of different causes of lameness on pain and productivity in order to investigate the relationship between animal welfare and profitability in individual finisher pigs. This will be the first step in aggregating the consequences of lameness to the herd level. 2. Materials and methods This study deals with nine specific causes of leg disorders in finisher pigs (90–100 kg) that may cause clinical signs of lameness. The nine causes were selected as they are the commonest causes of lameness in finisher pigs (Jensen and Toft, 2009). The specific causes are infectious arthritis caused by (1) Mycoplasma hyosynoviae (M. hyosynoviae) (Nielsen et al., 2001), (2) Erysipelothrix rhusiopathiae (E. rhusiopathiae) (Buttenschøn et al., 1995), (3) Haemophilus parasuis (H. parasuis) (Nedbalcova et al., 2006) and (4) Streptococcus suis (S. suis) (Clifton-Hadley et al., 1986), physical injuries such as (5) bone fractures of the leg(s), (6) lesions to the claw wall (which includes white line lesions and wall lesions) (Penny et al., 1963) and (7) lesions to the volar area of the feet (which includes sole, toe and heel erosions) (Penny et al., 1963). Additionally, two different manifestations of osteochondrosis are considered: (8) osteochondrosis manifesta (OCM), where a thickened and uneven cartilage is observed and (9) osteochondrosis dissecans (OCD), where lesions of fissured articular cartilage are observed (Ytrehus, 2004). 2.1. Expert questionnaires Two questionnaires were conducted in May 2010 focusing on the consequences of the nine causes of lameness on animal welfare and production. The questionnaire focusing on animal welfare was sent by e-mail to eight scientists from four different countries (Finland,
Sweden, UK and Denmark) with expertise in animal behaviour and welfare. The welfare experts were selected on the basis of their previous work on lameness, pain and welfare as well as their likely knowledge of the nine diagnoses of leg disorders. Likewise, the questionnaire dealing with production consequences was sent by e-mail to 10 Danish veterinarians with several years of experience in pig health and production. The production experts were selected based on their specialisation and working experience as pig veterinarians as well as interest in pig leg health. The welfare and production experts were selected from different criteria, and only three experts participated in both welfare and production questionnaires. The severity of pain was used as a proxy for the level of animal welfare for each cause of lameness. Hence, for each cause of lameness, the welfare experts were asked to evaluate on an arbitrary scale from 0 to 100, the severity of pain that a lame pig would experience (pain index scale). On the pain index scale 100 was equivalent to insufferable pain, 75 was severe pain, 50 was equal to moderate pain, 25 equalled mild pain and 0 equalled no pain (modified from Morton and Griffiths. (1985)). For each of the different lameness causes, the 10 production experts were asked about the probability of a pig being euthanized (0–100%), and the probability of a pig being treated with antibiotics and analgesics (0–100%). Moreover, the experts evaluated the likely change in the average daily weight gain (ADG) from 100 g/day to þ100 g/day, and feed conversion ratio (FCR) from þ0.3 feed units per kilogram weight gain (FU/kg) to 0.3 FU/kg for a pig suffering from each of the nine specific causes of lameness. 2.2. Simulation of the loss in profitability The expert information regarding the consequences of each of the nine causes was used to form probability ¨ et al., distributions, using the BetaPert distribution (Stark 2000; Vose, 2008), which expresses the uncertainty about a parameter using the minimum, maximum and most likely value. This distribution is commonly used to represent expert opinion in a wide range of fields. For this study, we used the median response from the experts as the most likely value, and the maximum and minimum individual response as minimum and maximum values to the BetaPert distribution. Prices in the study reflected the price level in 2010. As presented in Eq. 1, the profit margin of a pig is the difference between the total revenue and the variable costs. Profit margin ¼ V s C F C M C PIGLET
ð1Þ
where, VS is the slaughter value of a pig, CF is the feed cost of a pig during the entire finishing period, CM is the cost of medicine (antibiotics and analgesics) and CPIGLET corresponds to the cost of a piglet at 30 kg (assumed to be 325 DKK in this study). The formula for the slaughter value (VS) is given in Eq. 2. V S ¼ W i þðADG þ DADGÞ*D*Ratio*Pr s *ð1Peu Þ
ð2Þ
T.B. Jensen et al. / Livestock Science 149 (2012) 209–214
where, Wi is the initial weight of a pig in the finisher unit (30 kg). ADG is the average daily weight gain of a finisher pig without lameness, which in this study is set to be 0.85 kg/day, and DADG is the change in the ADG due to the cause of lameness. D is the time (in days) a pig on average will spend in the finisher unit. We assume a pig ideally will be sent to slaughter at 100 kg, and the ADG is 0.85 kg/ day, the total time equals 82 day. Ratio represents the conversion ratio between live weight and carcass weight, which in this study is set to 0.76 (Udesen, 1997). Prs is the price of one kilogram carcass meat (8.5 DKK/kg in this study) and Peu is the probability of euthanisation of a pig with a specific cause of lameness. The formula for the feed cost (CF) is given in Eq. 3. C F ¼ ðDPeu *D=2Þ*ðADGþ DADGÞ*ðFCRþ DFCRÞ*Pr F
ð3Þ
where FCR is the average feed conversion ratio (FCR), which in this study is set to be 2.8 FU/kg, and DFCR is the change in FCR due to the cause of lameness. PrF is the price of one feed unit (in this study 1.1 DKK/FU). In Eq. 3, time of euthanasia is assumed to be in the middle of the period a pig is placed in the finisher unit. Finally, the formula for the medicine cost (CM) is given in Eq. 4. C M ¼ P AB *C AB þP AN *C AN
ð4Þ
where PAB is the probability of a pig being treated with antibiotics and CAB is the cost of a commonly practised three day treatment with antibiotics (20 DKK). Likewise, PAN is the probability of a pig being treated with analgesics and CAN is the price of a three day treatment with analgesics (180 DKK). Using Eqs. (1–4), a pig that does not suffer from any cause of lameness has a profit margin of 104 DKK. The loss in profitability of a pig experiencing a particular cause of lameness was calculated in the interval from 30 kg until slaughter by subtracting the profit margin of a pig without lameness (104 DKK) from the profit margin of a pig with a particular cause of lameness (Eqs. 1–4).
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3. Results 3.1. Impact on pain Out of eight researchers in animal behaviour and welfare, six replied back corresponding to a response rate of 75%. Based on the median values of the expert opinions, bone fractures was the cause of lameness associated with the highest severity of pain (median value ¼90 on the arbitrary scale) (Table 1). This was followed by osteochondrosis dissecans (median value¼67.5) and infectious arthritis caused by S. suis (median value¼65). However, the variation in the expert opinions was considerably higher for these last two causes then for bone fractures. The lowest severity of pain was associated with lesions to the claw wall (median value¼45) and lesions to the volar area of the feet (median value ¼45), however the minimum and maximum values showed a large variation in the answers given by the experts (Table 1).
3.2. Loss in profitability Eight out of 10 Danish veterinarians returned the production questionnaire. This corresponded to a response percentage of 80%. From the experts’ opinions, pigs suffering from bone fractures had 90% (median value) risk of being euthanized (Table 2). The probabilities of euthanasia when a pig suffered from lameness due to other causes than bone fractures were lower (median value r40%). However, these probabilities varied considerably compared to that of bone fractures. Pigs suffering from one of the four infectious pathogens causing arthritis or bone fractures had the highest probability of being treated with antibiotics (median values¼80–90%). On the other hand, lesions to the claw wall and lesions to the volar area of the feet had the lowest probability of being treated with antibiotics (median value¼10%). With a minimum value of 0% and a maximum value of 100%, there were large variations in the answers from the experts. With regard to the probability of
2.3. Simulation of the impact on pain Using the experts’ responses from the welfare questionnaire, the animal welfare consequences (i.e., pain) for each cause of lameness was simulated as a BetaPertdistribution using the median, minimum and maximum values reported by the experts as most likely, minimum and maximum values. 2.4. Modelling The simulation models for loss in profitability and impact on pain were both implemented in R (version 2.9.1) (R Development Core Team, 2006). For each cause 10,000 samples of consequences were simulated from the relevant distributions and used to calculate the profit loss and the impact on pain. The resulting loss in profitability and impact on pain were summarized using median, minimum and maximum values, as well as graphical illustrations of the central 95% probability mass for the combination of pain index and profit loss for each cause.
Table 1 Median, minimum and maximum values of six experts opinions regarding the severity of pain due to the nine causes of lameness. Cause of lameness
Median value
Fracture 90 Lesions to the claw wall 45 Lesions to the volar area of 45 the feet M. hyosynoviaea 57.5 E. rhusiopathiaeb 60 H. parasuisc 57.5 S. suisd 65 OCMe 55 f OCD 67.5 a
Mycoplasma hyosynoviae. Erysipelothrix rhusiopathiae. c Haemophilus parasuis. d Streptococcus suis. e Osteochondrosis manifesta. f Osteochondrosis dissecans. b
Minimum value
Maximum value
75 15 15
95 65 50
20 35 30 30 20 35
70 80 75 70 65 80
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Table 2 Median, minimum and maximum values (in parenthesis) of eight expert opinions regarding the production effects of the nine causes of lameness. Cause of
Consequences
lameness
Euthani-sation (%)
Treatment: antibiotic (%)
Treatment: analgesic (%)
DADGa (g/day)
Fracture Lesions to the claw wall Lesions to the volar area of the feet M. hyosynoviac E. rhusio-pathiaed H. parasuise S. suisf OCMg OCDh
90 (80, 90) 15 (0, 50) 10 (0, 30)
80 (50, 90) 10 (0, 100) 15 (0, 100)
10 (10, 70) 10 (0, 20) 10 (0, 30)
100 ( 100, 75) 0.25 (0,15, 0.30) 25 ( 100, 0) 0.1 (0, 0.30) 25 ( 100, 0) 0.075 (0, 0.30)
0 40 20 20 40 30
90 80 80 80 40 50
20( 0, 80) 20 (10, 70) 20 (10, 70) 20 (10, 50) 15 (0, 50) 20 (10, 50)
(0, 20) (10, 80) (10, 50) (10, 50) (0, 80) (10, 50)
(50, 100) (50, 100) (60, 100) (60, 100) (0, 100) (30, 100)
25 50 25 50 25 25
( 75, 0) ( 75, 25) ( 75, 25) ( 75, 25) ( 100, 0) ( 100, 0)
DFCRb (FU/kg)
0.05 0.15 0.1 0.15 0.1 0.05
(0, 0,15) (0.05, 0.30) (0.05, 0.25) (0.05, 0.25) (0, 0.30) (0, 0.30)
a
Average daily weight gain. Feed conversion ratio. c Mycoplasma hyosynoviae. d Erysipelothrix rhusiopathiae. e Haemophilus parasuis. f Streptococcus suis. g Osteochondrosis manifesta. h Osteochondrosis dissecans. b
treating with analgesics, the median values of the expert opinions for all nine causes were between 10 and 20%. The largest variations in the answers were seen among the causes: bone fractures and the four infectious pathogens. Answers in regard to the ADG and FCR also varied according to the experts. Yet, the experts agreed that pigs with a bone fractures had the highest reduction in ADG (median value¼ 100 g/day) and highest increase in the FCR (median value¼0.25 FU/kg) (Table 2). The highest reduction in profit margin based on production estimates was in pigs with bone fractures (median value¼ 409.9 DKK) (Table 3). Leg disorders caused by E. rhusiopathiae caused the second highest reduction (median value¼ 185 DKK); however, the variation was much larger than for bone fractures. The lowest reduction in the profit margin was associated with M. hyosynoviae arthritis (median value¼21 DKK) and lesions to the volar area of the feet (median value¼5.7 DKK) (Table 3). 3.3. The relationship between profit loss and pain impact The relationship between the impact on pain and the loss in profitability of an individual pig is illustrated in Fig. 1. Bone fractures had the greatest impact on both pain and profitability. The lowest impact on both profit and pain was seen for lesions to the claw wall and lesions to the volar area of the feet (Fig. 1). 4. Discussion Our study shows that of the nine causes of leg disorders, bone fractures had the highest impact on welfare as it caused the most pain and had the highest impact on profitability. Reducing the occurrence of bone fractures in finisher pigs has a large positive effect for both the individual animals as well as the farmer, and therefore, it is important to be able to distinguish bone
Table 3 Simulated median, minimum and maximum values of the loss in profitability (DKK) based on expert information regarding the nine causes of lameness. Cause of lameness
Median value (DKK)
Fracture 514 Lesions to the claw wall 131 Lesions to the volar area of 99 the feet M. hyosynoviaea 86 E. rhusiopathiaeb 290 c H. parasuis 191 S. suisd 190 OCMe 259 OCDf 214
Minimum value (DKK)
Maximum value (DKK)
466 27 15
597 295 198
17 112 101 102 39 99
197 523 344 321 488 346
a
Mycoplasma hyosynoviae. Erysipelothrix rhusiopathiae. c Haemophilus parasuis. d Streptococcus suis. e Osteochondrosis manifesta. f Osteochondrosis dissecans. b
fractures from other causes of lameness. In a study of 130 sows from one Swedish herd, 43% of the sows diagnosed with arthritis post mortem was expected to have a bone fracture based on a previous clinical examination (Engblom et al., 2008). Hence, diagnosing a bone fracture based on clinical examination of individual pigs can be uncertain as they may be confused with other causes of lameness. Correct distinction between bone fractures and arthritis in finisher pigs would potentially reduce the profit loss. Among the four infectious pathogens, infectious arthritis caused by E. rhusiopathiae had the highest economic impact and a large effect on animal welfare according to the experts. The reason for the high effect on profitability
T.B. Jensen et al. / Livestock Science 149 (2012) 209–214
Fig. 1. The relationship between median loss in profitability (DKK) and median pain (pain index) for an individual finisher pig. The bars indicate the minimum and maximum values for pain index and profit loss for each of the nine causes of lameness.
can be explained by the high probability of euthanasia compared with the other infectious pathogens. Pigs infected with E. rhusiopathiae have usually been infected at an early stage of life, and may suffer from bacteraemia and show clinical signs of a generalized infection. Their feet are often placed under the center of the body and their limbs are painful and swollen (Wood and Henderson, 2006). The fact that E. rhusiopathiae can cause severe arthritis in pigs, explains the higher probability of euthanasia and the large negative effect on both profitability and animal pain. On the other hand, M. hyosynoviae had the lowest impact on profitability and caused only mild pain. Infectious arthritis caused by M. hyosnoviae is considered to be less severe, and pigs with clinical signs of lameness usually recover spontaneously within one to two weeks (Friis, 1987). This may explain the low impact of arthritis caused by M. hyosynoviae seen in this study. Claw lesions had the lowest effect on animal pain, and also only a minor effect on profitability. Lesions to the claw are common findings among finisher pigs (Mouttotou et al., 1997). In a study of 15 Norwegian sow herds, only severe claw lesions and claw infections were associated with clinical signs of lameness in sows (Gjein and Larssen, 1995). In our study, lesions to the volar area of the feet and lesions to the claw wall were clinical expressions aggregating a number of specific clinical manifestations. A number of these clinical manifestations (e.g., sole and heel erosions) often do not penetrate the sensitive corium, and hence do not cause pain to the pig. This may explain the reduced effect of claw lesions on pain as well as production as evaluated by the experts. Pain was considered a simple and valid indicator of the overall welfare of individual pigs in this study (Phillips, 2007; Anil et al., 2009). The Welfare Quality Research project focused on developing an objective and operational
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way to assess animal welfare (Botreau et al., 2009). In the future, when more standardised methods are developed for measuring and aggregating different aspects of animal welfare into one numeric value, our knowledge of the relationship between animal welfare and production may be validated. A number of studies in animal welfare research have used expert opinion for the evaluation of the welfare of animals (Bracke et al., 2008; Rodenburg et al., 2008). The experts in our study were selected as highly specialised in pig welfare and production both in Denmark and internationally, and we used the median value as well as the maximum and minimum values to illustrate the variation in the answers given by experts. However, other methods of handling expert opinion are also used in the literature. In a study by Van der Fels-Klerx et al. (2002), a heterogeneous expert panel was used for the quantification of a continuous variable. The individual experts were weighted according to their expertise in that study. In our study equal weight was given for each expert in both animal welfare and production as they had been carefully selected beforehand. However, we cannot rule out that some experts did not have the same level of knowledge for all nine causes of lameness, and therefore, assigned higher scores to causes of which they had more specific knowledge. Results from our study are presented as the consequences for individual pigs. In modern pig production the effect of disease (e.g., lameness) on profitability is generally of interest at the herd level, and it is necessary to know the specific causes of lameness and their prevalence. However, the prevalence of the nine causes differs widely in a herd (Jensen et al., 2009). The prevalence of pigs with bone fractures in a herd is often low (o0.1%) (Baumann and Bilkei, 2002), whereas the prevalence of pigs with at least one claw lesion has been reported to be as high as 94% (Mouttotou et al., 1997). Knowing the specific cause and prevalence of lameness, it is possible to aggregate the production effects of individual pigs to the herd level, when taking into account specific herd information like herd size and production type (i.e., such as all in all out or continuous production). However, aggregating the animal welfare effects of individual pigs to the herd level is indeed more challenging as the animal welfare implications of different scenarios need to be evaluated and compared (e.g., one pig with a bone fracture compared to 10 pigs with claw lesions). Therefore, more research on aggregating the consequences of lameness to the herd level is needed. In conclusion, according to the welfare experts, bone fracture was the most painful leg disorder, with lesions to the claw wall and volar area of the feet being the least painful leg disorders in finisher pigs. The production experts also asserted a fractured limb as having the highest impact on profitability, and M. hyosynoviae and lesions to the volar area of the feet as having the lowest impact on profitability. By combining quantitative information of welfare and production aspects, it is possible to rank the overall consequences of different disorders. This not only highlights areas in need of attention, but also provides incentives to farmers for improving animal welfare in the future.
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Conflict of interest statement To Livestock Science, I hereby confirm that there is no conflict of interest in regard to the manuscript: ‘‘Quantifying the impact of lameness on the pain and profitability of finisher pigs using expert opinions’’. On behalf of the authors of the manuscript, Tina Birk Jensen.
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