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J APPL POULT RES 2009. 18:432-439. doi:10.3382/japr.2008-00061
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Research Reports

Impact of lameness on broiler well-being

I. A. Nääs*,1, I. C. L. A. Paz{dagger}, M. S. Baracho*, A. G. Menezes{ddagger}, L. G. F. Bueno*, I. C. L. Almeida{dagger} and D. J. Moura*

* School of Agricultural Engineering, State University of Campinas-UNICAMP, PO Box 6011, Campinas, São Paulo, Brazil; {dagger} School of Veterinary Medicine and Animal Science, State University of São Paulo-UNESP, Botucatu, São Paulo, Brazil; and {ddagger} Center of Technology, Research Group on Biosystems Technology-UNICAMP, Campinas, Brazil

1 Corresponding author: irenilza{at}agr.unicamp.br


   SUMMARY
TOP
 SUMMARY
DESCRIPTION OF PROBLEM
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS AND APPLICATIONS
 REFERENCES AND NOTES
 
Various degrees of lameness were compared among male broilers ranging in age from 28 to 49 d that had been randomly selected from a commercial farm. Gait scores were given to the broilers while they walked on a force measurement platform system, and the force exerted by their feet was measured and compared in 2 distinct conditions: with and without administration of an analgesic. Postmortem femoral degenerative lesions were observed, and the femur strength in response to a compression load was measured and compared. Results showed a difference in the peak vertical forces of the right and left feet before and after medication. The researchers also found that as BW increased, the locomotion ability of broilers tended to decrease. After birds received the analgesic, the peak vertical force increased among the more severely lame broilers at 35 to 49 d of age and their walking speed was decreased, indicating that they might have felt pain during locomotion. No difference was found between the femur (right and left) strength in response to a compression load; however, the results showed that femurs of 28-d-old birds were less resistant to compression (P < 0.05) than those of older broilers. The foot force platform was a useful tool for assessing the walking ability of broilers.

Key Words: broiler chicken • leg abnormality • well-being • pain • foot force measurement


   DESCRIPTION OF PROBLEM
TOP
 SUMMARY
 DESCRIPTION OF PROBLEM
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS AND APPLICATIONS
 REFERENCES AND NOTES
 
The economic costs associated with leg weakness are due to culling on the farm and also to condemnations or downgrading at processing [1]. Bird well-being aspects include the ability of affected birds to eat and drink [2, 3], as well as the pain associated with the pathology of leg weakness [4–6]. In commercially reared broilers, it has been reported that 26 [7] to 31% [8] suffer leg abnormalities of sufficient severity for their well-being to be considered compromised.

The current literature describes a relatively high incidence of growth-associated leg weakness in broilers [7, 9, 10]. Bokkers and Koene [11] also been found that both fast- and slow-growth broiler strains presented the same behavioral pattern but that the time budget in distinct activities was different. Young, fast-growing broilers performed more actions on the litter, such as eating and drinking, than slow-growing broilers. In a behavioral study, Weeks et al. [12] reported that the walking movements of broilers declined with age, occupying an average of 3.3% of the time budget of a slaughter-weight broiler, and lameness significantly reduced this to a minimal 1.5% in the most seriously affected birds. Sound birds predominantly chose the usual standing posture for eating, whereas lame birds lay down to eat for almost half their feeding time. Fast-growing broilers were apparently frustrated in their walking behavior, leading to an increase in preening when growing older, and they were also naturally motivated to perform resting postural behaviors [10, 11].

The risk of occurrences of walking disabilities is influenced by genetic strain, sex, stocking density, and BW gain [13, 14], as well as by management factors such as lighting programs and rearing conditions [15, 16]. A large proportion of the problems lead to leg disorders that result in a reduced ability to walk, causing unnatural biomechanical forces and therefore gait alteration [5, 17]. Reduced walking or standing ability often leads to breast blisters and hock burn because the birds spend a long time crouching on poor-quality litter. Because lameness causes behavioral restriction and pain, it has become a major well-being concern in animal husbandry [3, 17, 18].

Because birds are known to have the capacity to experience pain, there is a need to minimize its occurrence through both prevention and treatment. Even though pain assessment in birds is difficult, they can be trained to self-medicate with analgesics, and researchers could directly assess the frequency and amounts administered as well as the specific responses of the birds [6, 19–21].

The purpose of this study was to determine the suitability of the force platform as a research tool to record objective data on the ground reaction forces broilers produced during walking after wk 4 of growth. Possible interactions between the walking ability of broilers and their femur physical strength in response to a compression load were also examined.


   MATERIALS AND METHODS
TOP
 SUMMARY
 DESCRIPTION OF PROBLEM
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 CONCLUSIONS AND APPLICATIONS
 REFERENCES AND NOTES
 
The experiment [22] took place at the Center for Technology at the State University of Campinas, Brazil.

Bird Management
Forty male broilers at 28, 35, 42, and 49 d of age (10 of each) from the same genetic strain [23] were randomly chosen from a commercial poultry farm, where they were reared at an average stocking density of 13 birds/m2. They were transported in boxes for 35 km to the laboratory and used in the trial. Immediately on arrival at the experimental site, the birds rested for 40 min and were given water. Each bird was individually identified by marking the head with a coat mark of a specific color for individual recognition. The birds were weighed and then separated by age and placed in boxes. The experiment began with the older birds.

Foot Force Measurement
When the bird walks, a specific pressure on the floor is generated that is a function of its BW and balance, indicating the way it lays its feet over that surface. A chamber was built with the objective of determining the pressure while walking [24]. A 0.01-m-wide pressure-sensitive mat with piezoelectric crystal sensing elements inside [25] was embedded in the middle of a 1-m-long runway. The lateral sides were built using transparent acrylic walls. Both inlet and outlet ramps had an angle of 5° from the floor, as seen in Figure 1aGo. The impact of both feet (right and left) on the ground while walking across the runway and during a 1-legged stance, as it changed the leg for displacement, was measured (Figure 1bGo).


Figure 1
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  		Figure 1. View of the broiler foot force measurement system (a) and a broiler walking on the foot force platform system (b), with the video cameras capturing the movement from the top and side angles.

 
The force measurement platform system (FMPS) consisted of 2 parts: the hardware [26], which recorded the pressure data and transferred the data to the software, and the software, which allowed for image visualization of the foot pressure distribution as well as for processing and analysis of the recorded data. The software, which was installed on a desktop computer, converted the captured values into a pressure map that could be seen in distinct colors in real time or saved for further analysis, as used in earlier studies [27, 28]. The mat was calibrated with the average BW of the birds in each box for the different age groups studied.

Walking Observation
Video recording was done using 2 digital video cameras while the birds walked across the pressure-sensitive walkway [29]. The first camera was placed at a distance of approximately 1.0 m to the side of the plane of motion (wooden platform with the FMPS section used for the ground pressure data collection). The second camera was placed over the middle of the runway, attached to a pole 1.3 m high. Both cameras were aligned on their vertical and horizontal axes, using a 90° angle from the plane of motion to record the broiler walking alignment.

Subjective gait scoring was used to assess bird mobility according to Kestin et al. [7]. The gait score (GS) consisted of a 6-point scale ranging from 0 to 5, where 0 represented no detectable gait abnormality and 5 indicated a bird incapable of performing a standing stance [30]. The GS was evaluated on individual birds by a trained observer. The time the bird spent crossing the walkway was also recorded by the software. Birds were first left on the platform inlet for about 15 min, where they could move freely before heading toward the walkway. In each age group, broilers were tested in random order on the FMPS until approximately 3 runs with complete force measurements were obtained for each bird.

Experimental Procedure
Information was obtained regarding the walking ability of broilers while they moved on the FMPS and the data were then recorded. After stimulating the birds to walk on the FMPS and arrive at the opposite side, the broilers were medicated orally with a quick-acting analgesic solution of metanizole sodium, which is a non-steroidal antiinflammatory drug that is commonly used in many countries as a human sedative and that has been tested on animals [19]. The amount of analgesic administered was proportional to the age and BW of the birds [31]. The time birds needed to drink the analgesic solution and rest lasted from 30 to 40 min, as suggested in previous studies [19, 32]. Subsequently, the birds were stimulated to walk across the FMPS again in the same order as before. They were allowed to move freely across the runway at a natural speed. During both phases, the force exerted on the FMPS by the feet (left and right) of the birds while walking and the time of displacement were recorded and analyzed. For ground force measurements, the start and end points of a step were determined by the pressure exerted on the sensing elements and displayed by the software. The values were then calculated automatically by the software. Speed and stance times were also recorded directly by the software and further calculations were made. The walking alignment observation was done by watching the recorded video.

Postmortem Examination and Measurements
Immediately thereafter, the foot force measurement procedure was completed and all birds were killed by cervical dislocation; a postmortem examination was carried out on all birds to determine physical abnormalities of both legs [4, 33, 34]. Special attention was given to femoral degenerative joint lesions [35].

A compression test was carried out to determine the compressive stress and deformation of both femurs (right and left) because, according to Taylor et al. [36], the femur is loaded primarily with compression force during stance walking. A compression test determines the behavior of materials under crushing loads. Femurs from individual birds were cleaned of adherent tissue, and the biomechanical strength of each bone was measured using a material testing machine [37]. The bones were held in vertical position and the compression load was applied in the cross-sectional area up to bone failure; the total crushing load at failure was determined in newtons.

Data Analysis
The force recorded on the FMPS was expressed as a percentage of the BW of each bird to allow comparisons between birds of different weights and ages. To analyzing the vertical force measurements made on each step, 1 step was chosen at random to avoid serial correlation between steps in the same run. The peak vertical force always exceeded the BW, and was then adjusted by subtracting the BW before being expressed as a percentage. Mean values were calculated, taking into account variation among birds. The statistical significance of differences between means was estimated using Student’s paired t-tests between the corresponding means.

Two-way ANOVA was applied to verify the variability between age groups and within groups for each foot (left and right). Data were considered to be statistically significant when P < 0.05. Data were analyzed using PROC GLM of SAS [38].


   RESULTS AND DISCUSSION
TOP
 SUMMARY
 DESCRIPTION OF PROBLEM
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
CONCLUSIONS AND APPLICATIONS
 REFERENCES AND NOTES
 
The mean values and SD of the BW of the birds were calculated; the group of older birds (49 d) presented higher BW (3,035.6 g) and higher SD (277), followed by the 42-d (3,000.0 g and 159), 35-d (2,438.3 g and 100), and 28-d (1,411.5 g and 100) birds. No statistical significance (P > 0.05) was found in BW between the groups of 49- and 42-d-old birds, although they differed from the other age groups (Table 1Go).


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  		Table 1. Summary of experimental average data of broilers from 28 to 49 d of age
 
Biomechanical Variables
Based on video observation, in general, older and heavier birds (>35 d of age) were found to have more difficulty walking and were given higher GS (3 to 5). The same result was found previously by Sorensen and Kestin [14], who concluded that at an early age (up to 28 d), locomotion disorders were a relatively minor problem and that few severely lame birds had a GS of 3 or higher. Several studies have established correlation coefficients between BW and walking ability, hock burn, and tibial dyschondroplasia, and have shown that as BW increases broiler locomotion ability tends to decrease [8, 9, 34]. Older birds (49 and 42 d) also took more time (75 and 60 s, respectively) to cross the 1-m walkway (Table 1Go). In most animals, walking speed increases with age, whereas the increase in stance time may naturally enable the peak vertical force to be reduced [12]. Even though there are biomechanical advantages to adopting slower speeds, because this reduces the peak vertical forces and therefore the stresses on the musculoskeletal system produced during walking, it has been recognized that lame birds tend to walk more slowly than sound ones [12, 28, 34]. In this study, the peak vertical force in both legs (right and left) increased from 28 to 35 d and then decreased with age (Table 1Go). Differences were also detected in the values of the force attributed to each leg (left and right) in both conditions (with and without analgesic intake, P < 0.05) for birds at all ages. Birds at 28, 35, and 49 d presented a significantly different peak vertical force in each leg, and this asymmetry may have predisposed them to lameness [28]. After birds had received medication, this asymmetry was found only in the group of 42-d-old broilers, which did not present it before being medicated.

Gait score estimations determined by watching the recorded video revealed a slight decrease in GS after intake of the analgesic solution, which was directly proportional to bird BW (Table 2Go). The current literature has provided evidence that lame birds suffer pain when they walk [6, 20, 32, 39]. Birds presenting some degree of lameness spend less time in activities that require them to stand, and this behavior is consistent with their suffering chronic pain while standing. A previous study [20] showed that lame broilers self-selected more feed containing an analgesic agent (carprofen) than sound birds. According to the authors, intake of the drug improved the ability of lame birds to walk because of its antiinflammatory and analgesic effects. Thus, there is good reason to believe that the well-being of these birds with GS higher than 3 is seriously compromised by leg weakness because they are unable to express their natural behavioral movement freely and are often are unable to reach food and water adequately [2, 3, 11, 14, 21].


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  		Table 2. Summary of data on gait score, mean walking time to cross the foot force measurement platform, and the percentage of birds affected by leg weakness
 
The time each bird used to cross over the runway at the FMPS, and the GS graded for each group of broilers without and with intake of the analgesic drug metanizole are presented in Table 2Go. There was a positive effect on both GS given to each group of birds, and the average walking time on the runway decreased (P < 0.05) for heavier and older broilers, indicating that there was a reduction in pain proportional to the improvement in their walking ability. Danbury et al. [20] reported that lame broilers improved their walking speed after ingesting a medicated feed, indicating that these birds probably had suffered pain before intake of the drug.

If standing and moving may cause discomfort, pain, or both, performing such activities may therefore represent a cost to a lame broiler and also increase the time to perform such activities. Similar results are found in the literature [2, 40], indicating that this pathological condition is painful, thus compromising the well-being of broilers after 35 d of age.

Physical Variables
No significant difference was found between the left and right femur strength for the compression load at all ages, nor was a difference in femur strength found for the group of femurs from broilers at 49, 42, and 35 d of age. However, the femur strength of broilers at 28 d of age was significantly less resistant than that of the others (P < 0.05), as expected because of their young age [5, 39, 41, 42].

By applying regression analysis, equation [1] was found, which indicates that femur resistance to the compression force increased as the bird grew older (R2 = 60.1%, P < 0.05). However, based on the results, the apparent lack of resistance of the femur to the compression load was correlated more with the age of the bird at 28 d. This finding is consistent with an earlier study [43] that explained the structural complexity and composition of bone associated with strength, which varied according to the age and nutritional status of the bird:


Formula 1([1])

In previous research, Dibner et al. [41] recognized that initial ossification did not yield bones that were structurally mature and mechanically robust. Important changes occurred that were responsible for the increase in bone-breaking strength observed in older birds.

Femoral degenerative lesions were evident as an age problem because they were found in 50% of the broilers at 49 and 42 d of age, in 70% of birds at 35 d of age, and in only 10% of birds at 28 d of age, showing that this pathology became more evident after wk 5 of growth. No correlation was found between femoral degenerative lesions and GS, and the obtained residues did not respond to the supposition of a normal distribution. Some skeletal abnormalities found in birds a few days after hatching have been reported to be partially related to the strain of broilers [4, 9, 33, 41], and it is possible that metabolic disorders are initiated during incubation. Probably because of a biomechanical imbalance during walking, degenerative lesions of the femur were evident as a problem after 28 d of age and limited the walking ability of broilers, generally at 35 d of age [5, 44].


   CONCLUSIONS AND APPLICATIONS
TOP
 SUMMARY
 DESCRIPTION OF PROBLEM
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS AND APPLICATIONS
REFERENCES AND NOTES
 

  1. The force platform provided efficient records for assessing the ground reaction forces produced by broilers of different ages while walking.
  2. Results indicated that the reduction of pain resulting from administration of metanizole significantly increased the walking ability of heavier and older broilers. There was also a slight improvement in their GS, especially in the birds more severely affected by lameness.
  3. Standing and moving may cause increased pain and discomfort, especially in broilers between the ages of 35 and 49 d, which compromises the time spent performing activities related to feeding and drinking, and ultimately affecting their overall well-being.
  4. Adequate management and nutritional methods, as well as stimulation of earlier walking activity, are recommended to maintain adequate walking ability in poultry flocks.


   REFERENCES AND NOTES
TOP
 SUMMARY
 DESCRIPTION OF PROBLEM
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS AND APPLICATIONS
 REFERENCES AND NOTES
 

  1. Almeida Paz, I. C. L., A. A. Mendes, T. S. Takita, L. C. Vulcano, P. C. Guerra, F. S. Wechsler, R. G. Garcia, S. E. Takahashi, J. Moreira, K. Pelícia, C. M. Komiyama, and R. R. Quinteiro. 2005. Comparison of techniques for tibial dyschondroplasia assessment in broiler chickens. Braz. J. Poult. Sci. 7:27–31.
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  6. McGeown, D., T. C. Danbury, A. E. Waterman-Pearson, and S. C. Kestin. 1999. Effect of carprofen on lameness in broiler chickens. Vet. Rec. 144:668–671.[Abstract/Free Full Text]
  7. Kestin, S. C., T. G. Knowles, A. E. Tinch, and N. G. Gregory. 1992. Prevalence of leg weakness in broiler chickens and its relationship with genotype. Vet. Rec. 131:190–194.[Abstract]
  8. Su, G., P. Sorensen, and S. C. Kestin. 1999. Meal feeding is more effective than early feed restriction at reducing the prevalence of leg weakness in broiler chickens. Poult. Sci. 78:949–955.[Abstract/Free Full Text]
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  22. Approved by the ethics committee on animal experimentation of the School of Veterinary Medicine and Animal Science, State University of São Paulo-UNESP, Botucatu, Brazil, Protocol no. 182/2007.
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  24. The dimensions were 0.48 m wide, 0.70 m high, and 1 m long, with an inlet ramp of 0.20 m, a horizontal plateau of 0.60 m in the middle, and an outlet ramp of 0.20 m.
  25. Tekscan Inc., South Boston, MA.
  26. The force mat hardware was formed by nearly 2,000 sensors organized in columns and rows. The output of each sensor was divided into 256 increments and read by the software in values called raw sum, ranging from 0 to 255.
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  29. JVC GDR-120U, 30 Hz with 520 vertical lines of resolution. JVC Service & Engineering Company of America, Atlanta, GA.
  30. GS = 0 describes a bird that moves agilely with no detectable gait abnormality; GS = 1 describes a bird that has a slight walking defect; GS = 2 describes a bird that has a definite and identifiable defect; GS = 3 describes a bird that has an obvious gait abnormality that affects its ability to move about, particularly its maneuverability, acceleration, and speed of movement; GS = 4 describes a bird that has a severe gait defect, walking only when driven to or when strongly motivated; and GS = 5 describes a bird that cannot walk at all unless pushed to do so.
  31. 28 d, 0.10 mL; 35 d, 0.15 mL; 42 d, 0.18 mL, and 49 d, 0.20 mL.
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  35. Even though postmortem examination does not give deeper information about the developmental aspects of physical abnormalities, it allows an overview of the physical consequences of the rearing conditions.
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  37. A Sintech 5/G materials testing machine (MTS, Eden Prairie, MN) was used with a 100-N load cell (precision 0.1 to 0.8 N). Crosshead displacement was monitored with an optical encoder to the nearest 0.001 mm and was corrected for system compliance. The compression load was applied at each femur head (left and right) directly at the femur vertical axis, with a speed of 1 mm/s.
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