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Poult Sci 2008. 87:1964-1970. doi:10.3382/ps.2008-00115
© 2008 Poultry Science Association
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ENVIRONMENT, WELL-BEING, AND BEHAVIOR

Bone Fracture Incidence in End-of-Lay High-Producing, Noncommercial Laying Hens Identified Using Radiographs1

W. D. Clark*, W. R. Cox{dagger} and F. G. Silversides*,2

* Agriculture and Agri-Food Canada, Agassiz Research Centre, Agassiz, British Columbia, Canada, V0M 1A0; and {dagger} British Columbia Ministry of Agriculture and Lands, Animal Health Branch, Abbotsford, British Columbia, Canada, V3G 2M3

2 Corresponding author: silversidesf{at}agr.gc.ca


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Bone fractures in laying hens are both a welfare and an economic concern for the poultry industry. The aim of this study was to use radiographs to quantify fracture incidence in 6 lines of noncommercial high-producing laying hens. A total of 451 hens (n = 71 to 78) were killed at 47 wk (White Leghorn-Black, White Leghorn-Blue) or 65 wk of age [Barred Plymouth Rock (BR), White Leghorn-Burgundy (WL-BUR), Columbian Plymouth Rock, Rhode Island Red (RIR)]. Radiographs were obtained with hens in 2 positions (lateral and ventrodorsal) and were used to identify fractures in the skeleton. Data on scallop-shaped indentations (possibly fractures) of the keel bone were also collected. After radiography, the left wings were removed for analysis of humeri, radii, and ulnae. Data for the 2 age groups were analyzed separately. The overall incidence of hens with at least 1 fracture was 6.6 and 15.7% in the 47- and 65-wk-old hens, respectively. Fracture incidence in 47-wk-old hens was not different between White Leghorn-Black and White Leghorn-Blue lines. Significant line differences were observed in the 65-wk-old hens, with at least 1 fracture found in 29.5% of RIR hens versus 9.5 and 4.2% observed in Columbian Plymouth Rock and WL-BUR lines, respectively. Fracture incidence in BR hens (18.2%) was greater than in WL-BUR hens. Fractures in RIR hens occurred predominantly in the furculum and wing bones, whereas pubic bones were most affected in BR hens. The proportion of hens with scallop-shaped indentations of the keel ranged from 36.1 to 88.2% and differed between lines in both age groups. High egg production did not seem to be associated with bone fragility in these lines. Two of the older lines (RIR and WL-BUR) had similar egg production, number of eggs to 60 wk, and egg shell weights at 4 ages but had a significantly different fracture incidence. The line differences in fracture incidence may have been affected by calcium metabolism, bone structure, and body weight.

Key Words: bone fracture • laying hen • radiograph • x-ray


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Bone breakage in laying hen flocks is a welfare concern in the poultry industry because of the pain likely involved with fractures in the live bird. Studies quantifying new or fresh fractures that occurred during shipping and handling observed incidences of 4 to 31% of birds (Gregory and Wilkins, 1989; Gregory et al., 1990, 1993a, b; Budgell and Silversides, 2004). Fractures identified as old or healing have been found at incidences ranging from 0 to 25% of birds (Gregory et al., 1990, 1993a,b; Budgell and Silversides, 2004).

Fractures can also impart economic concerns. High mortality rates, such as that observed by McCoy et al. (1996) in which pathological fractures were determined to be the cause of death in 35% of necropsied hens, can lead to decreased overall egg production. In addition, with nearly 100% of birds having at least 1 fracture at the end of processing (Gregory and Wilkins, 1989; Budgell and Silversides, 2004), the quality and usefulness of the meat product is decreased.

Research has examined several potential causal factors involved in high fracture incidence, including genetic components. Bishop et al. (2000) found that genetic selection for increased bone strength over several generations decreased the percentage of hens with fractures at end-of-lay. In contrast, Gregory et al. (1990) observed no differences between 4 commercial breeds. Budgell and Silversides (2004) observed no difference in shipping fractures among 1 heritage line and 2 commercial lines. However, the heritage line had 0% old fractures compared with 11 and 12% in the commercial lines.

Previous studies used manual dissection, which is time-consuming and laborious, as a means to identify old and new fractures in laying hens. Radiographs were used in the current study to try to simplify the identification of fractures and to attempt to analyze as much of the skeleton as possible. The objectives of this study were to use radiographs to determine the incidence of fractures in 6 lines of noncommercial, high-producing laying hens and to compare the incidence of fractures among hens in relation to egg production and bone parameters.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Chicks from 6 high-producing, noncommercial egg-laying lines (Silversides et al., 2007) were obtained in 2 groups. Four of the lines [Barred Plymouth Rock (BR), White Leghorn-Burgundy (WL-BUR), Columbian Plymouth Rock (CR), Rhode Island Red, (RIR)] were received approximately 19 wk before the other 2 lines [White Leghorn-Black (WL-BLK), White Leghorn-Blue (WL-BLU)]. Chicks were group-raised in batteries with plastic mesh flooring (approximately 500 cm2/bird) until housing at 16 wk of age. Hens were weighed and housed 3 per cage (688 cm2/hen) on 2 levels. Twenty-six cages per line were used for this experiment (78 hens/line). Diets were formulated to meet National Research Council (1994) recommendations and were provided to allow ad libitum consumption. The principal ingredients and nutrients of the diets provided during the laying period are shown in Table 1Go. All procedures were approved by the Animal Care Committee for the Agassiz Research Center in accordance with the guidelines established by the Canadian Council of Animal Care (1993).


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  		Table 1. Principal ingredients and nutrients of diets fed during the laying period
 
Egg production (marketable eggs) for each cage was recorded 5 d a week and extrapolated to 7 d, beginning at 16 wk of age and continuing until 60 (BR, WL-BUR, CR, RIR) or 39 wk of age (WL-BLK, WL-BLU). Egg weights were obtained for each cage once per week. Individual body weights were measured at 10-wk intervals, beginning at 20 wk of age. Egg quality parameters were assessed for eggs from half of the cages at the same time intervals beginning at 31 wk of age. The final egg quality measurements were obtained after the collection of egg production data was halted. Average egg weight, as well as yolk, albumen, and dry shell weight data were obtained for each cage. Albumen weight was calculated by subtracting yolk and shell weight from total egg weight. Hens were maintained for 5 to 8 wk after collection of production data was stopped.

The hens (71 to 78/line, 451 total) were killed at 65 (BR, WL-BUR, CR, RIR) and 47 (WL-BLK, WL-BLU) wk of age using pentobarbital sodium (Euthanyl Forte, Bimeda-MTC Animal Health Inc., Cambridge, Ontario, Canada) by intracardiac injection to prevent convulsions that could cause bone fractures. The carcasses were placed in bags and stored at –20°C. They were thawed before being radiographed.

Radiographs were obtained using a MinXray HF8015+ portable veterinary x-ray unit (MinXray Inc., Northbrook, IL). Birds were x-rayed in 2 positions with limbs extended (ventrodorsal and lateral) at 64 kV and 0.02 mA/s. Radiographs were examined using a light box and an incandescent bulb. The whole skeleton was examined with the exception of the head, neck, and bones below the tibiae. Fractures were identified as old (edges undefined or callus observed) or new (sharp edges without observable callus formation). The depth of scallop-shaped deformities on the keel was measured on the radiographs by positioning a straight edge along the ventral edge of the keel image and measuring the depth of the largest indentation.

After radiographs were taken, the left wing was removed from 1 hen per cage (n = 26 per line) and frozen at –20°C for further analysis. The wings were thawed, and the humeri, radii, and ulnae were dissected out and measured for length. The individual bones were then refrozen and later dried (100°C) for 24 h and weighed, followed by ashing at 600°C for 6 h. Percentage of ash was calculated on a dry bone basis. Bones with fractures were removed from the data set, because fracture healing typically involves formation and resorption of a mineralized callus (Brand and Rubin, 1987; Clark et al., 2005) that could affect ash content.

Data for fracture incidence (number of birds with at least 1 fracture in the specified bone) were analyzed using a contingency {chi}2 test for independence (Strickberger, 1976) to compare lines within each age group. Wing bones (humeri, radii, ulnae) were compared individually and as a group. The data for the incidence of scallop-shaped keel indentations were also analyzed using the {chi}2 test. Differences in the depth of the keel indentations were analyzed using a 1-way ANOVA in SAS Version 9.1 software (SAS Institute Inc., Cary, NC). Birds with a keel indentation of 0.0 mm were removed from the data set before ANOVA. The ANOVA procedures were also used to test differences between lines within age groups for bodyweights, egg production, egg quality, and bone data. Egg production data were summarized into 3 periods for the 4 older lines (prepeak, 16 to 27 wk; mid lay, 28 to 43 wk; and late lay, 44 to 60 wk) and 2 periods for the 2 younger lines (prepeak, 16 to 27 wk; and mid lay, 28 to 39 wk). When appropriate (P = 0.05), comparisons were made using the lsmeans-pdifffunction. The 2 age groups were not statistically compared in any of the analyses. The tables present raw means and standard errors.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Hen-day egg production, egg weights, and egg numbers for 2 to 3 time periods are shown in Table 2Go. No line effects were observed in the 47-wk-old hens for hen-day production in period 1 or period 2 or for total egg number to 39 wk of age. Egg weights for the WL-BLK hens were greater in both periods as compared with WL-BLU hens. No differences were observed in hen-day egg production in period 1 for the 65-wk-old lines; however, CR production was significantly lower in periods 2 and 3. The CR line also produced significantly fewer eggs to 60 wk of age. Egg weights were heavier for RIR hens in period 1 and RIR and WL-BUR in periods 2 and 3.


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  		Table 2. The effect of line on hen-day egg production, egg weight, and total egg numbers1
 
Egg quality, measured at 10-wk intervals, consisted of data for the weight of the eggs and egg components (Table 3Go). There were no line effects in the 47-wk-old hens for any parameters at 31 or 41 wk of age. Egg weights in the 65-wk-old lines were not different until 61 wk of age when eggs from RIR hens were heavier than eggs from BR and CR hens, and WL-BUR eggs were heavier than CR eggs. Egg shell weights differed among the older lines at all age categories except 61 wk, with CR shell weights tending to be lower than the other lines. The WL-BUR shell weights were heavier than BR shells. The RIR hen albumen weights were greater than BR and CR in all 4 age categories. Egg yolk weights were greater in CR hens than WL-BUR and RIR hens at 31 and 41 wk of age and WL-BUR hens at 51 wk. No effect of line in yolk weight was observed at 61 wk of age.


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  		Table 3. The effect of line on egg quality: weight of eggs and egg components1
 
The radiographs displayed the whole skeleton and various fractures well (Figure 1Go). Overlying tissue, however, made some bones difficult to interpret, resulting in missing data points (ribs, sternal processes, left scapulae). It was not possible to distinguish fractures in vertebrae, although spinal curvatures were observed in some birds (data not shown).


Figure 1
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  		Figure 1. Examples of fractures observed using radiographs: A) ulna fracture; B) furculum fracture; C) pubic bone fracture. Arrows point to fractured bone.

 
The overall proportion of hens with at least 1 fracture was 6.6 and 15.7% in the 47- and 65-wk-old hens, respectively. All of the fractures in the younger 2 lines and 88% of the fractures in the 4 older lines were classified as old. Bones in the wing, furculum, and pubis were most affected. In the younger lines, there were no significant differences in fracture incidence overall or in individual bones (Table 4Go). Line differences were observed in the 65-wk-old hens, with almost 30% of RIR hens having at least 1 fracture, significantly more than CR or WL-BUR hens. The BR hens had more fractures than hens in the WL-BUR line. The RIR hen fractures were primarily in the furculum, followed by wing bones (humerus, radius, and ulna), whereas the pubic bones were most affected in the BR hens. Significant differences were found between all lines (within age groups) for body weights at the end of the trial (Table 4Go).


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  		Table 4. The effect of line on the incidence (%) of specific bones fractured1
 
Scallop-shaped indentations were observed on the keel bone in over half of the hens (Table 5Go), and line differences were found for the incidence and depth of indentations. The WL-BLK line had a greater incidence of indentation, and the indentations were larger compared with WL-BLU line. In the 65-wk-old lines, the incidence was greater in RIR hens than WL-BUR and CR hens. Indentation depth for the older lines was larger for RIR than WL-BUR and BR hens.


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  		Table 5. The effect of line on the incidence (%) and depth of scallop-shaped keel indentations1
 
Bone length, dry weight, and ash weight data were significantly greater in all 3 wing bones in the WL-BLK line as compared with WL-BLU line (Table 6Go). Percentage of ash of the ulna was also greater, but the humerus and radius were not affected. Line differences were observed in bone lengths in the 65-wk-old hens, with WL-BUR having shorter bones than the other 3 lines. Wing bones from WL-BUR hens also had lower dry weights and ash weights, except when compared with CR humeri. Bone dry weights were greatest in RIR hens for the humerus and radius. Humerus and radius ash weights were greatest in bones from RIR and BR hens, although RIR were not different than CR for ulna ash weight. The results of percentage bone ash varied with bone. In the humerus, percentage ash was lower in RIR hens than the other 3 lines. There was no effect of line on radius percentage ash, but WL-BUR hens had the greatest percentage of ash in the ulna.


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  		Table 6. The effect of line on bone parameters of the humerus, radius, and ulna1
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The flock as a whole (including the hens used in this study) performed well in terms of egg production, with 5 out of 6 lines peaking at over 90% hen-day egg production and approaching production levels of commercial lines (Silversides et al., 2007). The subgroup used in the present study was similar to the whole flock. The CR line stood apart from the other 3 in the older group of hens, with lower hen-day production in periods 2 and 3 and fewer eggs produced over the whole production period.

Fracture incidence in caged hens has been reported to range from 3.5 to 31% (Gregory and Wilkins, 1989; Gregory et al., 1990, 1993a, b; Budgell and Silversides, 2004). The proportion of birds with at least 1 fracture in the present study falls within this range, and 2 of the strains are at the greater end (RIR and BR). Studies have demonstrated that incidence of fracture is affected by handling and catching technique (Gregory et al., 1993a) and housing system (Gregory et al., 1990). The difference between lines in the present study agree with Bishop et al. (2000) and Budgell and Silversides (2004) in suggesting that there is a genetic component to bone fragility and fracture, although differences between commercial lines have not been noted (Gregory et al., 1990; Budgell and Silversides, 2004). Body weights may have also had an effect on fracture incidence. Knowles et al. (1993) observed that even though bone strength increased with bird weight, the chance of bone breakage also increased. The authors suggested that this was due to the heavier weight allowing for greater momentum during handling and therefore a larger force during any impact. The body weights in the hens from the current study were significantly different between all lines, and in the older birds, the incidence of hens with at least 1 fracture was greatest in the heavier lines.

The furculum, wing, and pubic bones were the main bones found to be fractured in this experiment, which is similar to observations in old breaks in battery hens by Gregory et al. (1990). There was also a high prevalence of keel deformities (36 to 88%), in the form of indentations along the ventral edge. These deformities may be a result of fracture, although this was not confirmed in the present study. Fleming et al. (2004) dissected keels from caged and free-run hens on 4 farms and found incidences of deformity ranging from 2.6 to 16.7%. The deformities were described as twisted (folded or compression) or severe. Histopathology of keels with the various deformities showed evidence of fracture healing, leading the authors to conclude that trauma, not developmental problems, was the cause (Fleming et al., 2004). If the keel deformities observed in hens in the present experiment were caused by bone fracture, the incidence is similar to that found in other housing systems (Wilkins et al., 2004; Nicol et al., 2006).

Wing bone parameters varied among lines in both age groups. The pattern of differences in bone dry and ash weights was similar to those observed in overall body weights, with heavier birds tending to have heavier bone dry and ash weights. However, when bone weight data were analyzed using bird weight as a covariate (results not shown), not all significant differences between lines were removed, suggesting that although body weight contributed to bone parameters, there was also a line effect. The proportion of bone that was mineralized (percentage of bone ash) varied differently among lines for each bone examined. The percentage of ash differences may be at least partially explained by differences in the presence of medullary bone, which decreases the percentage of ash (Clark et al., 2007). In addition, the bones were not fat-extracted before ashing, which may have contributed to variability in percentage of bone ash values.

High egg production is often considered a cause or factor in laying hen osteoporosis and subsequent bone fragility; however, this does not appear to completely explain the results in the present experiment. Two of the 65-wk-old lines, WL-BUR and RIR, had comparable hen-day egg production (all 3 periods), total egg production, and egg weights (second and third periods). In addition, egg shell weights, suggestive of calcium turnover, were similar between these 2 lines at all age periods examined. In contrast, the incidence of hens with at least 1 bone fracture was approximately 7 times greater in the RIR line than in the WL-BUR line. This suggests that the WL-BUR hens may have had more efficient calcium metabolism.

When wing bone data are compared with overall fracture data, no clear connections can be made. The 47-wk-old lines did not differ in fracture incidence, but significant differences were observed in bone length, dry weight, and ash weight of all 3 wing bones and percentage of ash in the ulna. Differences in overall fracture incidence in the 65-wk-old lines were similar to differences among the lines for bone dry and ash weights but were not comparable to percentage of ash data. If the 2 extremes of wing bone fractures are compared (RIR, 7.69%; WL-BUR, 0%) to the wing bone parameters, WL-BUR bones were shorter and lighter than RIR for all 3 bones but were greater in percentage of ash for the humerus and ulna, suggesting a possible difference in bone structure.

In conclusion, differences in fracture incidence were observed among genetic lines of high-producing, noncommercial laying hens in the present experiment. Differences were also found in the specific bones that were fractured, as well as the incidence of keel deformities. The data collected in this study do not give clear answers as to why there were large differences between lines in terms of bone fracture incidence, other than demonstrating that egg production was not the sole explanation. Differences could have been due to calcium metabolism, bone structure, or simply due to body weight differences. A combination of factors is most likely involved.


   ACKNOWLEDGMENTS
 
We would like to express thanks to B. McCannel, L. Struthers, H. Hanson, K. Ingram, M. Fraser and C. Johnson for their assistance with the various aspects of the study; S. Duncan and J. Berger for their assistance with the x-ray equipment setup; British Columbia Egg Producers (Abbotsford, British Columbia, Canada) for their financial support; and Vétoquinol Canada Inc. (Lavaltrie, Québec, Canada) for donation of the Euthanyl Forte.


   FOOTNOTES
 
1 Agriculture and Agri-Food Canada Contribution Number 769. Back

Received for publication March 14, 2008. Accepted for publication June 13, 2008.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Bishop, S. C., R. H. Fleming, H. A. McCormack, D. K. Flock, and C. C. Whitehead. 2000. Inheritance of bone characteristics affecting osteoporosis in laying hens. Br. Poult. Sci. 41:33–40.[Web of Science][Medline]

Brand, R. A., and C. T. Rubin. 1987. Fracture healing. Pages 325–345 in The Scientific Basis of Orthopaedics. 2nd ed. J. A. Albright and R. A. Brand, ed. Appleton & Lange, East Norwalk, CT.

Budgell, K. L., and F. G. Silversides. 2004. Bone breakage in three strains of end-of-lay hens. Can. J. Anim. Sci. 84:745–747.

Canadian Council of Animal Care. 1993. Guide to the Care and Use of Experimental Animals. 2nd ed. Vol. 1. Canadian Council of Animal Care, Ottawa, Ontario, Canada.

Clark, W. D., W. R. Cox, and F. G. Silversides. 2007. Radiodensity in the central cavity of humeri in high-producing noncommercial laying hens. Br. Poult. Sci. 48:647–650.[CrossRef][Web of Science][Medline]

Clark, W. D., E. L. Smith, K. A. Linn, J. R. Paul-Murphy, and M. E. Cook. 2005. Use of peripheral quantitative computed tomography to monitor bone healing after radial osteotomy in three-week-old chickens (Gallus domesticus). J. Avian Med. Surg. 19:198–207.[CrossRef]

Fleming, R. H., H. A. McCormack, L. McTeir, and C. C. Whitehead. 2004. Incidence, pathology and prevention of keel bone deformities in the laying hen. Br. Poult. Sci. 45:320–330.[CrossRef][Web of Science][Medline]

Gregory, N. G., and L. J. Wilkins. 1989. Broken bones in domestic fowl: Handling and processing damage in end-of-lay battery hens. Br. Poult. Sci. 30:555–562.[CrossRef][Web of Science][Medline]

Gregory, N. G., L. J. Wilkins, D. M. Alvey, and S. A. Tucker. 1993a. Effect of catching method and lighting intensity on the prevalence of broken bones and on the ease of handling of end-of-lay hens. Vet. Rec. 132:127–129.[Abstract]

Gregory, N. G., L. J. Wilkins, S. D. Eleperuma, A. J. Ballantyne, and N. D. Overfield. 1990. Broken bones in domestic fowls: Effect of husbandry system and stunning method in end-of-lay hens. Br. Poult. Sci. 31:59–69.[CrossRef][Web of Science]

Gregory, N. G., L. J. Wilkins, S. A. Tucker, D. M. Alvey, and C. G. Belyavin. 1993b. Effect of lighting pattern during lay on bone strength and the prevalence of broken bones in end of lay hens. J. Appl. Poult. Res. 2:103–106.[Abstract/Free Full Text]

Knowles, T. G., D. M. Broom, N. G. Gregory, and L. J. Wilkins. 1993. Effect of bone strength on the frequency of broken bones in hens. Res. Vet. Sci. 54:15–19.[Web of Science][Medline]

McCoy, M. A., G. A. C. Reilly, and D. J. Kilpatrick. 1996. Density and breaking strength of bones of mortalities among caged layers. Res. Vet. Sci. 60:185–186.[CrossRef][Web of Science][Medline]

National Research Council. 1994. Nutrient Requirements of Poultry. 9th rev. ed. National Academy Press, Washington, DC.

Nicol, C. J., S. N. Brown, E. Glen, S. J. Pope, F. J. Short, P. D. Warriss, P. H. Zimmerman, and L. J. Wilkins. 2006. Effects of stocking density, flock size and management on the welfare of laying hens in single-tier aviaries. Br. Poult. Sci. 47:135–146.[CrossRef][Web of Science][Medline]

Silversides, F. G., D. McQ. Shaver, and Y. Song. 2007. Pure line laying chickens at the Agassiz Research Centre. Anim. Genet. Resour. Inf. 40:79–85.

Strickberger, M. W. 1976. Pages 148–149 in Genetics. 2nd ed. MacMillan Publishing Co. Inc., New York, NY.

Wilkins, L. J., S. N. Brown, P. H. Zimmerman, C. Leeb, and C. J. Nicol. 2004. Investigation of palpation as a method for determining the prevalence of keel and furculum damage in laying hens. Vet. Rec. 155:547–549.[Abstract/Free Full Text]





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