Introduction
The keel bone, which runs axially along the middle of the sternum and extends outward in a perpendicular manner to the ribs, provides the anchor for the attachment for the large breast muscles of birds (Duncker, Reference DUNCKER2000). This allows a bird to fly or to flap its wings and attain short bursts of flight. Along with flight, the keel provides the bird with an anchor for its abdominal muscles, helping to provide proper ventilation of its lungs (Duncker, Reference DUNCKER2000). Because a laying hen lacks a proper muscular diaphragm, it must rely on the use of air sacs throughout its body for oxygen exchange. The abdominal muscles attached to the keel help to oscillate air throughout the air sacs and provide ventilation for the lungs during inhalation and exhalation (Claessens, Reference CLAESSENS2009). Since the keel bone provides the laying hen with assistance in important behavioural processes, such as wing flapping and physiological processes such as respiration, damage to this bone is detrimental to the bird. In the modern laying hen lines, low breast muscle mass leaves the keel bone vulnerable to damage, and it is one of the most common sites for fractures (Fleming et al., Reference FLEMING, MCCORMACK, MCCTEIR and WHITEHEAD2004; Wilkins et al., Reference WILKINS, MCKINSTRY, AVERY, KNOWLES, BROWN, TARLTON and NICOL2011). In a study performed by Wilkins et al. (Reference WILKINS, BROWN, ZIMMERMAN, LEEB and NICOL2004), 65% of the hens sampled from 10 flocks housed in alternative (non-cage) systems showed old bone fractures, and 90% of the damage was seen in the keel.
Birds have a unique bone development and structure compared to mammals. The structural bone formation (cortical and trabecular bones) is complete by the onset of sexual maturity in hens. At this point, due to hormonal changes (e.g. oestrogen), there is a shift towards the formation of medullary bone, which is the labile source of Ca for eggshell formation (Whitehead, Reference WHITEHEAD2004). However, bone resorption continues to happen, and is not limited to the medullary portion. Consequently, there is a progressive loss of cortical and trabecular bones throughout the layers’ life, which is a characterised by osteoporosis, resulting in fragile bones which are more susceptible to fracture (Whitehead, Reference WHITEHEAD2004; Gregory and Wilkins, Reference GREGORY and WILKINS1989). Looking more specifically into keel bone fracture, there is evidence that the keel bone ossification process is not complete at onset of lay and continues until approximately 40 weeks (Buckner et al., Reference BUCKNER, INSKO, HENRY, WACHS and MACLAURY1947). Therefore, when egg production starts and the demand for Ca for eggshell formation increases, there is still a portion of keel bone that remained as cartilage and may not be completely mineralised during the production phase (Casey-Trott et al., Reference CASEY-TROTT, GUERRIN, SANDILANDS, TORREY and WIDOWSKI2017; Riber et al., Reference RIBER, CASEY-TROTT and HERSKIN2018). Additionally, there is a reduction in radiographic density of keel during the production phase, which was more evident at the leading edge of the bone, adjacent to the rest of the sternum (Whitehead and Fleming, Reference WHITEHEAD and FLEMING2000).
Many methods for determining the state of the keel bone have been introduced. The most prevalent of these methods is known as palpation, a process in which one runs two fingers down the side of the keel bone, feeling for imperfections or calcium deposits and paying particularly close attention to the tip of the sternum (Wilkins et al., Reference WILKINS, BROWN, ZIMMERMAN, LEEB and NICOL2004). Signs of a keel bone fracture include sharp bends, fragmented sections, and shearing (Casey-Trott et al., Reference CASEY-TROTT, HEERKENS, PETRIK, REGMI, SCHRADER, TOSCANO and WIDOWSKI2015). Specific deformities, such as bent, curved, or S-shaped keels are usually found among laying hens, even when they have not experienced an actual fracture. These are simply characterised by notable imperfections in the architecture of the keel bone, which ideally, is a straight plane extended perpendicularly from the ribs (Fleming et al., Reference FLEMING, MCCORMACK, MCCTEIR and WHITEHEAD2004). While some fractures might not provoke intense discomfort in a laying hen, other more severe fractures can cause acute pain, reduction of mobility, with potentially fatal outcomes (Fleming et al., Reference FLEMING, MCCORMACK, MCCTEIR and WHITEHEAD2004).
Recent studies have shown that the overall incidence rate for keel bone damage has begun to rise over the past years, ranging up to 85% of birds per flock being affected (Casey-Trott and Widowski, Reference CASEY-TROTT and WIDOWSKI2016). A proponent in the rise in keel bone damage may be linked to the increase in cage-free systems. In 2012, conventional battery cage systems were outlawed in the European Union (Appleby, Reference APPLEBY2003). This directive was then followed by countries such as New Zealand and Australia and is currently gaining popularity in North America (Weeks et al., Reference WEEKS, LAMBTON and WILLIAMS2016). The aim of this paper is to review the incidence of keel bone damage in laying hens for the three main housing systems (conventional or enriched cages, and cage-free systems) found in the current poultry industry, as well as to suggest possible solutions for the problems that laying hens currently face in respect to such damage.
A comparison of prevalence of keel bone damage in housing systems
The main housing systems found in current egg production are conventional cages, enriched cages and cage-free systems, which include multi-tier, barn, free-range and organic productions. While legislation has made battery cages illegal in Europe, laying hens in the United States are still predominantly housed this way (Pohle and Cheng, Reference POHLE and CHENG2009). Guidelines are followed to ensure bird health, with enough room for the hen to stand upright in the cage and optimise the welfare of the hens (Animal Husbandry Guidelines, 2010). Regardless of the actual advantages of the conventional battery cage system, there is still prevalent public concern for the welfare of hens. Enriched cages attempt to improve the environment and lifestyle of commercial laying hens. They are equipped with perches, dust-bath areas, and nesting areas, and strive to proliferate the opportunities for the birds to exhibit their natural behaviours (Pohle and Cheng, Reference POHLE and CHENG2009). The cage-free systems provide the most freedom of movement when compared to conventional cages and enriched cages, allowing the hens to walk, run, and fly (Rodenburg et al., Reference RODENBURG, TUYTTENS, SONCK, DE REU, HERMAN and ZOONS2005). Each cage-free system can house thousands of hens together and can be furnished with nesting areas, dust bath areas, and perches (Doyon et al., Reference DOYON, BERGERON, CRANFIELD, TAMINI and CRINER2016).
Several studies have investigated the prevalence of keel bone fracture using different house designs, genetic lines and ages (Wilkins et al., Reference WILKINS, BROWN, ZIMMERMAN, LEEB and NICOL2004; Sherwin et al., Reference SHERWIN, RICHARDS and NICOL2010; Wilkins et al., Reference WILKINS, MCKINSTRY, AVERY, KNOWLES, BROWN, TARLTON and NICOL2011; Petrik et al., Reference PETRIK, GUERIN and WIDOWSKI2015). Although bone health may be reduced due to restricted movement in conventional cages (contributing to the development of conditions like osteoporosis), conventional caged systems tend to have lower incidence of fractures due to the hens’ restricted movements and the lack of potential hazards (Fleming et al., Reference FLEMING, MCCORMACK, MCCTEIR and WHITEHEAD2004; Wilkins et al., Reference WILKINS, BROWN, ZIMMERMAN, LEEB and NICOL2004). Old fractures, which occurred prior to depopulation and have resulted in the formation of a callus, represent a great concern because they can lead to chronic pain (Sandilands et al., Reference SANDILANDS, MOINARD and SPARKS2009; Lay et al., Reference LAY, FULTON, HESTER, KARCHER, KJAER, MENCH, MULLENS, NEWBERRY, NICOL, O'SULLIVAN and PORTER2011), reducing welfare and potentially interfering with production. Overall, cage free systems have a significantly larger prevalence of keel damage when compared to the other housing systems (Wilkins et al., Reference WILKINS, MCKINSTRY, AVERY, KNOWLES, BROWN, TARLTON and NICOL2011), due largely to the use of the perch, a location where laying hens can reach to rest (Casey-Trott and Widowski, Reference CASEY-TROTT and WIDOWSKI2016). Even though the installation of perches has been shown to improve bone mineral density (Tactacan et al., Reference TACTACAN, GUENTER, LEWIS, RODRIGUEZ-LECOMPTE and HOUSE2009), it can increase bone breakages during landing failures when jumping (Lay et al., Reference LAY, FULTON, HESTER, KARCHER, KJAER, MENCH, MULLENS, NEWBERRY, NICOL, O'SULLIVAN and PORTER2011). It is important to arrange the perches according to bird density and the house should be designed in order to avoid fractures and improve bone health.
Sherwin et al. (Reference SHERWIN, RICHARDS and NICOL2010) assessed welfare of hens in 26 flocks housed in conventional cages, furnished cages, barn and free-range systems, with the prevalence of keel bone protrusion, fracture or deformation as an indicator of welfare. The birds were examined post-mortem. The overall prevalence of keel fracture was of 55.7% for all hens, with 84.8% being old and 47% being recent fractures. The keel protrusion prevalence was worse in the free-range system compared to the others; with old fractures being worse in barn (69.1%) and free-range (59.8%) systems compared to furnished cages (31.7%) and conventional cages (24.6%); and recent fractures were higher in conventional cage (24.6%) systems. The latter was mainly caused during depopulation, handling and transport. The furnished cage system has been proposed as most welfare-friendly. However, the authors concluded that, despite the differences between the four housing systems, the indicators of reduced welfare were present at high rates in all of them.
A study performed by Wilkins et al. (Reference WILKINS, MCKINSTRY, AVERY, KNOWLES, BROWN, TARLTON and NICOL2011) evaluated the prevalence of old fractures in 67 flocks of laying hens at the end of production, which they categorised as free-range, organic, barn and furnished cage systems. The authors reported that the prevalence of keel damage observed in flocks housed in non-cage systems was 28 to 95% when assessed by palpation, and 30 to 95% when assessed by dissection, and in furnished cages the prevalence was assessed to be 22 to 44%, and 15 to 55%, respectively. Conventional cages were not a part of this study.
Another study by Petrik et al. (Reference PETRIK, GUERIN and WIDOWSKI2015) showed the differences in incidence of keel fractures among cage-free and conventional caged housing systems. Throughout the entire 65-week study, fractures were always higher among the laying hens housed in the cage-free systems. Interestingly, more than half of the cage-free systems in this study did not have perches, yet the fracture prevalence was still much higher compared to caged hens. This higher prevalence could be due to collisions between birds on the floor or attempted jumping or flight upon agitation, followed by a bad landing.
Implications of keel bone damage
Bone fractures are a painful experience for any human. There is some discrepancy whether fractures of the keel are painful to laying hens. A study done by Nasr et al. (Reference NASR, NICOL and MURRELL2012a) hypothesised that the birds do indeed feel pain when their keel is damaged. They came to this conclusion by comparing the movements of birds with keel bone damage when injected with analgesics to birds with keel bone damage injected with a control saline solution. The researchers noticed that while the birds treated with pain medicine were able to move more freely despite their damaged keel, while the saline group still favoured and guarded their injuries.
While birds do indeed feel pain when they obtain a keel bone injury, this injury affects their daily routine. Another study showed that laying hens with keel fractures had a much slower mobility, took a longer time to fly up to perches, and spent more time sleeping on the floor than hens without damage (Nasr et al., Reference NASR, MURRELL, WILKINS and NICOL2012b). It has been shown that the egg production of birds with keel fractures was 6% lower than from birds without fractures (Nars et al., Reference NARS, MURRELL and NICOL2013). With this information, it can be concluded that keel fractures can negatively affect a hen in its day-to-day life, causing it pain, and restricting its movements.
Potential solutions
Despite cage-free systems having the highest rate of incidence in keel bone damage for laying hens, there is consumer pressure on the poultry industry to make the switch to the cage-free system (Wilkins et al., Reference WILKINS, MCKINSTRY, AVERY, KNOWLES, BROWN, TARLTON and NICOL2011). While conventional cages have already been outlawed in the European Union, increased pressure is being applied to the poultry industry in the United States to make the change as well (Weeks et al., Reference WEEKS, LAMBTON and WILLIAMS2016). Because of this switch, it is important to identify efficient methods that could potentially increase the welfare of laying hens.
One possible solution to the problem of increased keel bone damage is genetic selection. A study done by Fleming et al. (Reference FLEMING, MCCORMACK, MCCTEIR and WHITEHEAD2004) showed that it is possible to decrease the incidence of keel damage and fractures by genetically selecting laying hens for stronger keel bones. Through selecting over five generations of laying hens, they were able to increase bone density in the keel, and decrease the incidence of fractures, deformation and other damage. Additionally, Candelotto et al. (Reference CANDELOTTO, STRATMANN, GEBHARDT-HENRICH, RUFENER, VAN DE BRAAK and TOSCANO2017) were able to eliminate environmental and behaviour components (possible confounding factors), isolating the contribution of genetic variation to keel bone fracture. The authors found a clear difference in frequency of experimental fractures between crossbred and pure lines and confirmed the influence that genetics have in the susceptibility to keel bone fractures.
There are possible nutritional interventions that could be made to potentially increase bone, and hence, keel strength in laying hens. Laying hens need a large amount of calcium in their diets in order to combat losses from egg laying. While birds eat and absorb calcium during the day, they sleep (and therefore do not consume any calcium) during the night. When they are sleeping, their bodies use osteoclasts to break down bone and release calcium to the bloodstream, which can weaken the bones and cause osteoporosis when the hens are not correctly supplemented with calcium during the day (Whitehead and Fleming, Reference WHITEHEAD and FLEMING2000). One study by Guionette et al. (Reference GUIONETTE, GAUTRON, NYS and SOURMARMON1995) found a way to decrease osteoclast activity at night, leading to stronger bones overall, by giving hens access to sources of calcium with larger particle sizes. These large particle sizes require a longer time to digest, continuing into the night, and reducing the amount of time that osteoclasts would be active. This would reduce the amount of bone deterioration in the night, and result in decreased risk of osteoporosis.
Vitamin D3 supplementation shows promising potential in increasing bone strength and density among poultry. A study performed by Rao et al. (Reference RAO, RAJU, PANDA, SAHARAI, REDDY, SUNDER and SHARMA2008) observed the effect of excess vitamin D3 concentration on bone mineralisation of commercial broiler chicks. They found that by supplying excess vitamin D3, not only did the bone weight and strength increase, but serum calcium concentration increased as well. By adding supplemental vitamin D3 as well as larger calcium particles into the diet of laying hens, bone strength, and therefore keel strength, could increase.
Housing design plays a key role in the amount of keel bone damage found in laying hens. Wilkins et al. (Reference WILKINS, MCKINSTRY, AVERY, KNOWLES, BROWN, TARLTON and NICOL2011) reported that keel fractures had a 10-34% increase when metal perches were added to a cage-free system. While metal perches do not offer much grip for hens, often resulting in birds slipping and falling, a possible solution could be to provide perches with a rubber layer, which would reduce pressure on the keel as well as providing a grip for the birds upon landing (Scholz et al., Reference SCHOLZ, KJAER and SRADER2014). Stratmann et al. (Reference STRATMANN, FRÖHLICH, HARLANDER-MATAUSCHEK, SCHRADER, TOSCANO, WÜRBEL and GEBHARDT-HENRICH2015a) compared the use of soft perches (covered with polyurethane material) vs. metal perches, and the incidence of keel bone fractures/deviations in two hen strains in cage-free systems. The authors found less keel damage over the course of the laying period when perches were covered with the soft material (44.9%) compared to the metal ones (60.2%). However, at the end of the experiment (64 weeks of age), the incidence of fractures was similar (30%) between the types of perches, indicating that there may be limits to the benefits of soft perches. In addition to the soft material, there may be an influence of perch diameter, since the soft perch was double the size of the metal perch. Therefore, it is necessary to investigate further what brings more benefits by reducing keel damage: the diameter or the material of the perch.
Another possible solution to keel bone damage would be to provide ramps to perches, keeping birds from flying into the bars and crashing into the perches at a high speed (Heerkens et al., Reference HEERKENS, DELEZIE, AMPE, RODENBURG and TUYTTENS2016). Stratmann et al. (Reference STRATMANN, FRÖHLICH, GEBHARDT-HENRICH, HARLANDER-MATAUSCHEK, WÜRBEL and TOSCANO2015b) studied the use of cage-free system with perches, ramps or platforms, and found, at 60 weeks of age, that the use of ramps reduced the number of fractured keel bones by 23% compared to the control group (without modification). The authors found a significant reduction in collisions, falls and increase in controlled movements with the use of the ramps. Finally, providing more adequate lighting might help to prevent keel bone damage, so that birds will be able to see the perch they are aiming for, decreasing the amount of collisions that occur between the hen and the perch, and providing a safer landing for the bird (Moinard et al., Reference MOINARD, STATHAM, HASKELL, MCCORQUODALE, JONES and GREEN2004).
Conclusions
Several studies have compared the prevalence of keel bone fracture in different housing systems (Sherwin et al., Reference SHERWIN, RICHARDS and NICOL2010; Wilkins et al., Reference WILKINS, MCKINSTRY, AVERY, KNOWLES, BROWN, TARLTON and NICOL2011; Petrik et al., Reference PETRIK, GUERIN and WIDOWSKI2015). However, the prevalence of keel bone damage varies considerably among the studies due to differences in the system design, genetic line, age and method for determining the keel damage (e.g. palpation, post-mortem necropsy, and x-ray), which makes it difficult to compare results. Additionally, keel bone is not the only problem experienced by laying hens, and, even though it is an important influencer in the welfare and production, other factors should be considered in order to determine the best system. While the available literature discusses the possible causes and repercussions of keel bone damage, as well as potential solutions to this problem, there is still more work to be done in order to fully cover the breadth of this topic. Research in this area is increasingly important, as there is growing pressure from consumer groups and retailers for farmers to abandon conventional battery cages and move towards cage-free housing systems for laying hens.
