Osteoporosis in Cage Layers
C. C. Whitehead1 and R. H. Fleming
Roslin Institute, Roslin, Midlothian EH25 9PS, Scotland
ABSTRACT Osteoporosis in laying hens is a condition
that involves the progressive loss of structural bone during the laying period. This bone loss results in increased
bone fragility and susceptibility to fracture, with fracture
incidences of up to 30% over the laying period and depopulation not uncommon under commercial conditions. A
major cause of osteoporosis is the switch in bone formation from structural to medullary bone at the onset of
sexual maturity, but structural bone loss is accelerated
by the relative inactivity of caged birds. Allowing birds
more exercise, as in aviary systems, results in better bone
quality but may not decrease the overall fracture incidence. Good nutrition can help to minimize osteoporosis
but is unable to prevent it. Best nutritional practice involves transferring birds to a higher calcium diet at light-
ing up rather than at first egg, providing a source of
calcium in particulate form, and not withdrawing feed
some days before depopulation. Breeding may be an effective way of combating ostoporosis. Some bone strength
traits have been shown to be heritable, and divergent
selection for resistance or susceptibility to osteoporosis
has resulted in lines with markedly different bone characteristics. After three generations of selection, the lines
differ by 19% for keel bone mineral density, 13% for humerus breaking strength, and 25% for tibia breaking
strength and show a sixfold difference in fracture incidence under commercial breeding conditions. The difference in bone quality among the lines is maintained under
different housing systems.
(Key words: bone, laying hen, genetics, nutrition, osteoporosis)
2000 Poultry Science 79:1033–1041
INTRODUCTION
Osteoporosis in laying hens is defined as a decrease in
the amount of fully mineralized structural bone, leading
to increased fragility and susceptibility to fracture. It contrasts with another cause of bone mineral loss, osteomalacia, in which defective mineralization of bone tissue occurs, with thick seams of poorly mineralized organic matrix. Both conditions will lead to poor quality bone, but
osteomalacia is primarily associated with nutritional deficiencies of calcium, phosphorus, or vitamin D, whereas
osteoporosis is an altogether more complex problem.
In poultry, a condition involving bone loss, characteristic of osteoporosis, was first described in caged laying
hens by Couch (1955), who reported a problem termed
cage layer fatigue involving bone brittleness, paralysis,
and death. More recently, confirmation of osteoporosis
as the main reason for bone loss and subsequent fractures
in laying hens has been provided (Randall and Duff,
1988). The consequences of osteoporosis for the laying
hen skeleton can be severe. Caged layer fatigue seems to
be an extreme consequence of loss of structural bone in the
vertebrae that leads to spinal bone collapse and paralysis
Received for publication December 15, 1999.
Accepted for publication February 7, 2000.
1
To whom correspondence should be addressed: colin.whitehead@
bbsrc.ac.uk.
(Urist and Deutsch, 1960; Bell and Siller, 1962). Generally,
osteoporosis is not so severe as to result in caged layer
fatigue, but widespread structural bone loss can lead to
high incidences of fractures at various sites throughout
the skeleton.
Gregory and Wilkins (1989) reported results of a survey
of end-of-lay battery hens in the United Kingdom in
which 29% of hens had one or more broken bones during
their lifetimes. The fractures occurred during their time
in their cages or during depopulation, transport to a processing factory, and hanging on shackles. Astonishingly,
98% of carcasses were found to contain broken bones by
the time they reached the end of the evisceration line. A
subsequent survey of many European flocks confirmed
these findings, showing that, on average, fractures were
received by 10% of hens during their time in batteries
and a further 17% during depopulation and transport
(Gregory et al., 1994). The high fracture incidences show
that osteoporosis constitutes a severe welfare problem in
hens. Production losses and mortality also arise with
caged layer fatigue. These economic losses are compounded by the high fracture incidences during carcass
processing that lead to bone splinters in recovered meat
and have resulted in processors becoming unwilling to
handle spent layers (Brown, 1993).
Abbreviation Key: FTV = free thoracic vertebra; PTM = proximal tarsometatarsus.
1033
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WHITEHEAD AND FLEMING
The origins of osteoporosis are not well defined.
Whitehead and Wilson (1992) suggested that the problem
is partly genetic in origin, resulting from the breeding of
light-weight, energetically efficient birds that maintain a
high rate of lay over a prolonged period. Most modern
hybrid layer strains seem to be susceptible to osteoporosis, but older unimproved strains, such as the Roslin Jline Brown Leghorn, are relatively resistant (Rennie et
al., 1997). However, even in susceptible strains there can
be wide individual variation, with some hens retaining
good bone quality at end of lay. Confinement of birds in
cages with limited opportunity for exercise has undoubtedly contributed to the problem, resulting in a form of
disuse osteoporosis. The characteristics of osteoporosis
and the various factors influencing it are described in the
following sections.
CHARACTERISTICS OF OSTEOPOROSIS
Bone Types and Turnover
Bone is made up of hydroxyapatite crystals of calcium
phosphate deposited on an organic collagen matrix. There
are several different bone types in laying hens. The main
types providing structural integrity are cortical and cancellous (or trabecular) bone, both of which are forms of
lamellar bone. These bone types are formed during
growth, but when a hen reaches sexual maturity, a third
type of nonstructural bone, medullary bone, is formed.
After formation, bone undergoes a constant process of
remodeling, in which osteoclast cells resorb areas of bone
and are then replaced by osteoblasts that deposit new
bone. Osteoporosis arises where there is an imbalance
between these processes, resulting in a net resorption of
structural bone.
Medullary bone is a woven bone whose purpose is to
provide a labile source of calcium for shell formation. It is
characterized by the haphazard organization of collagen
fibres in its matrix and is mechanically weaker than structural bone types. Medullary bone occurs as spicules
within the marrow cavity and as a layer lining the surfaces
of structural bone components. The highest content of
medullary bone is usually found in the leg bones. The
mineral density of medullary bone is usually similar to
that of cancellous bone, so measures of radiological density or ash content in these bones give little information
relevant to osteoporosis.
The conventional view that medullary bone contributes
little to overall bone strength may not be totally correct.
The layer of medullary bone may sustain the connectivity
of trabecular bone during osteoporosis (Figure 1), and
the spicules may increase fracture resistance. More direct
evidence comes from observations on the humerus. This
bone is usually pneumatized as a genetic adaptation to
flight. However, variable proportions of hens in different
flocks can have nonpneumatized humeri that can contain
marrow and medullary bone for reasons that are unknown. The amount of medullary bone varies from a
partial filling around the periphery of the cortical cavity
FIGURE 1. Histological section of bone of a laying hen showing
trabecular bone (TB) coated with darkly stained medullary bone (MB).
Arrows indicate where the medullary bone helps to connect trabeculae.
to complete filling of the cavity. Measurements of humeral bone three-point breaking strength have been
highly correlated with the amount of humeral medullary
bone present (Fleming et al., 1998a). Medullary bone may
thus make some contribution to the overall fracture resistance of bone, although not to the same degree as structural bone.
Development of Osteoporosis
Some of these characteristics of laying hen osteoporosis
have been reviewed by Whitehead and Wilson (1992).
Osteoporotic hens show evidence of widespread loss of
structural bone throughout the skeleton. This loss has
been shown to start when hens reach sexual maturity and
to continue throughout the laying period (Wilson et al.,
1992) so that osteoporosis is most severe in hens at the
end of lay. Those observations are consistent with the
theory that at the onset of sexual maturity the rise in
circulating oestrogen results in a switch in bone formation
from structural to medullary bone and that continued
resorption of structural bone leads to osteoporosis. Osteoblast activity is regulated by estrogen, and it is likely that
the estrogen surge at sexual maturity stimulates formation of woven rather than lamellar bone. Evidence for a
depression in structural bone formation in laying hens
has been provided by Hudson et al. (1993) who observed
that fluorochrome label was not incorporated into cortical
bone. These findings have been confirmed by Fleming
(unpublished data) who also observed that loss of reproductive condition induced by forced moulting resulted in
rapid loss of medullary bone and resumption of structural
bone formation (Figure 2).
As osteoporosis progresses, cortical bone thickness is
decreased, and there is a less cohesive system of fewer,
thinner, and less well-connected trabeculae. This progression is reflected in lower breaking strengths, as measured
SYMPOSIUM: SKELETAL BIOLOGY AND RELATED PROBLEMS IN POULTRY
by the three-point bending test. Amounts of structural
bone can also be quantified by computerized histomorphometric analysis or by radiography for bones that contain little or no medullary bone. Other measures that have
been made to assess osteoporosis include cancellous bone
volumes of the free thoracic vertebra (FTV) and proximal
tarsometatarsus (PTM), radiographic densities of humerus and keel, and breaking strengths of humerus and
tibia. Whitehead and Wilson (1992) proposed a system
for assessing the severity of osteoporosis based on FTV
trabecular bone volume, with values greater than 16%
being normal, 14 to 16% being moderate, 8 to 11% being
severe, and <8% being very severe.
Patterns of bone loss with age vary among different
bones, as shown in Figure 3 (Fleming et al., 1998b). Striking changes occurred during the first 10 wk of sexual
maturity. A marked loss of cancellous bone occurred in
both the PTM and FTV, suggesting that, in these bones,
the major development of osteoporosis occurs within a
few weeks of the onset of egg production. Over this period
medullary bone rapidly accumulated in the PTM, but at
present there is no indication as to whether the loss of
cancellous bone is directly linked to the formation of
medullary bone. After 25 wk, further loss of cancellous
bone from the FTV is smaller, but loss of cancellous bone
and accumulation of medullary bone continue in the
PTM, although at reduced rates. However, there was a
continuous net increase in the total amount of bone, measured histomorphometrically, with the result that total
bone volume in the PTM can be greatest at 70 wk.
In bones apart from the PTM, radiographic density was
taken as an indirect measure of amount of bone material.
In the FTV, radiographic density increased between 15
and 25 wk whereas cancellous bone volume decreased.
Although relatively small amounts of medullary bone
form in the central parts of the FTV, this increase in density could, perhaps, be accounted for by accumulation
of medullary bone in the subchondral area. Subsequent
FIGURE 2. Histological section of bone from a hen that has gone
out of lay. Medullary bone (MB) has been overlaid by a newly formed
layer of trabecular bone (TB).
1035
FIGURE 3. Change with age in the volumes of different types of
bone in the proximal tarsometatarsus (PTM) and free thoracic vertebra
(FTV) in the laying hen.
decreases in radiographic density would be consistent
with the small decline in cancellous bone volume.
Tibial radiographic densities and breaking strengths,
both measured in the midshaft region, increased from
15 to 25 wk. The laying hen tibia is known to contain
appreciable amounts of medullary bone, and the increase
in radiographic density would be consistent with this
occurrence. The small increase in tibial breaking strength
between 15 and 25 wk could indicate some accumulation
of medullary bone but relatively little loss of structural
bone. The major decrease in bone strength between 25
and 50 wk implies considerable loss of structural bone,
which in the midshaft region of the tibia is mainly cortical
bone. These observations contrast with the findings in
the PTM that major structural bone loss occurred within
10 wk of sexual maturity and suggest that different principles may apply to structural bone resorption from epiphyseal and midshaft regions of leg bones. An important
factor in this difference may be the greater resorptive
surface areas of bone contained in the trabecular structures in epiphyseal regions than in the diaphyseal cortex.
The increases in humerus radiographic density and
breaking strength observed between 15 and 25 wk may
be accounted for by the development, in some birds, of
medullary bone in bones that are normally pneumatized
together with the absence of any appreciable loss of structural bone over this period. The subsequent large decline
in breaking strength after 25 wk would suggest that in
this bone, as in the tibia, the major onset of osteoporosis
occurs at a later age than for the PTM or FTV.
The radiographic density of the keel can also decline,
particularly at the leading edge of this bone adjacent to
the rest of the sternum (Figure 4). A more general increase
in keel radiographic density seen later in the laying period
1036
WHITEHEAD AND FLEMING
is consistent with the known presence of medullary bone
and does not give any insight into possible changes with
time in the structural component.
Consequences of Osteoporosis
The decline in structural cortical and trabecular bone
components does not cause changes in the external dimensions of long bones because cortical bone resorption
is confined to endosteal surfaces. However, the thinning
of cortical bone and loss of trabecular integrity results in
bones becoming weaker and more susceptible to fracture
if subjected to trauma. Ischium, humerus, keel, and furculum showed highest fracture incidences, with pubis, ulna,
coracoid, and femur also breaking frequently (Gregory
and Wilkins, 1989). Different fractures can occur at different stages in the birds life. In a survey of European flocks,
Gregory et al. (1994) reported that 17% of birds experienced fractures during battery cage life (old breaks) and
10% during depopulation, transport, and hanging on
shackles (new breaks). Fractures to the humerus and ulna
FIGURE 4. Radiographs of the keels of laying hens showing (a.)
radiodense bone (white area) at the front edge of the keel and (b.) loss
of bone density in this area in an osteoporotic hen. The loss of bone
density leads to fractures in this area.
FIGURE 5. Radiograph of the wing of a laying hen showing a spiral
fracture in the humerus. A fracture callus has formed and started the
healing process.
are frequent old breaks. Damage to the keel can arise
from contact with the cage front during depopulation,
and femur breaks arise commonly during shackling.
Fractures of the humerus are usually of the spiral type
(Figure 5), suggesting torsional forces arising from violent
contact with the cage. These fractures usually repair, with
the fracture callus able to unite quite widely displaced
bone surfaces. Fractures of the keel occur at the point of
bone erosion at the front edge shown in Figure 4 and
result in the bone bending over along the line of the
keel. Attempts at repair result in new bone growth in the
original direction of the keel and can result in a characteristic deformity. These repairs to different bones involve
the initial formation of fracture callus followed by structural bone and show that local factors can override the
more general suppression of structural bone formation
during lay.
Spinal bones can be severely affected by osteoporosis,
but fractures are rarely observed. Instead, the loss of trabecular and cortical bone (Figure 6) can lead to exposure
of the spinal column and it is presumed that pressure on
exposed nerves accounts for the paralysis observed for
caged layer fatigue. These lesions may also repair because
provision of extra calcium can result in recovery, although
this recovery may also be assisted by a temporary loss
of reproductive condition.
The welfare problem of osteoporosis is generally assessed in relation to fracture incidence. Avian bones are
enervated, and it is assumed from human analogy that
avian fractures are also painful. However, it is possible
that pain may also arise, in the absence of overt fracture,
from exposure of nerves.
SYMPOSIUM: SKELETAL BIOLOGY AND RELATED PROBLEMS IN POULTRY
FIGURE 6. Radiographs of the free thoracic vertebrae of laying hens
showing (a.) normal mineralization and (b.) severe loss of structural
bone brought about by osteoporosis. The radiographs were taken at the
same exposure.
EFFECTS OF EXERCISE AND
HUSBANDRY SYSTEM
Effects on Bone Characteristics
The effects of load-bearing and biomechanical forces
in stimulating bone formation and remodeling are well
established (Lanyon, 1992). Induced inactivity has been
shown to accelerate osteoporosis in birds (Nightingale et
al., 1972), and relative lack of activity of battery caged
hens accounts for the severity of the problem in these
birds. Effects of exercise and alternative housing systems
have been widely studied as potential means of alleviating osteoporosis.
Effects of exercise as a way of stimulating bone growth
during rearing have been studied, but neither housing
birds in pens nor giving extra exercise through use of a
carousel have improved bone quality at the start of lay
compared to cage rearing (Whitehead and Wilson, 1992).
Changes in bone quality during the laying period are
influenced by the nature of the exercise involved. Housing hens in pens has resulted in little change in spinal
trabecular bone (Wilson et al., 1993). This finding suggests
that merely allowing the birds more opportunity to walk
does not result in generalized bone improvements, although the limited nature of those observations did not
preclude the possibility of more local benefits, such as
in leg bones. Fitting perches to cages resulted in small
1037
improvements in PTM trabecular bone volume but no
benefit in tibia strength (Hughes et al., 1993). More vigorous exercise than walking or hopping onto low perches
is needed to markedly improve bone quality. This finding
was demonstrated by Knowles and Broom (1990), who
found superior tibia and humerus breaking strengths in
birds housed in terrace or perchery systems rather than
in cages. The improvement in humerus strength was particularly apparent in the perchery system that allowed
birds to fly.
Confirmation of these findings came from a more detailed study by Fleming et al. (1994) involving comparison
of battery cages with three different aviary systems. Considerable improvements in a wide range of bone morphometric and strength characteristics were observed in birds
housed in aviaries (Table 1), with the greatest improvement being in the strength of the humerus. The improvements in the strength of this bone was more pronounced
in the perchery, which was tiered with many high
perches, compared with the litter and wire system that
had only relatively low perches. Thus, opportunity for
flight was an important factor in improving humerus
strength. These findings for hens are consistent with findings for other species that biomechanical effects on individual bones are dependent upon the degree of strain
experienced by the bone.
There is little information on the mechanism by which
exercise improves bone characteristics in the hen. However, the finding by Newman and Leeson (1998) that tibial
strength increased within 20 d of transfer of hens from
cages to an aviary suggests that the mechanism may involve stimulation of structural bone formation, rather
than inhibition of resorption.
Welfare of Hens in
Different Housing Systems
There have been several studies to determine the welfare impact of the improved bone strength of birds kept
in alternative housing systems. Lower incidences of new
breaks have been found in birds depopulated from aviary
or free-range systems compared to battery cages (Gregory
et al., 1990; Van Niekerk and Reuvekamp, 1994). However, the incidences of old breaks, particularly in the furculum and keel, were higher with aviary and free-range
systems (Gregory et al., 1990). It may be concluded that
allowing birds more exercise in alternative systems will
improve bone strength, but this does not necessarily improve bird welfare proportionately. Birds in alternative
systems have greater opportunity to experience more
damaging accidents than do caged birds. For instance,
they can crash during flight, fall, or be pushed off perches.
It is likely that the designs and stocking densities of alternative husbandry systems can be established to minimize
welfare problems associated with osteoporosis. However,
alternative systems are also associated with other welfare
problems, such as feather pecking and cannibalism. Abolition of battery cages is not a simple panacea for welfare
1038
WHITEHEAD AND FLEMING
TABLE 1. Bone characteristics in end-of-lay hens housed in different husbandry systems
Husbandry system
Trait
Battery cage
Litter and wire
Perchery
Proximal tarsometatarsus
Cancellous bone volume (%)
14.2a
16.7b
16.8b
11.3a
13.6b
16.6c
21.8a
2.95a
25.7b
3.48b
28.6b
3.33b
13.1a
0.51a
0.75a
22.6b
0.67b
1.11b
25.4c
0.72b
1.25c
Free thoracic vertebra
Cancellous bone volume (%)
Tibia
Breaking strength (kg)
Radiographic density
(mm Al equivalent)
Humerus
Breaking strength (kg)
Cortical width (mm)
Radiographic density
(mm Al equivalent)
Within a row, values followed by a different letter differ significantly (P < 0.05) (Fleming et al., 1994).
a–c
problems, and it is apparent that alternative or additional
approaches to minimizing osteoporosis are needed.
EFFECTS OF NUTRITION
Nutritional deficiencies of calcium, phosphorus, or cholecalciferol have been shown to result in bone loss attributable to osteomalacia (Wilson and Duff, 1991) and are
likely to lead ultimately to greater severity of osteoporosis. However, there is no evidence that avoidance of osteomalacia can prevent the development of osteoporosis. A
recent study (Rennie et al., 1997) investigated the effects
of a number of dietary factors during the laying period
on bone composition. None of the factors had any effect
on the proportions of cancellous bone in spinal (FTV)
or leg (PTM) bones, but treatments involving feeding a
particulate source of calcium (oystershell) or supplementation with fluoride increased the proportions of medullary bone. Providing calcium in particulate form extends
the period of calcium absorption later into the night when
shell formation is taking place and has been shown to
have beneficial effects on shell quality. Provision of calcium with improved digestive characteristics can increase
the amount of medullary bone without having much impact on the loss of structural bone and shows that calcium
deficiency is not a primary cause of osteoporosis. Fluoride
is known to stimulate bone formation in other species,
but the increase in synthesis in hens is evidently confined
to medullary bone. Increases in medullary content may
nonetheless have a beneficial effect on bone quality, as
discussed earlier. Confirmation of the practical benefits
of particulate calcium sources has been provided by Fleming et al. (1998b) who found that feeding limestone particles resulted in improved bone strength in older hens.
This effect was probably attributable to the observed increase in medullary bone formation because the treatment
had little effect on cancellous bone volumes, as shown in
Table 2.
Nutrition during rearing is also important in maximizing bone content before the onset of sexual maturity.
Dietary supplementation with extra vitamin K during
rearing, a factor required for the synthesis of osteocalcin,
a protein involved in bone formation, may also benefit
some aspects of bone quality (Fleming et al., 1998b).
These observations are consistent with the hypothesis
that osteoporosis in hens arises as a result of cellular
processes rather than nutrient supply and that during the
laying period there is continued osteoclastic resorption
but little formation of structural bone. The balance of
cellular activity can be altered by feeding bisphosphonate,
a drug used in human medicine to combat postmenopausal osteoporosis. This drug acts by inhibiting the action of osteoclasts and has been shown to slow the loss
of cancellous bone in hens (Thorp et al., 1993). However,
use of bisphosphonate is unlikely to be a practical solution
for laying hen osteoporosis.
GENETIC FACTORS
The large individual variation observed in the bone
characteristics of hens at the end of lay, phenotypically
unrelated to egg production in a flock of highly productive hens (Rennie et al., 1997), suggests that osteoporosis
may be alleviated by genetic selection, perhaps without
serious consequence for egg productivity.
The possibility of a genetic solution to osteoporosis has
been studied by Bishop et al. (2000). The inheritance of
characteristics related to osteoporosis was studied over
five generations in a commercial pure line of White Leghorns previously selected for high egg production. Initially, measurements were made on a range of morphometric, radiologic, and strength characteristics of different
bones in hens at the end of the laying period to determine
heritabilities. Morphometric traits involving cancellous
and medullary bone volumes were found to be poorly
heritable (FTV cancellous bone volume, h2 = 0.19 and
PTM cancellous bone volume, h2 = 0.0). This finding was
surprising in view of the use of cancellous bone to assess
severity of human postmenopausal osteoporosis (Khosla
et al., 1994) and as a criterion in earlier laying hen studies
(Whitehead and Wilson 1992; Wilson et al., 1993; Rennie et
al., 1997). In contrast, heritabilities of other characteristics
SYMPOSIUM: SKELETAL BIOLOGY AND RELATED PROBLEMS IN POULTRY
were higher (tibia strength, h2 = 0.45; humerus strength,
h2 = 0.30; and keel radiographic density, h2 = 0.39). There
was also a positive correlation between body weight and
bone strength.
A restricted selection index designed to improve bone
characteristics, yet hold body weight constant, was derived from genetic parameters obtained from these preliminary analyses, using standard selection index theory.
Three biologically meaningful and moderately to highly
heritable traits that could be measured in a short period
of time for many birds were included in the index, namely
keel radiographic density (KRD), humerus strength
(HSTR) and tibia strength (TSTR). By including characteristics of wing, leg, and axial skeleton, this index gave a
wide representation of the overall skeleton. The index
was bone index = (0.27 × KRD) + (0.37 × HSTR) + (0.61
× TSTR) − (0.25 × BW). The coefficient for body weight
was increased to 0.35 for selection of the G5 generation
to counter a slight divergence in this trait that started
to appear between the lines. Selection was performed
retrospectively each year with chickens hatched and
raised from all available hens in the experiment. On the
basis of the data collected on the hens at the end of their
laying period, selection decisions were made with entire
full-sib families of chickens being kept or rejected. Selection commenced by assigning birds in generation G3 to
either the high (G3H) or low (G3L) line on the basis of
their dams’ (G2) bone index.
Consequences of Selection
Genetic parameters for the traits in the bone index,
and the bone index itself, showed that all traits were
moderately to highly inherited throughout the study; the
heritability of the bone index was 0.4. The genetic and
phenotypic correlations also show that the three bone
measurements in the index were moderately to strongly
correlated with each other. Finally, the bone measurements were all positively correlated with body weight,
indicating that selection for improved bone strength characteristics alone, without the restriction placed on body
weight, would have resulted in considerably heavier
birds. Different mean values in the bone strength measurements in different years indicated that these traits
were strongly affected by environmental factors, raising
the possibility of genotype by environment interactions.
However, comparison of full-sib flocks reared on different
locations gave little evidence for genotype by environment interactions, within the range of environments investigated.
From Year 3 onward, the lines diverged progressively
for keel radiographic density, humerus strength, tibia
strength, and the bone index in the desired direction.
Bone characteristics in G5 are shown in Table 3. For the
hens, the lines differed by 19% for keel radiographic density, 13% for humerus strength, and 25% for tibia strength.
The differences were highly significant (P < 0.01) from
Year 4 onward, with the exception of humerus strength
in Year 4 in which the difference, although in the desired
direction, was not significant. Although selection was
based on measurements made on hens, selection was
found to also affect bone strength in males as well, with
high index males outperforming low index males for all
traits. The differences between the lines in G5 were tibia
strength 10% (P < 0.01), humerus strength 13% (P < 0.05),
keel radiographic density 15% (P < 0.01) and body weight
7% (P < 0.01). The incidences of humeral fractures in hens
occurring during the production period and depopulation showed a sixfold difference between the lines in G5.
The responses to selection are encouraging insofar as
it appears possible to create sizeable differences in bone
strength characteristics of hens in a relatively short period
of time, using conventional selection techniques. This response can also be made to be independent of body size,
should that be the desire of the breeder, although faster
progress could be made if body weight were to be allowed
to increase. Moreover, the absence of significant or meaningful genotype by environment interactions implies that
TABLE 2. Effect of providing limestone as powder or particles (3 mm diameter)
on bone characteristics in end-of-lay hens1
Limestone type
Trait
Powder
Particles
Probability
Proximal tarsometatarsus
Total bone (%)
Cancellous bone (%)
Medullary bone (%)
23.4
6.6
16.8
28.6
7.3
21.4
<0.001
NS
<0.05
Free thoracic vertebra
Cancellous bone (%)
10.4
10.2
NS
Tibia
Radiographic density (mm Al)
Breaking strength (kg)
1.96
19.5
2.26
23.6
<0.01
<0.05
0.73
11.8
0.78
12.1
NS
NS
0.61
0.68
Humerus
Radiographic density (mm Al)
Breaking strength (kg)
Keel
Radiographic density (mm Al)
1
(Fleming et al., 1998b).
1039
<0.01
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WHITEHEAD AND FLEMING
TABLE 3. Bone characteristics and body weights at the end of the laying period in female and male
chickens after three generations of selection for high (H) or low (L) bone index (G5 generation)1
Females
Males
Line
Trait
Body weight (kg)
Keel radiographic density
(mm Al equivalent)
Tibia strength (kg)
Humerus strength (kg)
Humerus fractures (%)
H
1.67
0.58
30.7
15.4
2.8
Line
L
1.63
0.48
23.9
13.5
18.4
Probability
<0.001
<0.001
<0.001
<0.001
H
2.29
0.77
68.2
50.0
L
2.14
0.67
61.5
44.0
Probability
<0.01
<0.01
<0.01
<0.05
1
(Bishop et al., 2000).
selection progress seen in a breeding flock should also be
expressed under commercial egg production conditions.
Although we mainly studied hens, it is interesting that
the bone characteristics included in the bone index were
also changed in males by selection (Table 3), suggesting
that selection has altered some factors in bone metabolism
common to both sexes. Male chickens do not suffer from
osteoporosis, but this finding raises the possibility that
selection procedures aimed at alleviating osteoporosis in
hens could also be carried out in male birds.
Changes in bone strength per se are unlikely to be of
special interest, however, unless accompanied by changes
in the incidence of bone fractures. The keel and humerus
are two bones frequently observed to be fractured in commercial practice (Gregory and Wilkins, 1989). Although
the cage and handling conditions in the present study
were not intended to resemble the practices on commercial laying farms, selection has clearly resulted in an altered incidence of fractures in these bones. Few fractures
of the tibia, a much stronger bone, were observed in this
study. The responses in bone breakage incidence were
reflected in the genetic correlations with bone strength.
All bone measurements are strongly correlated with the
presence or absence of breakages and the number of sites
of broken bones, indicating that genetically altering bone
strength will indeed alter the incidence of bone fractures.
Can the selection procedure be simplified or improved
to avoid the need for retrospective selection performed
on excess birds? Bone strengths in different parts of the
skeleton appear to be strongly correlated, indicating that
selection to improve the strength of one bone within the
skeleton should increase the strength of the skeleton as
a whole. This finding has important implications in terms
of reducing the number of measurements required to
categorize the strength of the skeleton as a whole; relatively few measurements should be required, making selection for bone strength more feasible. Alternatively, selection could be improved by the use of in vivo predictors
of bone strength at an early stage of the laying period,
so that eggs are fertilized, collected, and hatched only
from selected hens. A predictive in vivo method involving
digitized fluoroscopy of the humerus under experimental
conditions has been described by Fleming et al. (1998c).
Other metabolic comparisons now being carried out on
the lines may identify alternative approaches.
The genetic and phenotypic relationships between bone
strength characteristics and egg production and quality
characteristics are key factors to be identified before selection for improved bone quality can be incorporated into
commercial breeding programs. Preliminary evidence
suggests that there has been a slight deterioration in shell
quality in the high bone index line, and this important
relationship is currently under further investigation.
DISCUSSION
The appearance of osteoporosis in high-performance
hens has been attributed to two factors. First, confining
birds in cages has weakened bones by promoting a form
of disuse osteoporosis. Second, it has been suggested that
a contributing factor has been modern selection procedures that have produced birds of low body weight and
food intake but with a large egg output. The amount of
calcium deposited in shells in the course of the laying
year in these birds is very high in relation to their body
reserves of calcium. However, initial evidence suggests
that high egg productivity within a given period does
not accelerate depletion of structural bone because zero
correlation has been observed at the phenotypic level
between egg output and PTM cancellous bone volume
(Rennie et al., 1997). Shell quality falls in older hens, but
there is no evidence that this is related to poor bone
quality; the proportion of medullary bone may be at its
highest in older birds (Fleming et al., 1998b). It is more
likely that an important factor predisposing modern hens
to osteoporosis is the extended length of the period during
which they are in a continuously reproductive condition.
This increased period of structural bone resorption results
in more severe osteoporosis by the end of the laying
period. Thus, continued selection for persistency of lay
is likely to result in birds that are even more susceptible
to osteoporosis.
What can be done to prevent osteoporosis? Allowing
birds greater opportunity to exercise can help, but there
are problems with this approach. Improvements in bone
strength seem to be related to the degree of exercise in
which the particular bone is involved, but this can lead
to increased risk of trauma, as has been discussed previously. Transferring of birds from battery cages to alternative housing systems does not necessarily decrease
SYMPOSIUM: SKELETAL BIOLOGY AND RELATED PROBLEMS IN POULTRY
fracture incidence in proportion to the improvement in
bone strength and may increase welfare problems from
other causes.
Nutrition has a part to play, first, by avoiding deficiencies that can make the problem worse and, second by
promoting good nutrient supply. Provision of a particulate source of calcium is particularly helpful. It is also
likely that transferring pullets onto a diet of higher calcium content at lighting up rather than at first egg will
help to decrease the loss of structural bone during the
initial period of formation of medullary bone. The practice
of feed withdrawal some days before depopulation is to
be deplored; this practice will accelerate loss of bone mass
at a time of severe risk of bone damage. But these good
nutritional practices will still not prevent osteoporosis.
Genetics may offer a practical solution to osteoporosis.
Bone strength characteristics in end-of-lay hens have been
found to be moderately to strongly inherited and respond
readily to selection. A change in the incidence of bone
fractures has been a correlated response to the selection,
with a lower incidence of fractures occurring in hens
selected for increased bone strength. The implication of
these findings is that selection for enhanced bone strength
can be used as a long-term measure to help alleviate
osteoporosis. However, until a genetic strategy can be
expected to have an impact in commercial layers, it will
be important to optimize the nutritional and husbandry
factors that also influence osteoporosis.
ACKNOWLEDGMENTS
Much of the research described in this paper was supported by the Ministry of Agriculture, Fisheries and Food
and the European Commission.
REFERENCES
Bishop, S. C., R. H. Fleming, H. A. McCormack, D. K. Flock, and
C. C. Whitehead, 2000. The inheritance of bone characteristics
affecting osteoporosis in laying hens. Br. Poult. Sci. 41:33–40.
Bell, D. J., and W. Siller, 1962. Cage layer fatigue in brown
leghorns. Res. Vet. Sci. 3:219–230.
Brown, R. H., 1993. Egg producers concerned about loss of spent
fowl slaughter market. Feedstuffs 65(52):1.
Couch, J. R., 1955. Cage layer fatigue. Feed Age 5:55–57.
Fleming, R. H., C. C. Whitehead, D. Alvey, N. G. Gregory, and
L. J. Wilkins, 1994. Bone structure and breaking strength in
laying hens housed in different husbandry systems. Br. Poult.
Sci. 35:651–662.
Fleming, R. H., H. A. McCormack, L. McTeir, and C. C.
Whitehead, 1998a. Medullary bone and humeral breaking
strength in laying hens. Res. Vet. Sci. 64:63–67.
Fleming, R. H., H. A. McCormack, and C. C. Whitehead, 1998b.
Bone structure and strength at different ages in laying hens
and effects of dietary particulate limestone, vitamin K and
ascorbic acid. Br. Poult. Sci. 39:434–440.
Fleming, R. H., H. A. McCormack, L. McTeir, and C. C.
Whitehead, 1998c. Digitised fluoroscopy (DF) predicts break-
1041
ing strength in osteoporotic avian bone in vivo. Br. Poult. Sci.
39:S49–S51.
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.
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-oflay hens. Br. Poult. Sci. 31:59–69.
Gregory, N. G., L. J. Wilkins, T. G. Knowles, P. Sorensen, and
T. Van Niekerk, 1994. Incidence of bone fractures in European
layers. Pages 126–128 in: Proceedings of the 9th European
Poultry Conference. Vol II. UK Branch of WPSA, Glasgow,
UK.
Hudson, H. A., W. M. Britton, G. N. Rowland, and R. J. Buhr,
1993. Histomorphometric bone properties of sexually immature and mature White Leghorn hens with evaluation of
fluorochrome injection on egg production traits. Poultry Sci.
72:1537–1547.
Hughes, B. O., S. Wilson, M. C. Appleby, and S. F. Smith, 1993.
Comparison of bone volume and strength as measures of
skeletal integrity in caged laying hens with access to perches.
Res. Vet. Sci. 54:202–206.
Khosla, S., E. G. Lufkin, S. F. Hodgson, L. A. Fitzpatrick, and
L. J. Melton, 1994. Epidemiology and clinical features of osteoporosis in young individuals. Bone 15:551–555.
Knowles, T. G., and D. G. Broom, 1990. Limb bone strength and
movement in laying hens from different housing systems.
Vet. Rec. 126:354–356.
Lanyon, L. E., 1992. Functional load-bearing as a controlling
influence for fracture resistance in the skeleton. Pages 61–66
in: Bone Biology and Skeletal Disorders in Poultry. C. C.
Whitehead, ed. Carfax Publishing Co., Abingdon, UK.
Newman, S., and S. Leeson, 1998. Effect of housing birds in
cages or an aviary system on bone characteristics. Poultry
Sci. 77:1492–1496.
Nightingale, T. E., L. H. Littlefield, and L. W. Merkley, 1972.
Osteoporosis induced by unilateral wing immobilization.
Poultry Sci. 51:1844–1845.
Randall, C. J., and S.R.I. Duff, 1988. Avulsion of the patellar
ligament in osteopenic laying fowl. Vet. Rec. 128:397–399.
Rennie, J. S., R. H. Fleming, H. A. McCormack, C. C. McCorquodale, and C. C. Whitehead, 1997. Studies on effects of nutritional factors on bone structure and osteoporosis in laying
hens. Br. Poult. Sci. 38:417–424.
Thorp, B. H., S. Wilson, S. Rennie, and S. E. Solomon, 1993. The
effect of a bisphosphonate on bone volume and eggshell
structure in the hen. Avian Pathol. 22:671–682.
Urist, M. R., and N. M. Deutsch, 1960. Osteoporosis in the laying
hen. Endocrinology 66:377–391.
Van Niekerk, T.G.C.M., and B.F.J. Reuvekamp, 1994. Husbandry
factors and bone strength in laying hens. Pages 133–136 in:
Proceedings of the 9th European Poultry Conference. Vol.
II. UK Branch of WPSA, Glasgow, UK.
Whitehead, C. C., and S. Wilson, 1992. Characteristics of osteopenia in hens. Pages 265–280 in: Bone Biology and Skeletal
Disorders in Poultry. C. C. Whitehead, ed. Carfax Publishing
Co., Abingdon, UK.
Wilson, S., and S.R.I. Duff, 1991. Effects of vitamin or mineral
deficiency on the morphology of medullary bone in laying
hens. Res. Vet. Sci. 50:216–221.
Wilson, S., S.R.I. Duff, and C. C. Whitehead, 1992. Effects of
age, sex and housing on the trabecular bone of laying strain
domestic fowl. Res. Vet. Sci. 53:52–58.
Wilson, S., B. O. Hughes, M. C. Appleby, and S. F. Smith, 1993.
Effects of perches on trabecular bone volume in laying hens.
Res. Vet. Sci. 54:207–211.