The Problem of Broken Bones During the Handling

ABSTRACT The major welfare concern during the
handling of laying hens is that of broken bones. With
particular reference to the United Kingdom, this paper
reviews the work that has been done to quantify the
problem, to examine the causes, and to investigate
factors that affect it. The number of freshly broken bones
found in live birds prior to slaughter and the number of
old healed breaks found at slaughter are unacceptablyhigh. End-of-lay hens from battery cages have especially
fragile bones and these are easily broken during the
rough handling that is received during depopulation.
Birds from more extensive laying systems have stronger

bones and suffer fewer breaks during depopulation but
have a greater prevalence of old healed breaks. The old
breaks occur as a result of collisions due to poor design
within these housing systems. The number of fresh
breaks can be reduced by increasing bone strength and
handling birds with more care. The numbers of old
breaks can be reduced by better design of housing
systems and the physical environment within them.

INTRODUCTION
This paper reviews the main welfare problem that
occurs during the handling of hens within the United
Kingdom—that of broken bones. The handling and
transport of hens has been reviewed by Swarbrick
(1986), Broom and Knowles (1989), and Knowles and
Broom (1990a). This review focuses on the work that has
been carried out since the publication of these articles.
The most recent figures from the Ministry of
Agriculture, Fisheries and Food are for 1993, and these
put the total number of laying hens producing table
eggs within the UK at approximately 33 million birds.
As one laying cycle is approximately 52 wk and most
birds are slaughtered after the first production cycle, this
means that at present (1995) approximately 31.7 million
hens are transported for slaughter each year. However,
there has been a trend for the total number of laying
hens to decrease by approximately 800 thousand birds
per year since 1983, so if this trend continues, the figure
for 1997 will be closer to 30 million birds transported to
slaughter. More than 90% of these birds are kept in
battery cages.
The first survey describing the prevalence of broken
bones in caged hens within the UK found that 29% of
live birds had broken bones by the time they had
reached the water bath stunner, with on average 0.5
broken bones per bird (Gregory and Wilkins, 1989). The
main bones that had been broken were the ischium, keel,
humerus, and pubis, and these accounted for 70% of the
breaks. The authors identified removal from battery
cages and hanging on the slaughter line as the major
causes of the damage. A similar survey with broilers
found that 3% of the live birds had received broken
bones before they had reached the water bath stunner
(Gregory and Wilkins, 1990). As 600 million broilers are
slaughtered annually, this means that approximately 18
million live broilers and 9.5 million hens receive breaks
each year. From the point of view of welfare, such large
numbers of animals with broken bones is entirely
unacceptable. Broom (1986) defines welfare as the state
of an individual as regards its attempts to cope with its
environment. Most people would agree that such
extreme physical damage is indicative of an inability to
cope and shows very poor welfare. The pain associated
with such damage is likely to be great. Although the
numbers of broilers with broken bones is greater, it is
likely that the situation with hens could be improved
more easily as a much greater proportion of hens suffer
from breaks.
THE PREVALENCE OF BROKEN BONES
1798
Received for publication August 12, 1995.
Accepted for publication December 15, 1997.
1To whom correspondence should be addressed: toby.knowles@
bris.ac.uk
IN LIVE BIRDS
It is important to describe how the prevalence of
breaks is estimated, as differing methods will result in a
range of values for the same population. Methods used
have included palpation of the whole carcass, or specific
parts, after it has been hung on the line, the use of meat
FIRST NORTH AMERICAN SYMPOSIUM ON POULTRY WELFARE 1799
TABLE 1. List of the bones examined in the
surveys of Gregory and Wilkins
Femur Scapula
Tibia Coracoid
Fibula Furculum
Humerus Radius
Ribs Ischium
Ulna Ilium
Sternum Pubis
inspectors’ records, and physical dissection of the
carcass with the examination of specific bones. All but
the latter method tend to underestimate the number of
broken bones (Gregory and Wilkins, 1992). All recent
surveys within the UK have been carried out by
Gregory and Wilkins and employed the latter method,
in which birds were first killed in a convulsion-free
manner in order to avoid further breaks. During
dissection, only the bones identified in Table 1 were
examined for fractures, as a full dissection of each
carcass was considered to be too time-consuming for the
number of birds required for the surveys: it has been
estimated that sample sizes of at least 100 birds within a
flock are needed to give an accurate assessment of the
prevalence of breaks (Gregory and Wilkins, 1992).
In the first survey by Gregory and Wilkins (1989), it
was found that 29% of live hens from cages have freshly
broken bones, but also that 5% of caged birds had old
breaks that had healed (Gregory et al., 1990). The most
probable cause of the old breaks was poor handling
during rearing and placement. The range of fresh breaks
in different flocks can be very large, from 0 to 50%
(Gregory and Wilkins, 1989), making it difficult to
accurately determine an overall figure for the UK. But
the wide range in incidence between flocks does indicate
that there must be particular husbandry and handling
practices that lead to broken bones. A better understanding
of these could lead to an improvement in the
situation.
Following publication of the initial figures in 1989, a
joint industry-welfare guide to the handling of spent
hens was produced by the British Poultry Federation
and the National Farmers’ Union. These general guidelines
emphasized the need for preparation and planning,
ensuring that sufficient staff were available and that
they were all aware of the need for careful handling. The
recommendations also included the use of low light
levels, catching the birds by two legs instead of by just
one, and the use of a slide at the entrance of the cage to
prevent birds being knocked against the feeding trough.
More recent surveys have found 14% of caged birds
with fresh breaks but up to 13% with old breaks
(Gregory et al., 1994). This finding may mean that the
situation with respect to new breaks has improved but
an accurate overall determination is difficult.
UNDERLYING PREDISPOSING FACTORS—
OSTEOMALACIA AND OSTEOPOROSIS
It has been known for many years that modern laying
hens can have unusually weak bones (Rowland et al.,
1968; Rowland and Harms, 1970). Previous authors, such
as Riddle (1981), considered osteoporosis to be the sole
cause of bone weakness. In osteoporosis, the bone is
normally mineralized but its total mass is reduced, often
with slender trabeculae and large spaces within the
bone. However, Randall and Duff (1988) reported an
increase in the incidence of bone disease in which flocks
showed a variable response to dietary treatments. They
proposed that the osteopenia (bone loss) they found
could be due to a combination of osteoporosis and
osteomalacia. In osteomalacia, the bone is present but
incompletely mineralized. Birds suffering from osteopenia
due to osteomalacia, or osteoporosis exacerbated by
osteomalacia, respond to dietary treatment, whereas
birds suffering from osteoporosis alone do not respond
to dietary treatment. Generally, bone fragility in end-oflay
hens on a properly balanced diet is due to
osteoporosis, because in modern, high production hens
structural bone is mobilized throughout the laying
period in order to contribute to the formation of
eggshell. However, there are other factors that can affect
the problem.
Lanyon et al. (1986) have shown in laying hen turkeys
that for bone to maintain its normal thickness and
functional structure it must be subject to some level of
dynamic loading or osteoporosis results. They also
demonstrated that the effects of disuse (lack of loading)
and bone loss due to calcium deficiency were additive,
but that bone loading provided a substantial conservative
influence on bone mass even under conditions of
calcium deficiency, in which there was extensive mineral
resorption. Thus, where a bird’s movements are restricted
and it is unable to provide normal dynamic
loading, the effects of the restriction and any dietary
insufficiencies will be additive, but when a bird is free to
move and provide normal loading, the effects of dietary
insufficiencies will be reduced.
Osteomalacia and osteoporosis both cause a weakening
of the bone. Knowles et al. (1993) have shown that
birds with weaker bones are more likely to sustain
broken bones, and that even the differences in bone
strength found within a population of birds kept in the
same type of cage and on the same diet are enough to
influence the likelihood of a bird sustaining a break.
FACTORS AFFECTING BONE STRENGTH
AND THE PREVALENCE
OF BROKEN BONES
Husbandry System
Different husbandry systems allow various degrees of
freedom of movement, and the more restrictive systems
lead to weaker bones and thus to an increased likelihood
of a break during handling (Knowles et al., 1993). Studies
relating freedom of movement and bone strength within
different systems have been carried out by Knowles and
Broom (1990b), Nørgaard-Nielson (1990), Gregory et al.
(1991), Fleming et al. (1994), and van Niekerk and
KNOWLES AND WILKINS 1800
Reuvekamp (1994). Generally, battery cages allow the
least amount of movement and produce birds with the
weakest bones whereas percheries allow the most movement,
promote wing movement, and produce stronger
bones. In one survey, Gregory et al. (1990) found 24% of
birds from battery cages to have freshly broken bones,
prestun, compared with only 10% of birds from perchery
systems. The same paper reports another survey in which
31% of birds from cages had freshly broken bones
compared with 14% of birds from free range systems. As
well as producing weaker bones, there is a greater
likelihood in intensive systems that birds will come into
contact with solid objects during catching. This too would
tend to increase the prevalence of breaks.
The introduction of a perch into a battery cage systems,
and its increased use, have been shown to increase the
strength of the bones in the leg but the effect was only
minor and was thought unlikely to affect the prevalence of
breaks (Hughes and Appleby, 1989; Hughes et al., 1993;
Wilson et al., 1993).
The presence of an old healed break at slaughter could
be thought of as indicative of poorer welfare than a break
that has occurred a few hours prior to slaughter. An old
break will have been felt over a prolonged period of time.
Those found have often mended very poorly, perhaps
resulting in a lifetime of pain. The prevalence of old breaks
has been shown to vary considerably with different types
of housing system. Although the prevalence of new
breaks is lower in perchery and free range systems than in
battery systems, old breaks tend to be more prevalent in
the more extensive systems. Gregory et al. (1990) give
figures of 5, 12, and 25% of birds with healed broken
bones, from battery, free range, and perchery systems,
respectively. Gregory and Wilkins (1991) attributed the
high prevalence of old breaks in the perchery units to
accidents during flight and landing. Within percheries,
the design and layout of the furniture are likely to be
important in determining the number of accidents, as
large differences in the prevalence of old breaks between
types of perchery have been observed (Gregory and
Wilkins, 1992). In order to put the figures for old breaks
into perspective, Gregory and Wilkins (1991) carried out a
survey of captured pigeons. Three per cent of pigeons
thought to have been racing pigeons had old healed
breaks, whereas 6% of feral pigeons were found to have
old breaks. However, a direct comparison cannot be made
because hens, as heavier birds, would be more likely to
sustain a break than pigeons during an accident of similar
severity. Additionally, the number of wild birds with old
breaks will be reduced through selective predation and an
inability to feed.
Light Intensity
The effect of light intensity during lay in battery hens
was investigated by Gregory et al. (1993a). They found that
birds kept at 15 lx had more old, healed breaks than birds
kept at 2 or 0.5 lx. In a trial looking at lighting patterns,
Gregory et al. (1993b) found no effect on the breaking
strength of the tibia or humerus at the end of lay with an
intermittent pattern [3 h light:3 h dark (´4)] compared
with conventional regimens (15 h light:9 h dark) or (17 h
light:7 h dark).
Rearing Method
Anderson and Adams (1994) found no difference
between the tibia breaking strengths of 68-wk-old hens
reared in cages or reared on litter, but Gregory et al. (1991)
found a greater number of broken bones in hens that had
been reared on litter. Most of the difference was due to a
greater damage to the humerus in the litter birds, which
also had weaker humeri. No consistent difference in tibia
breaking strength between the treatments was found.
When birds are caught they predispose themselves to
injury if they make violent attempts at escape. Reed et al.
(1993) reported that enriching the environment of caged
hens with plastic balls and bottles and exposing them to
daily human handling reduces their fear reactions during
catching and that this resulted in fewer potentially
injurious contacts with the cage. They later reported that
hens with lower fear reaction scores tended to sustain less
bruising and fewer breaks (Reed et al., 1994).
Age at Sexual Maturity,
Age at Culling, and Molting
Gregory et al. (1991) retarded sexual maturity to 157 d
in one group of caged layers and at 82 wk of age compared
the prevalence of broken bones with a control group that
had achieved sexual maturity at 147 d. The two groups
were not measurably different, with 19 and 18% of birds,
respectively, suffering broken bones. However, further
studies revealed a positive correlation between age at
sexual maturity and the breaking strength of the tibia and
humerus and also a negative correlation between age at
sexual maturity and the prevalence of freshly broken
bones (Gregory and Wilkins, 1992), although the differences
found in breaking strength were not great. In a small
study involving three groups of approximately 120 hens
slaughtered at 57, 67, and 77 wk, Gregory et al. (1991)
found no change in the prevalence of broken bones with
increasing age. Gregory et al. (1991) found that forced
moulting at 50 wk of age had little effect on bone strength
over the moulting period, but bone strength increased by
7% in the humerus and 17% in the tibia from the end of
molt to the end of lay at 86 wk.
Breed and Strain
Large strain differences in bone strength were found by
Rowland et al. (1972) in the U.S. In the UK, differences in
tibia strength between breeds were found by Knowles et
al. (1993) but the differences were small and were not
measurably associated with the prevalence of new breaks.
Gregory et al. (1991) found no difference in the prevalence
FIRST NORTH AMERICAN SYMPOSIUM ON POULTRY WELFARE 1801
TABLE 2. The diets used in the study by Whitehead (1994)
1. Control – wheat/fish/soybean meal (CP, 170 g/kg; ether
extract, 20 g/kg; Ca, 35 g/kg; P, 6 g/kg)
2. Control diet plus added maize oil at 50 g/kg
3. Control diet with limestone flour replaced by oystershell
4. Control diet with sodium fluoride supplement (200 mg/
kg)
5. Control diet with vitamin C supplement (250 mg/kg)
6. Control diet with 1,25-dihydroxyvitamin D supplement
7. Diet with less CP (150 g/kg) with vitamin K supplement
(20 mg/kg)
8. Diet with less P (4.5 g/kg)
of new breaks among different breeds within the UK.
However, in later work, they included a white breed that
was found to have a stronger tibia but weaker humerus
(Gregory and Wilkins, 1992). White breeds have also been
found to have a greater prevalence of breaks (Gregory et
al., 1994). It is likely that the modern breeds of brown bird
that are now used almost exclusively within the UK have
become more homogenous with continued selection for
production.
Catching Method
It has been shown that the way in which the birds are
handled at catching can have a great effect on the number
of bones that are broken. A researcher working with a
team of professional “pickers” caused fresh breaks in only
14%of the birds that he caught and carried out of a battery
system compared with an average of 24% for the other
“pickers” (Gregory and Wilkins, 1989). The effect that the
method of removal from the cage has on the prevalence of
broken bones has been evaluated in a series of trials
(Alvey et al., 1991; Gregory et al., 1992, 1993a). In general,
pulling birds from the cage by one leg produces more
breaks than pulling birds from the cage by two legs.
Pulling birds out in a group, rather than singly, also tends
to produce more breaks. However, these differences did
not exist in all trials, suggesting that the effect was specific
to particular combinations of flock and picker. Most of the
differences found between treatments were attributable to
a greater number of broken femurs. It was thought that
one cause of broken bones was contact with the sides of
the feed trough as birds were withdrawn from the cage.
However, the inclusion of a slide over the trough did not
affect the number of breaks in any of the trials. Knowles
and Broom (1993) investigated the corticosterone
response of hens to different catching methods. Generally,
levels of plasma corticosterone rise during a traumatic
event. Although not significant, there was some indication
that catching birds individually by both legs produced the
smallest increase in plasma corticosterone levels. Carrying
the inverted birds out of the house by hand, as is normal
commercial practice, produced a greater corticosterone
response than crating birds directly from the cage and
then carrying them from the house in the crate, but there
was no difference in the numbers of broken bones
between the two treatments.
The effect of light intensity during catching was
investigated by Gregory et al. (1993a). Reducing light
levels to 2 lx during catching for birds normally housed at
15 lx improved handling. Increasing light levels to 12 lx for
birds normally housed at 2 lx had no effect on ease of
handling.
Diet
A number of trials have been carried out to investigate
the possibility of remedying bone fragility due to
osteoporosis by dietary means. Whitehead (1994) fed eight
different diets throughout the laying year (Table 2). He
found that none of the diets prevented osteoporosis and
that a high fat diet, with added maize oil, actually
accelerated bone loss. Medullary bone content was
increased by fluoride or ground oyster shell. He concluded
that osteoporosis could not be prevented by
dietary means but that a good diet was necessary for
minimizing its severity.
Orban et al. (1993) studied the effect of feeding different
levels of dietary ascorbic acid (from 0 to 3,000 ppm) for 4
wk on the mineral content, density, and breaking strength
of the femur, tibia, and metatarsus of laying hens. They
found no consistent difference in any of these measurements
between treatments. Koelkebeck et al. (1993) found
some evidence that carbonated water increased the tibia
breaking strength of older laying hens exposed to a shortterm
heat stress.
CONCLUSIONS
The problem of bone breakage during the handling of
end-of-lay hens, particularly those confined in battery
cages, continues to be a major welfare issue. The amount
of trauma incurred by birds at depopulation can be
reduced by two means. Firstly, an improvement in bone
strength might enable the birds to better withstand the
insults inflicted during depopulation. However, with
caged birds, only small, inconsistent improvements have
been demonstrated by modifications to husbandry
practices such as lighting, cage design, and rearing
method. The second and more direct method is to
reduce the number of insults incurred. Careful catching
has been shown to greatly reduce the number of bones
broken. The ease with which birds can be removed from
different designs of cage is also likely to have some
effect. The number of birds having breaks that occurred
both before and during lay and that have subsequently
healed is also a major welfare issue. But this condition is
most prevalent in the more extensive husbandry systems,
which allow more freedom of movement and
promote bone strength, and also produce the least
number of broken bones at depopulation. The indications
are that a better knowledge of how these injuries
occur could lead to better design and placement of the
furniture and fittings within these systems and a
reduction in the number of old breaks found at
slaughter.
An important point to be emphasized is that any
measures intended to reduce the numbers of either old
KNOWLES AND WILKINS 1802
or new breaks can only be validated by subjecting a
large number of individual carcasses to a full dissection,
a costly and time-consuming process.
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