Welfare, health, and hygiene of laying hens housed in furnished cages and in alternative housing systems.

Abstract

The aim of this review was to compare welfare, health, and hygienic status of laying hens housed in furnished cages and in alternative systems. In alternative systems (floor housing and aviaries), birds have more freedom of movement and a more complex environment than in furnished cages. However, housing birds in much larger flocks in alternative systems leads to an increased risk of feather-pecking. Furthermore, air quality can be poorer in alternative systems than in furnished cages. This can affect health and hygienic status. There are only limited data on a direct comparison between furnished cages and alternative systems. Therefore, there is a need for an on-farm comparison of welfare, health, and hygienic status in these systems.

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Welfare, Health, and Hygiene of Laying
Hens Housed in Furnished Cages
and in Alternative Housing Systems
T. Bas Rodenburg, Frank A.M. Tuyttens, and Bart Sonck
Agricultural Research Centre
Merelbeke, Belgium
Koen De Reu and Lieve Herman
Agricultural Research Centre
Melle, Belgium
Johan Zoons
Provincial Centre for Applied Poultry Research
Geel, Belgium
The aim of this review was to compare welfare, health, and hygienic status of laying
hens housed in furnished cages and in alternative systems. In alternative systems
(floorhousingandaviaries),birdshavemorefreedomofmovementandamorecom-
plex environment than in furnished cages. However, housing birds in much larger
flocks in alternative systems leads to an increased risk of feather-pecking. Further-
more,airqualitycanbepoorerinalternativesystemsthaninfurnishedcages.Thiscan
affect health and hygienic status. There are only limited data on a direct comparison
between furnished cages and alternative systems. Therefore, there is a need for an
on-farm comparison of welfare, health, and hygienic status in these systems.
Conventional cage housing for laying hens will be prohibited from 2012 in the
European Union (EU), following EU directive 1999/74. From 2012 on, only fur-
JOURNAL OF APPLIED ANIMAL WELFARE SCIENCE, 8(3), 211–226
Copyright © 2005, Lawrence Erlbaum Associates, Inc.
CorrespondenceshouldbesenttoT.BasRodenburg,DepartmentofMechanisation,Labour,Build-
ings, Animal Welfare and Environmental Protection, Agricultural Research Centre, Burg. Van
Gansberghelaan 115, 9820 Merelbeke, Belgium. Email: dvl@clo.fgov.be

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nished cages and alternative systems (floor housing and aviaries) will be al-
lowed. With the ban on conventional cages coming closer, a strong effort has
been put into the further development of furnished cages and alternative sys-
tems. In some countries, such as Germany and The Netherlands, the poultry in-
dustry is moving toward alternative systems. Germany even is considering ban-
ning all cage systems, including furnished cages. In The Netherlands, furnished
cages are allowed, but economic and societal forces make the construction of al-
ternative systems more attractive for the poultry industry. In other countries,
such as the United Kingdom and Sweden, furnished cages are used as well as al-
ternative systems. In Belgium, the poultry industry is moving toward furnished
cages, although a definite decision has yet to be made.
In furnished cages, hens have more space than in conventional cages (750
cm2vs. 550 cm2per bird). In addition, they have access to a nest; a perch; and an
area with some litter for pecking, scratching, and dust-bathing. Depending on
the system, birds are kept in relatively small groups, ranging from 5 to 100
birds. Alternative systems can be aviaries or floor housing systems. In both
types of system, birds are kept in large groups with a minimal space allowance
of 1,111 cm2per bird. Birds have access to nests, perches, and a large pecking
and scratching area with litter. In aviary systems, birds also have access to dif-
ferent tiers. The major differences between furnished cages and alternative sys-
tems—with regard to welfare—are related to group size, freedom of movement,
and complexity of the environment (see Table 1). In alternative systems, group
size and freedom of movement are larger than in furnished cages, and the envi-
ronment is more complex. These differences between the systems may affect
welfare, health, and hygiene. The aim of this study was to compare welfare,
health, and hygienic status of laying hens housed in furnished cages and alterna-
tive housing systems.
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RODENBURG ET AL.
TABLE 1
Major Differences in Design Between Furnished Cages and Alternative Systems
Furnished Cages Alternative Systems
Group size
Freedom of movement
Space allowance per bird
Space allowance per group
Complexity of the environment
Litter
Perches
Access to different tiers
Small
Limited
750 cm2
Small
Medium
Limited amount
Low
No
Large
Yes
1,111 cm2
Large
Complex
Large amount
High
Yes (aviaries)
No (floor housing)

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GROUP SIZE
Group size has a major impact on the social behavior and organization of laying
hens. Douglis (1948) found that laying hens could recognize and react to 27
conspecifics. Guhl (1958) reported a dominance hierarchy in a flock of 96 birds.
In much larger groups, birds do not recognize each other individually. This does
not lead, however, to a high incidence of aggression in large groups (Hughes,
Carmichael, Walker, & Grigor, 1997). There is evidence that birds in large
groups (> 100 birds) use other signals, such as body size and comb size, to es-
tablish dominance relationships—the larger bird with the bigger comb being the
more dominant (D’Eath & Keeling, 2003; Pagel & Dawkins, 1997). In small (0
to 20 birds) and large (> 100 birds) groups of laying hens, aggression does not
appear to be a problem. Intermediate group sizes of about 30 birds may consti-
tute social problems that can affect production (Keeling, Estevez, Newberry, &
Correia, 2003). Keeling et al. (2003) compared groups of 15, 30, and 60
floor-housed birds and found that groups of 15 or 60 birds had a better perfor-
mance than groups of 30 birds. Therefore, it may be advisable to avoid group
sizes of about 30 birds.
Group size also affects the risk of feather-pecking, the pecking at, and pulling
out of, feathers of conspecifics. It is a form of redirected pecking behavior, devel-
oping either from food pecking (Wennrich, 1974), ground pecking (Blokhuis,
1986), or pecking during dust-bathing (Vestergaard & Lisborg, 1993).
There are different forms of feather-pecking—gentle and severe feather peck-
ing (Savory, 1995). Mainly, severe feather-pecking will lead to feather damage
and result in denuded areas. Pecking in these denuded areas can lead to wounding
of the victim and to the development of cannibalism (Savory, 1995).
Aseparateformofcannibalismisvent-pecking.Pecksattheventcanleadtose-
rious wounding and death of the victim (Savory, 1995). More feather-pecking is
observedinlargegroupsthaninsmallgroups(Bilcík&Keeling,2000;Nicoletal.,
1999). Nicol et al. (1999) compared groups of 72, 168, 264, and 368 birds in
percheries and found the most feather-pecking in the largest groups. Bilcík and
Keeling (2000) found similar results with groups of 15, 30, 60, and 120 birds in
floor pens. There is evidence that birds can learn feather-pecking behavior from
otherbirds(Zeltner,Klein,&Huber-Eicher,2000),althoughMcAdieandKeeling
(2002) found evidence only for transmission of gentle feather-pecking and not for
transmission of severe feather-pecking.
However, even if severe feather-pecking does not spread from feather-peckers
tononfeather-peckers,afeather-peckerinalargegroupofbirdscandomuchmore
damage than a feather-pecker in a cage with a small group. Furthermore, it is very
difficult to identify feather-peckers in large groups of laying hens; once an out-
breakoffeather-peckingorcannibalismtakesplaceinanalternativesystem,itwill
be very hard to stop. An advantage of alternative systems with respect to
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feather-pecking is that the birds have more opportunities to hide (perches, tiers)
and space to escape, than they do in furnished cages, which can let them avoid
feather-peckers. Furthermore, the genetic background of the birds used affects the
risk of feather-pecking (Bessei, 1984; Kjaer & Sørensen, 1997; Rodenburg et al.,
2003). Alternative systems often use hybrids who are more docile and who have a
lower propensity to develop feather-pecking than the traditional hybrids used in
conventional cages.
In cages, feather-pecking and cannibalism also can cause problems, and abra-
sion can damage the feathers (Hughes, 1980). A. A. Taylor and Hurnik (1994)
compared the feather condition of 3-year-old birds in conventional cages with
birds in an aviary system and found that caged hens had poorer feather cover than
did hens in the aviary system. At the Provincial Centre for Applied Poultry Re-
search in Gheel, Belgium, feather conditions of laying hens in furnished cages and
in an aviary system were compared in two subsequent experiments. In the first ex-
periment, feather condition was much better in the aviary system than in the fur-
nished cages. In the second experiment, however, there were no major differences
in feather condition between the two systems (Zoons, personal communication).
In a survey among farmers, Pötzsch, Lewis, Nicol, and Green (2001) studied the
risk factors for vent-pecking in alternative systems. They identified the following
risk factors: dim light around the nestboxes (to encourage nest use), diet changes,
useofhangingbelldrinkers,andearlyonsetoflay.Thefirstthreefactorsalsowere
shown to increase the risk of feather- pecking.
These results indicate that changes in housing and management can help mini-
mize the risk of feather-pecking and cannibalism in alternative systems. Rearing
also plays an important role. Huber-Eicher and Sebö (2001) showed that chicks
who had access to litter from 1 day of age spent more time foraging and less time
feather-peckingat5andat14weeksofagethandidchickswhohadaccesstolitter
from 2 weeks of age. Nicol et al. (2001) found similar results. They showed that
early experience with litter reduced the chance of feather-pecking in later life and
stimulated ground-pecking and dust-bathing.
Group size also can affect fearfulness in laying hens. Bilcík, Keeling, and
Newberry (1998) showed that birds from groups of 120 had longer, tonic, immo-
bility responses than did birds from groups of 15, indicating that the former birds
were more fearful. Feather-pecking has been associated with fearfulness (Hughes
& Duncan, 1972), groups with feather damage being more fearful than groups
without feather damage. Furthermore, Rodenburg et al. (2004) found that birds
who are fearful at a young age have a stronger propensity to develop high levels of
pecking as adults. Hansen, Braastad, Storbråten, and Tofastrud (1993) compared
fear in laying hens in conventional cages and those in aviary systems. They found
that there was no difference between systems at 30 weeks of age. At 70 weeks of
age,however,birdsincagesweremorefearfulthanwerebirdsinaviaries.Theau-
thors concluded that fearfulness of birds in cages increased considerably over
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time,whereasthelowerfearfulnessofbirdsinaviariessuggeststhatfreedomfrom
fear is more secured in this system.
The spatial distribution of birds over the system can be affected by group size.
Channing, Hughes, and Walker (2001) compared group sizes between 323 and
912birdsandfoundalargevariationindensityofbirdswithinspecificareasofthe
pen, varying from 9 to 41 birds/m2. This variation was greatest in the larger group
sizes. Extremely high stocking densities in specific areas of the pen can result in
birds’ suffocating when other birds pile on top of them (Channing et al., 2001).
FREEDOM OF MOVEMENT
Birds in alternative systems have more space than do birds in furnished cages.
Especially for comfort behaviors such as wing flapping, stretching, body shak-
ing, and tail wagging, a relatively large amount of space is required. Albentosa
and Cooper (2004) compared furnished cages with 762 cm2per bird (eight
birds/cage) with cages with 3,048 cm2per bird (two birds/cage) at two different
cage heights (38 cm and 45 cm). Birds showed more wing and leg stretches and
more tail wags in two-bird cages than in eight-bird cages, but levels of comfort
behavior were low in all groups. No effect of cage height was found. Appleby et
al. (2002) found similar results: Comfort behavior, although infrequent in both
furnished and conventional cages, was less frequent in conventional cages.
Appleby (2004) studied the spatial requirements of laying hens and concluded
that birds in large groups have more freedom of movement. He also calculated the
minimum space requirements in furnished cages: eight hundred square centime-
ters per bird for groups of eight or more, 850 cm2per bird for groups of four to
seven, and 900 cm2per bird for groups of three or fewer. In this analysis, that lay-
ing hens synchronize certain behaviors—nesting, perching—was taken into ac-
count. According to this study, the space allowance of 750 cm2in the current EU
regulations may provide the birds with too little space to display all behavior for
which they are motivated, particularly when group sizes are small (Appleby,
2004).
The greater freedom of movement in alternative systems allows the birds to
walk, run, and fly. Such exercise also provides the birds with stronger bones than
those of birds who are housed in conventional cages (Nørgaard-Nielsen, 1990).
Olsson and Keeling (2000) showed that laying hens are highly motivated to perch
and, if offered a choice, choose a high perch (63 cm) over a low perch (23 cm). In
addition,cageheightcanaffectperchuse.Struelensetal.(2004)usedpercheswith
seven different heights in cages measuring 45 cm, 50 cm, 55 cm, and 150 cm in
heightandfoundthatthebirdspreferredhighperchesbutthattheywerelimitedby
cage height (distance from perch to roof). A negative side of high perches in alter-
nativesystemsisthatbirdsmayinjurethemselvesandevenbreakboneswhenthey
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miss the perch. Research shows that the following affect the risk of inaccurate
landings:
1. Direction of the jump (with jumping downward being more risky).
2. Material of the perch (with PVC or metal being more risky than wood).
3. Light intensity in the house.
4. Color of the perch (Moinard et al., 2004; Scott, Hughes, Lambe, &
Waddington, 1999; Scott & MacAngus, 2004; Taylor, Scott, & Rose,
2003).
Furthermore, rearing plays an important role. Gunnarsson, Yugvesson, Keeling,
and Forkman (2000) showed that rearing without early access to perches impairs
the spatial skills of laying hens.
Traditional housing systems for laying hens frequently have used square
wooden perches. In modern systems, round metal perches are used. Lambe and
Scott(1998)compareddifferentperchmaterialsanddesignsandfoundnoparticu-
lar preferences. They found that wooden perches are difficult to clean and provide
attractive hiding places for red mites (Dermanyssus gallina). An infestation with
red mites can lead to reduced weight gain, anemia, and even increased mortality
(Kilpinen et al., 2005). Tauson and Abrahamsson (1996) compared wooden and
plasticperchesandfoundthatplasticperchesledtoahigherincidenceoflegprob-
lems (bumble foot) than did wooden perches—even when the perch was fitted
with a soft rubber cover.
COMPLEXITY OF THE ENVIRONMENT
To fulfill their behavioral requirements, laying hens need a complex environ-
ment with opportunities for feeding and drinking, pecking and scratching, nest-
ing, perching, hiding, and performing comfort behavior. Alternative systems of-
fer a more complex environment than do furnished cages (Cooper, Albentosa, &
Redgate, 2004; Olsson, Duncan, Keeling, & Widowski, 2002; Olsson &
Keeling, 2000; Olsson, Keeling, & Duncan, 2002). As a group, the birds in an
alternative system have a large floor space available and free access to perches
and litter. In alternative systems, litter covers one third of the floor space. This
allows the birds to display pecking, scratching, and dust-bathing behavior. In
furnished cages, the total floor space available to a group of birds is limited.
Birds cannot move over long distances or between different tiers.
In furnished cages, a limited amount of litter is supplied in the pecking and
scratching area, resulting in reduced opportunities for foraging and dust-bathing
behavior compared with alternative systems. Cooper et al. (2004) reported higher
levelsofshamdust-bathingthanofactualdust-bathinginfurnishedcages,indicat-
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ing that birds had too little space for dust-bathing in litter. Lindberg and Nicol
(1997) discussed whether pecking at the feed in the feed trough during sham
dust-bathing in a cage environment could provide a substitute for access to litter.
In their study, birds showed dust-bathing in the dustbox, in the nestbox, and by the
feed trough. It is possible that hens start dust-bathing in other parts of the cage be-
causetheyseeanotherhendust-bathinginthedustbox(socialfacilitation).Olsson,
Keeling, and Duncan (2002), however, found no evidence that this is the case.
Theyfoundsomeevidencethatearlyexperiencemayplayarole:Ifchicksarepre-
vented from dust-bathing and develop sham dust-bathing, they may persist in this
behavior even though litter is available. Furthermore, Olsson, Duncan, et al.
(2002) showed that sham dust-bathing does not fulfill a hen’s motivation to
dust-bathe,asbirdswhohadbeenshamdust-bathingpreviouslywereasmotivated
to dust-bathe in litter as birds who had not been sham dust-bathing. Nestboxes are
available both in furnished cages and in alternative systems.
Struelens et al. (2005) studied laying hen preferences for nesting material in
furnished cages. They found that, for egg-laying, the birds preferred peat or artifi-
cial turf over a coated, wire-mesh floor. The absence of nesting material also will
increase the chance that hens lay their eggs in the litter area or in the main cage. In
alternative systems, there sometimes are problems with the distribution of the
birds over the available nests, especially at the beginning of the laying period.
Nests at the front and in the back of the house are crowded, and nests in the middle
are empty. This can lead to increased mortality when the birds pile up on top of
each other. Practical solutions include vertical panels on the perches in front of the
nests, removing the nesting material of the first nestboxes in a row, or closing the
first nestboxes altogether. Modifying the nest color may be another solution.
Huber-Eicher (2004) showed that hens prefer a yellow nest to other nest colors.
This preference seems related to color preferences in early life, as birds who
showedapreferenceforyellowatanearlyagewereindifferenttoallnestcolorsas
hens, whereas all other birds preferred yellow nests during the laying period.
Compared with conventional cages, furnished cages offer a more complex en-
vironment. Appleby, Smith, and Hughes (1993) showed that pre-laying behavior
and dust-bathing behavior were more settled in furnished cages than in conven-
tional cages and that the perches were used intensively. Abrahamsson, Tauson,
and Appleby (1996) also concluded that the facilities provided in furnished
cages—if properly constructed and managed—were used extensively.
HYGIENE
Hygiene is relevant not only for health and welfare but also for food safety. The
large amount of litter and the high level of bird movement in alternative systems
are considered potential risk factors: They result in higher levels of bacteria and
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fungi in the air and in higher dust levels compared with conventional and fur-
nished cages. Furnished cages do not seem to lead to higher levels of bacterial
contamination than do conventional cages. De Reu, Grijspeerdt, Heyndrickx,
Zoons, et al. (2005) compared the bacterial eggshell contamination of eggs laid
in conventional cages with eggs laid in the nestboxes of furnished cages. They
found a comparable contamination with total aerobic mesophilic bacteria for ei-
ther cage system (4.0 to 4.5 log CFU/eggshell). For Gram-negative bacteria, this
also was the case (ca. 3.0 log CFU/eggshell). Similarly, Cepero, Yanguela,
Lidon, and Hernandis (2000) and Ceparo, Maria, and Hernandez (2001) found
no differences in counts of aerobic mesophilic bacteria but reported a higher
prevalence of coliforms on shells of eggs laid in furnished cages. Mallet,
Guesdon, and Nys (2004) studied the hygienic aspects of eggs laid at different
locations in furnished cages compared with eggs laid in conventional cages.
Overall, a small but statistically significant difference was observed between
eggs from furnished cages (4.8 log CFU/eggshell) and eggs from conventional
cages (4.56 log CFU/eggshell). This was due to the eggs being laid outside the
nest in the litter area (4.96 log CFU/eggshell) or in the cage (4.94 log CFU/egg-
shell). The bacterial load on eggs laid in the nests of the furnished cages (4.51
log CFU/eggshell) was similar to the load found in conventional cages (4.56 log
CFU/eggshell). The microbial load recorded by Cepero et al. (2001); Mallet et
al. (2004); and De Reu, Grijspeerdt, Heyndrickx, Zoons, et al. (2005) in fur-
nished cages remained below 5 log CFU/eggshell and sometimes below 4.5 log
CFU/eggshell, limits that could be considered to refer to eggshells with an ac-
ceptable hygienic quality.
A higher contamination of eggshells with total aerobic mesophilic bacteria in
alternative systems was found compared with conventional and furnished cages
(Protais et al., 2003b; De Reu, Grijspeerdt, Heyndrickx, Zoons, et al., 2005). The
increase was more than 1 log unit (up to 5.1 to 6.0 log CFU/eggshell), with much
highercountsonthoseeggslaidonthefloor(upto7logCFU/eggshell).Therewas
a poor relationship between visual soiling of eggs and shell bacterial load (ignor-
ing ground eggs). For Gram-negative bacteria, no significant differences were
foundamongthethreehousingsystems(DeReu,Grijspeerdt,Heyndrickx,Zoons,
et al., 2005).
DeReu,Grijspeerdt,Heyndrickx,Uttendaele,andHerman(2005)analyzedthe
criticalcontrolpointsindifferenteggproductionchainsofconsumptioneggsandre-
portedthatthemostcriticalpointforcontaminationofeggsinanorganicaviarysys-
tem was the initial contamination at the nestboxes. This was not the case in cage
systems,indicatingthatcontaminationinalternativesystemsmorefrequentlytakes
place immediately after laying and, in cage systems, possibly during processing.
It remains unknown whether the differences in bacterial numbers among eggs
produced in different housing systems have an impact on the quality of eggs and
egg products. Only Petrak, Petrak, Jelic, Nedjeli, and Hraste (1999) found a direct
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relationship between initial eggshell contamination and what later is found in egg
products. Harry (1963); Smeltzer, Orange, Peel, and Runge (1979); and De Reu et
al. (in press) reported a correlation between bacterial eggshell contamination and
egginfection.InthestudiesbyCeperoetal.(2001;Ceperoetal.,2000),thehigher
prevalenceofcoliformsontheshellsofeggslaidinfurnishedcageswasnotcorre-
lated with signs of coliform contamination in egg yolk or albumen.
The total count of aerobic mesophilic bacteria in the air of the poultry house
was correlated with the bacterial eggshell contamination at the henhouse (De Reu,
Grijspeerdt, Heyndrickx, Uyttendaele, & Herman, 2005; De Reu et al., in press;
Protais et al., 2003a, 2003c). Averages of 4 log CFU/m3air for the conventional
and furnished cages were found, compared with a 2 log units higher average (> 6
log CFU/m3) in the aviary housing. Zoons (personal communication) reported a
contamination of dust five times higher in aviaries than in furnished cages (10.1
mg/m3vs.2.1mg/m3).Ellen,Bottcher,vonWachenfelt,andTakai(2000)reported
that dust levels are four to five times higher in alternative systems than in conven-
tionalcages.MichelandHuonnic(2004)reportedaconcentrationofdust15times
higher in aviaries than in conventional cages (a maximum of 31.6 mg/m3vs. 2.3
mg/m3). Larsson, Larsson, Malmberg, Martensson, and Palmberg (1999) found 2
mg/m3dust in conventional cages and 4 mg/m3in alternative systems (aviaries).
They also found a tendency for a stronger inflammatory reaction and increased
bronchialresponsivenessinhumanswhoworkedinalternativesystems,compared
with humans who worked in conventional cages.
Only a small part of the airborne particles are bacteria, but bacteria can nega-
tively affect animal health (Pedersen et al., 2000) and the health of the farm work-
ers (Larsson et al., 1999). In addition, it can lead to higher levels of eggshell
contamination(DeReu,Grijspeerdt,Heyndrickx,Zoons,etal.,2005).Todate,lit-
tle is known about the effect of housing system on Salmonella contamination of
eggsandeggproductsorabouttherelationshipwithhumansalmonellosis.Astudy
of the U.K. Food Standards Agency did not find significant differences in Salmo-
nella spp. contamination on the eggshell due to the housing system (Food Stan-
dards Agency, 2004).
AMMONIA
Highlevelsofammoniaintheairalsocancauseproblems.Emissionratesofammo-
niaarehigherforalternativesystemsthanforcages,withaviarysystemsmanaging
lower ammonia rates than floor housing systems (Groot Koerkamp et al., 1998).
Kristensen,Burgess,Demmers,andWathes(2000)showedthatlayinghens,when
givenachoice,preferfreshairoverairwith25partspermillionor45partspermil-
lion ammonia, indicating that the birds can detect ammonia in the air and show an
aversion.Highlevelsofammoniainthehousewellmayleadtowelfareandhealth
problems, both for the animals and for the caretakers. Von Essen and Donham
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(1999)statedthathighendotoxin,ammonia,anddustlevelscontributetoacuteand
chronic respiratory symptoms in farm workers. Wathes, Jones, Kristensen, and
McKeegan(2004)reportedthatchronicexposuretoammoniaincreasessusceptibil-
itytorespiratorypathogensinpoultry;mayleadtoimpairedperformance;and—af-
ter exposure to high levels—to eye problems.
HEALTH IN RELATION TO HOUSING SYSTEM
The effect of housing system on health parameters has been investigated in a
number of studies. Abrahamsson et al. (1996) compared health of birds in con-
ventional and furnished cages. They found some differences in foot health be-
tween the systems and more keel bone lesions in the furnished cages. The high-
est mortality was registered in the get-away cage, a type of furnished cage.
Furthermore, it has been found that birds from furnished cages had stronger
bones at slaughter, compared with birds from conventional cages. Abrahamsson,
Fossum,andTauson(1998)studiedmortalityandhealthinanaviarysystem.Mor-
tality varied between pens and between batches and generally ranged between 3%
and 8% per laying period. In some pens and batches, mortality was much higher
(16%to21%).Themajorcausesofmortalityweresalpingitis(inflammationofthe
oviducts) and cannibalism. In some batches, coccidiosis, lymphoid leucosis (big
liverdisease),andredmiteinfestationscausedproblems.Otherabnormalitiesfound
werekeelbonedeviationsandfootabscesses,bothincreasingwithage.Micheland
Huonnic(2004)comparedthehealthoflayinghensinconventionalcagesandaviary
systemsandfoundthatmortalitywashigherinaviariesbutremainedwithinaccept-
able limits (up to 5%) and that the rate of injurious pecking was low.
Mortality in the aviary systems mainly was due to problems with adapting to
environment (smothering). Feather quality was better in aviaries than in cages,
probablybecauseofabrasion.Theincidenceofinjurieswashigherinaviariesthan
incages.Birdsinaviarieshadstrongerbones,withthestrongestbonesfoundinthe
birds who were raised in a system with perches (Michel & Huonnic, 2004). As
mentioned previously, access to perches also can lead to broken bones. Gregory,
Wilkins, Eleperuma, and Balantyne (1990) studied new and old bone fractures in
laying hens from various housing systems after depopulation. They found 31%
newbreaks(duetodepopulation)inbatteryhens,whereasonly5%ofthebirdshad
old breaks (due to the housing system). In hens from a perchery, 10% had new
breaks; 25% had old breaks.
ON-FARM WELFARE ASSESSMENT
Amethodtoassesswelfareonfarmswouldallowacomparisonbetweenfarmsand
housingsystems.Inrecentyears,anumberofdifferentwelfareassessmentmethods
havebeendevelopedandevaluated.On-farmwelfareassessmentmethodsarebased
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onarangeofwelfareparameters,whichcanbedividedintotwocategories:(a)envi-
ronment-based or (b) animal-based parameters (Johnsen, Johannesson, & Sandoe,
2001). Environment-based parameters are related to the system, the management,
and the stockmanship of the farmer, whereas animal-based parameters record the
“response” of the animals to that particular system.
Some environment-based parameters, such as space allowance or litter quality,
are relatively easy to assess and have a good repeatability. Animal-based parame-
ters,suchaslevelsofstresshormones,abnormalbehavior,ordisease,aremoredi-
rect measures of welfare; however, the recording and interpretation of
animal-based parameters can be time-consuming and difficult (Johnsen et al.,
2001). For laying hens, a limited number of welfare assessment methods is avail-
able. The main method based on environment-based parameters is the animal
needs index or TGI (Bartussek, 2001; Striezel, Anderson, & Horning, 1994). This
method includes one animal-based parameter, namely, general feather condition
of the birds.
Mollenhorst, Rodenburg, Bokkers, Koene, and deBoer (2005) compared the
animal needs index with two animal-based methods: (a) individual feather condi-
tion scoring and (b) behavioral observations of abnormal behavior and time bud-
gets. They conducted all measurements on 10 farms with conventional cages and
on 10 farms with deep litter systems and found positive correlations between the
animal needs index, a high score indicating good welfare, and high levels of loco-
motion and comfort behavior. Furthermore, they found a negative correlation be-
tween the animal needs index and the amount of feather damage to the wings. The
results of their study showed that the animal needs index was sensitive enough to
show differences between different types of housing systems but not differences
within the same housing system. Deep litter systems had a higher score, indicating
better welfare, than did conventional cages (Mollenhorst et al., 2005).
Oden,Keeling,andAlgers(2002)evaluatedtwotypesofalternativesystemsin
Sweden. They used the distribution of the birds in the system and the frequency of
aggression as indicators of differences in access to resources in the different sys-
tems. They found that access to litter and nestboxes was insufficient in both sys-
tems using stocking densities between 10 birds/m2and 19 birds/m2. Other
indicators in this study included feather-pecking behavior, dust-bathing activity,
and fear reaction (Oden et al., 2002). It would be a valuable tool to be able to com-
bine such different welfare indicators to an overall welfare score. However, to
combinetheseseparateindicatorsintoanoverallwelfareassessment,theirrelative
weights have to be compared.
AgrotechnologyandFoodInnovationsB.V.(2004)developedawelfareassess-
mentmethodforlayinghenstoevaluatesystemsandgivethemascorefrom0to10.
Toassignweightingfactors,theyevaluatedscientificliteratureonhousing,manage-
ment, and welfare of laying hens—based on the procedure described by Bracke
(2001)—andcreatedamodelcontainingthisinformation.Theyvalidatedthismodel
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bycomparingthescoresproducedbythemodel(basedonscientificliterature)with
scores given by experts on poultry behavior and welfare and found a substantial
agreementbetweenthetwo.Intheirstudy,furnishedcagesandalternativesystems
scored, respectively, 2.3 and 5.8 out of 10 points using the model and 4.2 and 7.5
pointsusingtheexpertopinions(Agrotechnology&FoodInnovationsB.V.,2004).
CONCLUSIONS
The aim of this review was to compare the welfare, health, and hygienic status
of laying hens housed in furnished cages and in alternative housing systems. In
alternative systems, birds have more possibilities to display various behaviors,
resulting in stronger bones and higher levels of foraging, dust-bathing, and other
comfort behaviors, than in furnished cages. Conversely, the large group size
leads to an increased risk of feather-pecking, although some studies also have
found a poorer plumage cover in furnished cages than in alternative systems. Air
quality is poorer in alternative systems than in furnished cages: High levels of
dust, bacteria, fungi, and ammonia can be detected. This can affect health and
hygienic status. Data on a direct comparison between furnished cages and alter-
native systems are limited; therefore, an on-farm comparison of welfare, health,
and hygienic status in these systems is needed.
ACKNOWLEDGMENT
This project was funded by the Department of Health, Food Chain Safety, and
Environment of the Federal Government of Belgium.
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