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To cite this article: H. Van Den Brand Dr. , H.K. Parmentier & B. Kemp (2004) Effects of housing system (outdoor vs cages)
and age of laying hens on egg characteristics, British Poultry Science, 45:6, 745-752
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British Poultry Science Volume 45, Number 6 (December 2004), pp. 745–752
Abstract 1. Effects of two housing systems (cages vs outdoor) on external and internal egg
characteristics were investigated.
2. In total 785 eggs from three different lines in cages and 268 eggs from outdoor-housed layers were
examined for egg weight, albumen, yolk and shell content, albumen height and pH, and albumen and
yolk dry matter content.
3. Interactions between layer age and housing systems were found for egg weight, eggshell content,
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albumen height, albumen pH, and dry matter content of the albumen and yolk. This was mainly due to
the greater variation with age in the outdoor layers, compared to the caged layers.
4. Irrespective of age eggs from outdoor layers were relatively broader than eggs from the caged layers.
Yolk colour was considerably darker in the outdoor group (11.0 vs 9.3).
5. We concluded that it is more difficult to maintain constant external and internal egg quality in an
outdoor housing system than in a battery cage system. Factors that determine the greater fluctuations
in internal egg quality need to be investigated.
In the European Union, battery cages for laying Animals and housing
hens will be prohibited from 2012, meaning
Eggs from laying hens, originating from ISA
that alternative housing systems, including
Warren medium heavy layers, divergently
free range or outdoor systems, are being
developed. The consequences of alternative selected for antibody response against sheep
housing systems (especially outdoor systems) red blood cells (SRBC), were used in both
for egg quality are currently unclear. Some housing systems. One-third of the hens
studies have described the effects of different had been selected for a high immune response
housing systems on egg quality (Torges et al., against SRBC (H line) for 22 generations, one-
1976; Pavlovski et al., 1981), but there has third for a low immune response against
been little research on egg quality of current SRBC (L line) and the remainder were a
breeds in outdoor systems (Leyendecker et al., random-bred control line (C line). More details
2001a,b). regarding the background of the selection lines
As outdoor systems become more impor- are described elsewhere (Van den Brand et al.,
tant, their effects on egg characteristics (exter- 2004).
nal and internal) need to be clear. Another From hatching until 11 weeks of age, all
factor influencing egg quality is layer age birds were housed in two-deck breeder cages.
(Lapão et al., 1999; Silversides and Scott, Sexes were kept separately. At 11 weeks of
2001) and changes in egg quality with advan- age, chickens of the three lines were ran-
cing age may be dependent on environmental domly assigned to one of two housing systems:
circumstances, such as housing conditions. (1) One hundred and fifty hens (50 of each
The aim of the current study was to describe line) were housed individually in battery
the effects of housing systems (cages vs outdoor cages (BC) of 20 cm 40 cm 40 cm. Hens of
system) and layer age on external and internal the three lines were randomly divided among
egg characteristics. cages. The light schedule was 16 h (06:00 to
Correspondence to: Dr. Henry van den Brand, Adaptation Physiology Group, Wageningen, Institute of Animal Sciences, Wageningen University,
PO Box 338, 6700 AH Wageningen, The Netherlands. Tel: þ31-317-483120. Fax: þ31-37-485006. E-mail: henry.vandenbrand@wur.nl
Accepted for publication 27th July 2004.
22:00 h) light 8 h dark, and a stable temperature between the egg weight and the weight of the
was maintained between 17 and 20 C. This shell and yolk.
light schedule matched the amount of daylight The other 50% of the eggs were stored in a
for the hens in the outdoor system. (2) In the refrigerator at 5 C for 8 d. To separate the
outdoor (FR) system 34 hens and 6 cockerels of albumen and yolk easily, the eggs were boiled
the H line, 32 hens and 6 cockerels of the C for 10 min. After cooling for 5 min in running
line and 30 hens and 6 cockerels of the L line water, the shell, yolk and albumen were sepa-
were kept on a free range system with a large rated and weighed. Dry matter content of the
shelter (5 m 5 m 3 m). Hens and cockerels boiled yolk and albumen was analysed, by drying
could go outside to a pasture of about 350 m2, the yolk and albumen overnight at 70 C,
where there was a small shelter of straw and followed by 4 h at 103 C.
pallets (1.5 m 2 m). In the large shelter,
6 perches of 2.5 m each with a height of 50 cm
Statistical analyses
were placed on the sawdust floor. Twenty-four
nest boxes were present. The light schedule in All data were analysed using the GLM procedure
the large shelter was similar to that of the cage of SAS (1999) with age and housing system
house. In the outdoor system all hens of the three as main effects and the two-way interaction
lines were housed together with the cockerels, so between these factors. When the main effects
the origin of individual eggs was not clear. were significant, least square means were sepa-
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All hens (and cockerels) were fed ad libitum, rated using the least significant difference proce-
with a commercial feed for laying hens dure. Effects of line on egg characteristics in
(11.82 MJ ME/kg, 160 g CP/kg, 6.2 g lysine/kg the BC housed hens are given in Van den Brand
5.5 g methioninene þ cysteine/kg, 37.0 g Ca/kg, et al. (2004).
2.9 g available P/kg. Water was available
ad libitum. The beaks of all birds in both housing
RESULTS
systems remained intact.
Egg production started at 18 weeks of age in the
Egg measurements BC layers, whereas the first egg was laid at 21
weeks of age in the FR layers. At the start of the
Freshly-laid eggs were collected from each
experiment (25 weeks of age), the production
sire family at a layer age of 25, 29, 33, 37, 41,
percentage was 84 and 75% for the BC and FR
45, 49, 55 and 59 weeks (June 2002 to February
layers, respectively.
2003). At each collection period approximately
20 to 30 eggs per line in cages or from the FR
hens were taken. In total 1053 eggs (H line
Interactions between layer age and housing
cage: 273, C line cage: 276, L line cage: 236,
system
outdoor, 268) were collected and measured
within 3 h of being laid. Several interactions between layer age and
Eggs were weighed and the length and housing system were found. Egg weight increased
breadth were measured. From these measure- with layer age in both housing systems. The FR
ments the shape index was calculated (breadth/ layers had lower egg weight than the BC layers at
length 100). After weighing 50% of the the beginning of the experiment, but egg weight
eggs were broken on to a flat surface and the increased faster and was greater at a layer
height of the albumen was measured halfway age of 59 weeks (Figure 1). Eggshell percentage
between the yolk and the edge of the inner thick decreased with layer age in the BC group,
albumen by using an albumen height gauge whereas eggshell percentage fluctuated with age
(Ames, Waltham, MA, USA). The colour of in the FR group (Figure 2).
the yolk was determined using the Roche Overall, albumen height and dry matter
colour fan (1979). Thereafter the yolk was content decreased with age, whereas yolk dry
separated from the albumen and weighed and matter content increased with layer age.
the pH of the albumen was measured using a Albumen pH increased slightly until week 41
standard pH meter (Radiometer Copenhagen and thereafter decreased. This increase or
PHM 82, Denmark). The albumen was removed decrease with layer age differed between housing
from the shells and shells plus membranes systems, resulting in an interaction between layer
were weighed. Shell thickness (without inner age and housing system. This was demonstrated
and outer shell membranes; membranes were for albumen height (Figure 3a), albumen pH
removed manually) was measured at three places (Figure 3b), albumen dry matter content (Figure
(top, middle, bottom), using a micrometer 4a) and yolk dry matter content (Figure 4b). For
(Mitutoyo, Miyazaki, Japan). The weight of all these characteristics, the BC group showed a
the albumen was calculated as the difference more consistent increase or decrease with layer
HOUSING SYSTEM AND EGG QUALITY 747
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Figure 1. Fresh egg weight in relation to layer age and housing system (least square means; overall SEM ¼ 0 .50).
Figure 2. Eggshell percentage in relation to layer age and housing system (least square means; overall SEM ¼ 0 .25).
age, whereas the FR group fluctuated consider- times, both groups showed similar patterns with
ably more. In addition to the greater fluctua- layer age.
tion with layer age, FR layers showed
more variation in most egg characteristics at a
Age effects
given age.
For yolk colour also, an interaction Regardless of housing system yolk weight
between layer age and housing system was increased with layer age, whereas albumen
found, attributable to a low average yolk colour weight decreased, resulting in an increase in
at week 33 for the FR group (9.2). At other yolk: albumen ratio with advancing age (Table 1).
748 H. VAN DEN BRAND ET AL.
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Figure 3. Albumen height (a; SEM ¼ 0 .51) and albumen pH (b; SEM ¼ 0 .05) in relation to layer age and housing system
(least square means).
Regardless of housing system no effect on characteristics did not differ between the BC and
eggshell thickness was found. The shape index FR layers (Table 1). Overall, yolk colour was
of the eggs decreased with age, meaning that considerably darker in the eggs of the FR layers
with increasing age eggs became relatively (Table 2).
longer. Yolk colour changed with age, but no
clear pattern could be observed (Table 2).
DISCUSSION
Figure 4. Egg albumen (a; SEM ¼ 0 .16) and egg yolk (b; SEM ¼ 0 .17) dry matter content in relation to layer age and housing system
(least square means).
As a result of this delayed first oviposition, laying interactions between housing system and age
percentage was lower at the start of the experi- were not presented. Overall, Torges et al. (1976)
ment and egg weight was also lower in the FR and Mostert et al. (1995) demonstrated no
layers. With advancing age, egg weight increased effect of housing system on egg weight, in
in both housing systems, in agreement with agreement with the present study, whereas
numerous other studies (Hill and Hall, 1980; Leyendecker et al. (2001b) found no difference
O’Sullivan et al., 1991; Peebles et al., 2000; in egg weight between cage-housed and FR layers
Silversides and Scott, 2001). However, as far as when white layers (LSL) were used. However,
we are aware, the greater increase with advancing when brown layers (Lohmann Traditional) were
age for FR layers has not previously been used, egg weight was lower in the FR system.
demonstrated. Hughes et al. (1985), Mostert Pavlovski et al. (1981) and Hughes et al. (1985)
et al. (1995) and Leyendecker et al. (2001b) reported greater egg weight for FR layers than
measured egg weight over a period of 40 to 50 for caged layers. Based on the interactions we
weeks, at 4-week intervals, but effects of age or found, it can be concluded that it is important
750 H. VAN DEN BRAND ET AL.
Table 1. Effects of layer age and housing on egg weight, egg shape (breadth/height 100), proportions of eggs and yolk:albumen ratio
(g/g) (least square means)
Egg weight (g) Shape (%) Yolk (%) Albumen (%) Shell (%) Shell thickness (mm) Yolk/albumen
N 1053 1053 510 510 526 519 510
Age < 0.001 < 0.001 < 0.001 < 0.001 0.14 0.21 < 0.001
Housing 0.92 < 0.001 0.17 0.31 0.72 0.85 0.18
Age housing 0.002 0.61 0.77 0.64 0.03 0.15 0.79
a—h
Least square means of layer age and housing lacking a common superscript differ (P < 0.05).
Table 2. Effects of layer age and housing on albumen height, albumen pH, yolk colour and dry matter content of the albumen and yolk
(least square means)
Albumen height (mm) Albumen pH Yolk colour DM albumen (%) DM yolk (%)
N 511 511 517 512 511
interaction between age and housing system as study, an increase in albumen pH was found
eggshell percentage. This means that in caged until week 41, with subsequently a decrease.
birds, eggshell quality decreased with age, The reason for this contrast with the literature,
whereas in outdoor birds, this characteristic in which a continuous increase in albumen pH
remained constant or even increased with age. with age is shown, is unclear. Possible reasons
In most studies (Pavlovski et al., 1981; Hughes for the increase in albumen pH with layer
et al., 1985; Mostert et al., 1995; Leyendecker age have been summarised by Lapão et al.
et al., 2001b) greater eggshell thickness or (1999). It could be due to a more advanced
strength was found in eggs from outdoor layers. development of the embryo at oviposition or
Eggshell thickness in relation to housing system greater metabolic activity in eggs of older
could possibly be used as a bio-indicator for layers. Benton et al. (2001) demonstrated that
layer health and/or layer production. Effects fertilized eggs have higher albumen pH and
of age on eggshell percentage and eggshell lower albumen height than unfertilized eggs.
thickness differ between studies (with cage Because the FR layers were housed together with
housing). O’Sullivan et al. (1991) and Peebles cockerels and BC layers were housed individu-
et al. (2000) found no clear effect, whereas ally, lower albumen height and higher albumen
Silversides and Scott (2001) found a negative pH in the FR systems could be expected. In our
effect of age on eggshell percentage. These study, this was not the case, possibly due to other
somewhat ambiguous results between studies variables differing between the two housing
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