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Internal egg temperature in response

to preincubation warming in broiler
breeder and turkey eggs
Article in The Journal of Applied Poultry Research March 2006
Impact Factor: 0.59 DOI: 10.1093/japr/15.1.1

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2006 Poultry Science Association, Inc.

Internal Egg Temperature in Response

to Preincubation Warming in Broiler
Breeder and Turkey Eggs
R. A. Renema, J. J. R. Feddes,1 K. L. Schmid, M. A. Ford, and A. R. Kolk
Department of Agricultural, Food, and Nutritional Science,
University of Alberta, Edmonton, AB, Canada T6G 2P5

Primary Audience: Broiler Flock Managers, Researchers, Field Service Technicians,

Hatchery Personnel
SUMMARY
Various methods of preincubation warming have been used in commercial hatcheries to increase
hatchability, decrease incubation time, and increase embryonic blastoderm development. A study
was conducted to determine the effect of preincubation warming and egg size on the warming rate
of eggs. Three egg groupings were evaluated: small broiler breeder eggs (52 to 57 g), large broiler
breeder eggs (64 to 69 g), and turkey eggs (74 to 107 g). The eggs were subjected to 2 temperature
treatments. The conventionally incubated eggs were moved directly from storage (17.5C) to the
incubator (adjusted to 37.5C). The preincubation warmed eggs were moved from the storage
room to the preincubation room (28C) for 12 h and then to the incubator. Internal egg temperature
was measured once per minute to calculate the rate of warming. The warming rate potential (k
value) differed for egg type and temperature treatment. The values for small and large broiler
breeder eggs and turkey eggs were 0.0506, 0.0488, and 0.0471 kJ/min per kJ of energy in the egg,
respectively. This study characterizes the maximum rate of temperature change that occurs when
eggs are transferred from a storage or preincubation area to the incubator, creating baseline values
for future work with the modification of hatchery management protocols. These data can contribute
to more informed decisions regarding hatchery temperature profile strategies and their effect on
the developing embryo.
Key words: preincubation warming, warming rate, egg size
2006 J. Appl. Poult. Res. 15:18

DESCRIPTION OF PROBLEM
In the hatching egg industry, eggs are stored
in the breeder barn until transport to the hatchery
occurs and at the hatchery until space becomes
available in the incubators. Eggs are stored below the minimum temperature for embryonic
development [1]. This temperature has been reported to be 28C by Funk and Biellier [2] and
more recently 20 to 21C [1].
1

Corresponding author: john.feddes@ualberta.ca

Preincubation warming is the warming of

eggs prior to placement in the incubator. During
prolonged storage, the periodic or intermittent
warming of eggs can improve hatchabilityparticularly for birds that have a low rate of hatchability [3, 4]. Recommended storage temperatures are lower for storage periods of greater
than 7 d [6]. However, little benefit has been
reported for storage periods of less than 14 d [5,
6, 7, 8]. By decreasing the storage temperature

JAPR: Research Report

2
further below physiological zero, any disproportionate development of embryo tissues is slowed
[8]. Hen age can modulate the impact of temperature changes on the embryo. Meijerhof et al.
[9] suggested that older birds tend to lay eggs
with fewer viable embryos that have an increased sensitivity to temperature and a reduced
ability to withstand storage. Ultimately, preincubation warming methods are most beneficial to
birds with poor rates of hatchability [4], embryos
subjected to long-term preincubation storage [5],
and when lower storage temperatures are used
[6].
When eggs are prewarmed, the temperature
of their environment changes from below physiological zero to an environmental temperature
where further development is possible. The intermittent preincubation warming during prolonged storage allows further proportional tissue
development and increases hatchability [8].
Once these eggs are transferred to the incubator,
the minimum temperature for development will
not be the same for all embryonic tissues [10].
At the embryonic level, this means that it is
beneficial to bring the eggs up to incubation
temperature quickly to avoid abnormal growth
and an increased likelihood of embryonic mortality. However, incubator design may limit the
ability of the egg temperature to reach adequate
levels at a reasonable rate. Preincubation warming just before transfer into the incubator can
increase the basal egg temperature, possibly reducing the embryonic stress by reducing the period in which final warming occurs. The importance of providing the optimum temperature profile to achieve optimally incubated eggs cannot
be discounted. Hen age should already be accounted for in incubation management, because
eggs from younger hens require slightly different
temperature and humidity levels than eggs from
intermediate or old hens for optimal embryogenesis and hatchability [11].
There may be other differences due to variation in incubation needs among modern genetic
lines. Vleck [12] suggested that domestic strains
of birds are less tolerant of variability in the
physical environment than are wild birds. Decuypere and Michels [8] follow this by noting
that heavily selected broiler lines are the least
tolerant of temperature variation when compared
with other domestic strains. With many hatcher-

ies moving from multistage incubation toward

single-stage incubation, strain-specific incubation management is possible. To achieve an ideal
incubation temperature profile for different sized
eggs from different strains, there needs to be a
basic understanding of temperature change
within different egg sizes and types.
Meijerhof and van Beek [13] described the
influence of climatic conditions on the temperature development during warming or cooling
of eggs through mathematical modeling. They
predicted exponential temperature development
during an imposed temperature change on the
eggs. The rate of warming for an object can be
calculated with Equation 1 [14]
(Tfinal T) / (Tfinal Tinitial) = e (hA/cv)t
Equation [1]
k = hA/cv
Equation [2]
The warming rate potential is described by
the convection coefficient (h), egg area (A), egg
density (), egg specific heat capacity (c) and
egg volume (v). The units of k are kilojoules
per minute of warming per kilojoule of energy
in the egg. Equations 1 and 2 can be combined
into Equation 3 to express warming rate potential
(k) as
k = ln(Tfinal T)/t
Equation [3]
The objective of this study was to determine
if a difference exists between the rate of internal
warming of eggs that are prewarmed prior to
incubation and the warming rate of eggs set
immediately upon removal from the cooler. The
effect of egg size on the rate of warming was
also of interest.

MATERIALS AND METHODS

Egg Source
Sixty hatching eggs consisting of 20 small
broiler breeder eggs (52 to 57 g), 20 large broiler
breeder eggs (64 to 69 g), and 20 turkey eggs
(74 to 107 g) were obtained for each of the 3
consecutive replicates of the trial. The small and
large eggs were gathered from a 35-wk-old

RENEMA ET AL.: CHARACTERIZATION OF EGG WARMING

broiler breeder flock and the turkey eggs were
obtained from a 41-wk-old turkey breeder flock.
Fresh eggs were acquired for each replicate of
the study and subjected to the experimental treatments within 2 d of being laid. Each egg was
assigned a number according to tray position
and weight. The eggs were placed in 2 separate
68-egg trays. Each tray contained 10 eggs from
each type arranged in a sequence of small broiler
breeder egg, large broiler breeder egg, and turkey egg in a repeating pattern resulting in an
intermixed arrangement. With this arrangement,
the temperature effects were assumed to be the
same for each replication since flock production
had progressed to a point where egg composition
was much more stable than in very early lay.
Temperature Measurement
A 4-mm diameter hole was drilled into the
top of each egg. A thermistor sensor [15] was
inserted through the opening to a depth of 1.5
cm to ensure the tip was likely in the yolk. The
thermistor was secured to the shell with hot glue.
Each tray also contained a thermistor for measuring the ambient temperature. The thermistors
were connected to a data acquisition module
that transmitted the temperature data to a nearby
laptop computer. Trays were placed inside the
egg cooler (17.5C) overnight to allow the internal egg temperature to equilibrate with ambient
temperature. Tray 1 was then held at room temperature (28C) for 12 h, while tray 2 remained
in the egg cooler. After 12 h, trays 1 and 2
were placed in the incubator, and temperature
measurements continued for both of these trays
for another 48 h. The trays were placed in a
5,000 egg capacity incubator [16] adjusted to
37.5C. The eggs remained in an upright position
throughout the study. This aforementioned
movement of trays created 3 warming treatments: storage to incubator (SI), storage to room
(SR) and room to incubator (RI). Individual egg
temperatures were recorded every min onto a
spreadsheet by the laptop computer. The warming profiles of the eggs are shown in Figure
1 as a mean of all egg types. For each egg,
temperature change per minute (T/min), k
value (kJ/min per kJ of egg energy; equation
3), and the time required to reach a stabilized
temperature tamb were determined (Table 1). The
elapsed time to reach a stabilized temperature

was the time the mean of the egg temperatures

first reached the ambient air temperature of the
eggs. The k and T/min values were determined
from the linear part of the egg-warming curve
using equation 3. The kmass value was normalized
for egg mass by dividing the k value by the egg
mass and multiplying by 1,000 (Table 1).
The experimental eggs were not placed adjacent to other treatment eggs, and no other eggs
were placed in the incubator or storage area
during the study. This allowed for maximal rates
of heat exchange between the egg and its environment and avoided confounding by impeded
airflow caused by egg placement.
Data Analyses
Each replicate of the trial was a 3 3 factorial
design with 3 temperature treatments and 3 egg
sizes. The 3 consecutive replicates were carried
out for 1 wk. A 3-way ANOVA (egg type
temperature treatment replicate) was conducted using the GLM procedures of SAS [17].
The experimental unit was the egg type or tray
within each experimental replicate. The least
significant difference procedure was used to separate means when significant differences were
indicated. Significance was assumed at P 0.05.

RESULTS AND DISCUSSION

The warming characteristics for the 3 egg
types and the 3 temperature profiles were determined (Table 1). Egg mass differed (P 0.05)
among the 3 egg types (small broiler breeder,
large broiler breeder, and turkey; Table 1). The
egg types also differed in their T/min and k
value characteristics, and the kmass value differed
among the 3 egg types. The interaction of egg
type by warming treatment was not significant.
The value of tamb was not different for egg type.
The T per minute and the k value showed
no significant difference between the large
broiler breeder and turkey eggs (Table 1). However, the kmass value differed among these egg
types. As shown in Figure 2, in which a representative portion of the warming profile is presented
for illustration, the warming profiles appear to
be very similar. These results were unexpected
as we had hypothesized that because larger eggs
have a smaller surface area to volume ratio they
would warm more slowly than smaller eggs. The

JAPR: Research Report

Figure 1. Mean comparison of warming profiles between preincubation warming and conventional incubation for
all 3 egg types.

surface area (4r2) to volume ratio (1.33 r3)

was determined mathematically for the egg types
as 3/r where r is the radius of an equivalent
circle to that of an egg [18]. The eggs were
assumed to have a specific gravity similar to that
of water (1 g /mL), because the specific gravity

of an egg is between 1.066 and 1.094. The surface area to volume ratio was 1.3 for small eggs,
1.2 for large eggs, and 1.1 for turkey eggs. Although there was a difference in the surface area
to volume ratio and an average weight difference
of 22 g between the large broiler breeder and

Table 1. Egg warming characteristics for 3 different egg types subjected to 3 different temperature treatments

Source
Egg type
Small broiler breeder4
Large broiler breeder5
Turkey6
SEM
Warming treatment
Storage to incubator7
Storage to room8
Room to incubator9
SEM

Egg
weight
(g)

Temperature
change
(Cmin1)

Time
to ambient
temperature
(tamb)1 (min)

k2
(kJmin1kJ)

kmass3
(kJmin kJ1g 1,000)

54.22c
66.05b
87.74a
0.56

0.204a
0.195b
0.190b
0.0027

210
213
218
5

0.0506a
0.0488b
0.0471b
0.0007

0.93a
0.74b
0.54c
0.03

0.295a
0.132c
0.163b
0.0027

196b
309a
136c
5

0.0507a
0.0441b
0.0517a
0.0007

Means within a column and a source with no common superscripts significantly differ (P < 0.05).
Time to ambient temperature from the imposition of the temperature treatment (min).
2
Warming rate potential calculated from the linearly increasing portion of the warming rate profile.
3
k value normalized for egg mass.
4
Target range 52 to 57 g.
5
Target range 64 to 69 g.
6
Target range 74 to 107 g.
7
Moved from storage to incubator temperature (SI).
8
Moved from storage to room temperature (SR).
9
Moved from room to incubator temperature (RI).
ac
1

RENEMA ET AL.: CHARACTERIZATION OF EGG WARMING

Figure 2. A sample response of egg type to temperature change from the room to incubator.

turkey eggs, the warming behavior between

these egg types expressed as a k value was similar; however, the warming behavior was different when expressed on a mass basis (kmass; Table
1). This finding suggests that the mass rather
than the surface area to volume ratio of the egg
explained the difference in warming rate. The
dynamics of temperature may be more apparent
between egg types in a full incubator, where
egg size and incubation tray design may affect
airflow. Coleman et al. [19] previously indicated
that egg mass and egg size are directly proportional to the amount of time required for an egg
to reach ambient temperature.
The T/min, tamb, and k values were different
for the 3 temperature profiles: SI, SR, and RI
(P 0.05) (Table 1). Figure 3 illustrates a portion
of the warming profile of large broiler breeder
eggs for each of the treatments. A difference
was found in the warming rate between preincubation treated eggs (SR RI) and conventionally
treated eggs (SI), for which it was shown that
the 3 types of eggs in the preincubation warming
treatment had a more gradual warming rate.
The warming profile was found to be more
gradual in the preincubation warming temperature treatment (Table 1; Figures 1 and 3) because
of the lower temperature gradient between the
storage and the preincubation room. These
rooms were not heated with forced-air systems,

which would virtually eliminate air movement

in the immediate vicinity of the egg compared
with those placed directly into the incubator.
Consequently, the tamb value for conventionally
warmed eggs (SI) was 196 min; the prewarmed
eggs went from storage temperature to incubator
temperature (SR tamb + RI tamb) in 445 min. This
was also reflected in the warming rate (T/min).
Eggs in the SI treatment warmed at a rate of
0.30C per minute, which was significantly different from the SR warming rate (0.13C/min)
and the RI warming rate (0.16C/min; Table 1).
These differences are attributed to the difference
in temperature between time of introduction to
the treatment and reaching the new temperature.
The k values determined in this study from
the rates of warming were compared with the k
values for eggs cooled in storage as previously
determined [20]. Eggs that were partially exposed to moving air in the cooling trial had a k
value of 0.0167 kJ/min per kJ of egg energy,
whereas eggs enclosed with no air movement
had a k value of 0.0023 kJ/min per kJ of egg
energy. The values for the partially exposed eggs
were exceeded by approximately 3 times in this
trial (0.0506, small broiler breeder eggs; 0.0488,
large broiler breeder eggs; and 0.0471 kJ/min
per kJ of egg energy for turkey eggs). The lowdensity filling of the trays used in this warming
trial allowed for a high degree of egg surface area

JAPR: Research Report

Figure 3. A sample of initial temperature response of large broiler breeder eggs to 3 different temperature treatments.

exposure to air movement within the incubator.

This demonstrates that maximum rates of temperature change among the egg types and temperature treatments occurred. Full egg trays and
incubators may result in a reduced rate of temperature change if airflow is hindered. For example, a range in embryo temperatures within the
incubator can be related to both airflow and egg
size. Although embryos of all sizes will die when
their internal temperature reaches 48.5C, larger
eggs can reach this temperature earlier because
of their greater production of metabolic heat
[21]. The practical application for larger eggs
may affect the efficiency of heat transfer between the air and the egg. Larger eggs will have
less ability to lose heat per unit of mass as well
as less surface area per unit of mass. Also, egg
shape (narrowness or roundness of the egg) can
affect hatchability by impeding embryo rotation
late in incubation [22]. However, egg shape can
also affect the shape and thickness of the air
cell and influence airflow at the egg surface and
between the eggs. Air velocity affects heat transfer, meaning that heat transfer can be partially
inhibited if air velocity is limited [23].
Proudfoot and Hulan [24] indicated that it
took approximately 1 h to raise the internal egg
temperature from 16 to 38C in a warming chamber. In the current study, the time to a completely
stable, ambient temperature was measured,

which explained some of the difference in times

between these 2 studies. Figure 3 shows that the
period of most rapid temperature change was
quite comparable. Wilson [7] has suggested that
prolonging the period the embryo spends between 27 and 35C can result in disproportionate
development of tissues. The treatments in the
current study brought the eggs to a constant
temperature near the bottom of this range (28C)
to allow a more uniform movement through this
temperature range. Whereas a 26C room temperature would have been more desirable for
this study, this was difficult to achieve in the
research hatchery. Under ideal incubator conditions, the process of bringing the egg up to incubation temperature would be quite rapid. Because variation in egg heating can occur due to
efficiency of air movement and heat transfer to
the egg, partially heating the eggs prior to transfer into the incubator could make this final heating phase more rapid. The current study provides
background data that can contribute to more informed decisions regarding hatchery temperature profile strategies, such as rate of temperature
change for bird strain, bird age, or egg size.
The empirical values determined for warming rates of the 3 egg types could be used as a
basis for further studies on optimal incubation
conditions. Managers of multispecie hatcheries
may benefit from the knowledge that turkey eggs

RENEMA ET AL.: CHARACTERIZATION OF EGG WARMING

have similar warming characteristics to large
broiler breeder eggs. Although preincubation
warming leads to a warming process that is overall more gradual, it may also ensure eggs do
not need as much time in the incubator to fully
initiate embryo development. It may at least create a more uniform initiation of embryonic development compared with what may result from
direct transfer to an incubator with nonuniform

heat transfer conditions. By bringing eggs up to

a temperature just below that where differential
tissue development begins [7], the time to final
temperature is reduced (Table 1), which may
somewhat compensate for inconsistencies in the
rate of heating. Special cases, such as the thinner-shelled eggs from older birds may require a
different rate of temperature change to ensure
viable embryonic development.

CONCLUSIONS AND APPLICATIONS

1. Warming rate potentials for small broiler breeder eggs (52 to 57 g), large broiler breeder eggs
(64 to 69 g), and turkey eggs (74 to 107 g) were 0.0506, 0.0488, and 0.0471 kJ/min per kJ of
energy potentially stored in the egg under ideal incubator conditions.
2. Increased egg size was assumed to decrease warming rate. This hypothesis was true for small
broiler breeder and large broiler breeder eggs; however, turkey eggs were much like broiler
breeder large eggs, even though turkey eggs are much larger. Strain or egg type may influence
the development of optimal heating profiles.
3. Eggs that were transferred directly from storage to incubator warmed at a rate of 0.30C/min,
whereas the prewarmed eggs warmed at rates of 0.13C and 0.16C/min for the storage to room
and room to incubator treatments, respectively. However, by prewarming the eggs, the time to
reach the ambient incubator temperature was 60 min less (136 min) for eggs transferred from
room to incubator compared with those transferred directly from storage to the incubator (196
min). This finding has application in the comparison of efficiencies of incubator performance
and egg warming rate.

REFERENCES AND NOTES

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Acknowledgments

22. Narvuslim, V. G., and M. N. Romanov. 2002. Egg physical

characteristics and hatchability. Worlds Poult. Sci. J. 58:297303.

The supply of eggs by G. Olson and Lilydale Hatchery and the

invaluable assistance of the staff and students of the Alberta Poultry
Research Centre are greatly appreciated.