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Effects of Cryogenic Cooling of Shell Eggs on Egg Quality1

D. R. Jones,*,2,3 J. B. Tharrington,† P. A. Curtis,†,4 K. E. Anderson,* K. M. Keener,† and F. T. Jones‡

Departments of *Poultry Science and †Food Science, North Carolina State University, Raleigh, North Carolina, 27695; and
‡Department of Poultry Science, University of Arkansas, Fayetteville, Arkansas, 72701

ABSTRACT This study was conducted to investigate (Experiment 1: 73.27, GN; 72.03, LN; and 71.4, TC and
the effects of cryogenic cooling on shell egg quality. Gas- Experiment 2: 74.42, GC and 70.18, TC). The percentage
eous nitrogen (GN), liquid nitrogen (LN), and gaseous of loss eggs in the GN treatment was significantly (P <
carbon dioxide (GC) were utilized to rapidly cool eggs 0.01) greater than those of the LN and TC treatments.
in a commercial egg processing facility and were com- Vitelline membrane strength was greater for the cryogeni-
pared to traditional cooling (TC). A modified food freezer cally cooled eggs versus traditional processing. Vitelline
was attached to existing egg processing equipment in membrane breaking strength decreased over storage
order to expose eggs to the selected cryogen.
time. Vitelline membrane deformation at rupture was
In Experiment 1, eggs were treated with GN, LN, and
significantly (P < 0.05) greater for the cryogenically cooled
TC then stored and tested over 10 wk. Experiment 2 eggs
were treated (GC and TC) and evaluated for 12 wk. Qual- eggs compared to the traditional eggs in each experiment.
ity factors that were measured included Haugh units, Use of the technology could allow for egg quality to
vitelline membrane strength and deformation at rupture, be maintained for a longer time, which could increase
and USDA shell egg grades for quality defects. international markets and potentially lead to extended
Haugh unit values were greater for cryogenically shelf lives.
treated eggs as compared to traditionally cooled eggs
(Key words: cryogenic cooling, Haugh unit, egg grade, vitelline membrane)
2002 Poultry Science 81:727–733

INTRODUCTION trolled to achieve safe, high-quality shell eggs. Funk


(1935) reported that individual eggs held at 10 C (50 F)
Food safety and quality are major concerns of the cooled at a rate of 22 C (40 F)/h. When eggs were placed
consumer with eggs being of interest since they have in wire baskets, the cooling rate decreased to 3.6 C (6.5
been linked to a number of foodborne illness outbreaks. F)/h. When stored in wood cases, the cooling rate was
The United States produced 5.98 billion dozen eggs in decreased to 0.72 C (1.3 F)/h. Damron et al. (1994) found
2000. Of those eggs, 3.3 billion dozen were marketed as that shell eggs do not continue to cool during transporta-
shell eggs, which resulted in a per capita egg consump- tion. Refrigerated trucks were able only to maintain the
tion of 258 eggs. Although egg processors are held liable temperature of the eggs. Therefore, eggs must be cooled
for food safety incidences, ensuring the quality and before shipping.
safety of shell eggs is the responsibility of everyone in Previous work conducted by Curtis et al. (1995) found
the distribution chain. higher Haugh unit scores (HU) for eggs cryogenically
Previous research has demonstrated that time and cooled with carbon dioxide gas, as compared to those
temperature are important factors that need to be con- eggs traditionally cooled, after 30 d of storage. Kahra-
man-Dogan et al. (1994) reported that HU values de-
crease over storage time. Moats (1978) and Rhorer (1991)
found temperature to be the most important factor for
2002 Poultry Science Association, Inc.
Received for publication September 20, 2001. interior quality deterioration of shell eggs. Williams
Accepted for publication November 27, 2001. (1992) has reported that elevated temperatures and de-
1
Mention of trade mark, proprietary product, or specific equipment lays in cooling led to lower HU values. He also stated
does not constitute a warranty by North Carolina State University and
does not imply its approval to the exclusion of other products that may that maintaining albumen quality required quick cool-
be suitable. ing to 0 C.
2
Current address: USDA-ARS, Russell Research Center, Athens,
GA 30604.
3
To whom correspondence should be addressed: drjones@saa.
ars.usda.gov. Abbreviation Key: GC = gaseous carbon dioxide; GN = gaseous
4
Current address: Department of Poultry Science, Auburn University, nitrogen; HU = Haugh unit; LN = liquid nitrogen; SE = Salmonella
Auburn, AL 36849. enteritidis; TC = traditionally cooled.

727
728 JONES ET AL.
TABLE 1. Effect of cryogenic treatment on cooling curve intercept and slope in Experiments 1 and 2

Treatment Intercept Slope


Experiment 1
Gaseous nitrogen 3.703Z ± 0.030 −0.0001Z ± 0.0001
Liquid nitrogen 3.985Y ± 0.036 −0.0015Y ± 0.0002
Traditional 4.186X ± 0.036 −0.0026X ± 0.0002
Experiment 2
Carbon dioxide 3.789Z ± 0.019 −0.0018Z ± 0.0002
Traditional 4.217Y ± 0.027 −0.0048Y ± 0.0003
X–Z
Means within a column for each experiment with the same letter are similar (P < 0.001).

D’Aoust et al. (1980) found that eggs, stored at room of 1997. This time frame was chosen because it has been
temperature, with low numbers of Salmonella enteritidis identified as having the highest temperatures during the
(SE) contamination had increased SE growth after 2 d. year. Each experiment consisted of two separate testing
In 1994, Humphrey reported that the time before an periods with two replicates of each treatment being pro-
egg can support salmonella growth is dependent on the cessed. The first experiment used liquid (LN) and gas-
storage temperature. In addition, Miyamoto et al. (1998) eous (GN) nitrogen as the cryogenic cooling medium
found that cooling suppressed salmonellae penetration compared to traditional cooling (TC). The second experi-
through the egg shell, whereas Catalano and Knabel ment used gaseous carbon dioxide (GC) as the cryogenic
(1994) have stated that slowly chilled eggs were more coolant and compared those eggs with TC eggs. In each
prone to SE penetration than are rapidly cooled eggs. experiment, large-size, nest run eggs were processed
Gast and Beard (1990) and Humphrey et al. (1991) using a Diamond 8200 washer/grader.5 Eggs were
have stated that intraovarian salmonellae contamination washed, candled, and placed in foam cartons. Rapidly
occurs in the albumen or outside the vitelline membrane. cooled eggs came from two designated packer heads
Humphrey (1994) has further reported that bacterial and were passed through a cooling tunnel where they
growth occurs when storage related changes allow pene- were exposed to the cryogen with the lids of the foam
tration of the organism into the yolk. He also stated cartons open. Immediately after, the lids were closed
that the rate of change in membrane permeability is and the cartons were placed in cardboard cases (30
temperature-dependent. dozen per case). TC eggs came from two additional
Water movement has also been identified as an im- packer heads and were placed directly into cardboard
portant link for microbial invasion of the yolk. Romanoff cases without exposure to the cooling tunnel. Separate
and Romanoff (1949) stated that osmotic movement of TC eggs were used as a control for each period of Experi-
water across the vitelline membrane (from the albumen) ments 1 and 2.
leads to enlargement and flattening of the yolk. Heath The cooling tunnel, a modified 18-ft JE-U4 freezer,6
(1976) reported that vitelline membrane weight in- used for this study was not specifically designed for
creased at refrigerated temperature and with this in- cooling shell eggs. Average tunnel temperatures were
creased weight there was a decrease in the rate of water −110 ± 3 C and −51 ± 3 C for the GN and GC, respectively,
movement. Furthermore, Smolinska and Trziszka (1982) at the shell surface. The LN was applied directly to the
have stated that selective properties of the vitelline eggs in the carton, and due to the gaseous interface, the
membrane depend on the conditions and period of stor- shell temperature was −120 C.
age. Therefore, the rate of cooling could play an im- A 30-case pallet was formed for each treatment repli-
portant role in the microbial integrity of the egg by cate and stored in a commercial cooler at 7 C. The cooling
changing the physical properties of the vitelline curve data for each treatment were collected with a pal-
membrane. let simulator as described by Curtis et al. (1995). A tem-
Therefore, this study was conducted to investigate the perature probe connected to a Cox Tracer7 data logger
effects of in-line commercial cryogenic cooling on shell was placed in the yolk of the centermost egg of a case
eggs. Physical qualities of eggs were monitored to quan- from each treatment during a replicate (n = 2). The data
tify the effects of this process. logger recorded temperatures every 13 min for 14 d.
The eggs were tested during 10 wk of storage for the
first experiment and 12 wk of storage for the second
MATERIALS AND METHODS experiment. Tests were conducted Monday through
The current study was conducted in a commercial egg Thursday each week. Eggs were tested for interior qual-
processing facility during July, August, and September ity (HU), USDA grade, and vitelline membrane breaking
strength and deformation at rupture. HU measurements
were conducted with the procedure outlined by Haugh
(1937) with the aid of a QCD instrument range.8 A 15-egg
5
Diamond Systems, Farmington, MI. sample was tested daily from each treatment replicate (n
6
Praxair, Inc., Burr Ridge, IL.
7
Cox Recorder, Belmont, NC. = 60 eggs/wk) with cracked eggs being excluded. Eggs
8
Technical Services and Supplies, Dunnington, York, England. were stored at 4 C until analysis.
EFFECTS OF CRYOGENIC COOLING OF SHELL EGGS ON EGG QUALITY 729
Egg grading was conducted by USDA egg graders.
During the week of processing, a sample of 100 eggs
from each treatment replicate was graded daily (n =
400 eggs/wk). A sample of 50 eggs of each treatment
replicate was graded daily (n = 200 eggs/wk) for the
remaining storage time. The graders assessed the per-
centages of loss and cracked eggs as described by the
USDA Egg Grading Manual (USDA, 1990).
Vitelline membrane breaking strength was measured
daily on a sample of 10 eggs from each treatment repli-
cate (n = 40 eggs/wk). Nine weeks of storage was used
for this measurement in the first experiment due to dif-
ficulty in achieving consistently measurable results after
9 wk of storage. Eggs were broken into a shallow dish
FIGURE 1. Average cooling curves for each treatment in Experiment
to allow orientation of the yolk for penetration along 1. ▲ Gaseous nitrogen; 䊉 Liquid nitrogen; 䊐 traditional.
the equatorial region. It was previously reported (Lyon
et al., 1972) that the strongest section of the vitelline
membrane is near the chalazae. Therefore, care was that reached 8.3 C within the first hour of being placed in
taken to prevent contact of the probe with the germinal the pallet simulator. The LN and TC treatments required
disc and the chalazae. The albumen was not separated more than 5 d to reach an equivalent temperature. Czar-
from the egg to prevent drying of the vitelline membrane ick and Savage (1992) and Anderson et al. (1992) have
during testing. The compression measurements were also reported a minimum of a 5-d interval for the cen-
made using a TA.XT2i texture analyzer9 with a test speed termost egg in a pallet of traditionally processed eggs
of 3.2 mm/s set at 10 g full scale. A 1-mm rounded end, to reach 7 C.
stainless steel probe was used to apply direct pressure The GN eggs maintained the highest (P < 0.01) average
on the vitelline membrane until the membrane ruptured. HU score (73.27), and the LN and TC treatments were
Cracked eggs were also excluded from vitelline mem- 72.03 and 71.40, respectively (Table 2). The gradual de-
brane measurements. Eggs were stored at 4 C until cline of HU values over time is illustrated in Figure 2.
analysis. In this figure, the LN and TC eggs declined to A grades
Data were analyzed by general linear models proce- (HU ≤ 72) approximately 1 wk before those in the GN
dure of SAS software (1996). Means were separated by treatment.
the least-squares method. A regression analysis was con- The percentage of cracked eggs was significantly
ducted on log transformations of each cooling curve. greater (P < 0.001) in the GN eggs (10.49%) than the
Slopes and intercepts were determined for the rate of LN and TC treatments, which were similar (6.02% and
temperature decline and were then analyzed by general 5.77%, respectively) (Table 2). Two factors are thought
linear models procedure from SAS software to establish to be the cause of the increased cracking. First, eggs
significant differences between the curves. were frozen in the tunnel by direct contact between the
eggshell and gaseous nitrogen. Second, the force used
RESULTS AND DISCUSSION to deliver the gaseous nitrogen was approximately 320
psi, which resulted in eggs being blown from the cartons
Experiment 1 with a high amount of egg-to-egg contact. The cracked
Analyses of the intercepts and slopes of the cooling
curves are shown in Table 1. The GN eggs had the lowest
(P < 0.001) intercept value indicating the greatest heat
loss prior to palletizing. The GN slope indicates that the
cooling process was complete within the first hour post-
processing. These results illustrate a greater rate of ini-
tial cooling for the GN eggs. The LN eggs cooled with
a moderate rate of heat loss, whereas TC eggs had the
least heat loss prior to packaging in the cases. The aver-
age cooling curves for the treatments in this experiment
are illustrated in Figure 1. These curves were con-
structed by combining both replicates of each treatment.
All curves illustrate the 14-d post-processing and graph-
ically illustrate the effectiveness of the GN treatment

FIGURE 2. Storage time and treatment effects on Haugh unit values


9
Texture Technologies, Scarsdale, NY. in Experiment 1. ▲ Gaseous nitrogen; 䊉 liquid nitrogen; 䊐 traditional.
730 JONES ET AL.
TABLE 2. Effect of treatment on Haugh units, percentages of cracked and loss eggs, and vitelline
membrane strength and deformation at rupture in Experiment 1

Vitelline
Vitelline membrane
membrane deformation
breaking at rupture
Treatment Haugh Unit Cracked (%) Loss (%) strength (g) (mm)
Gaseous nitrogen 73.27 ± 0.14
A
10.49 ± 0.34
Z
5.57A ± 0.22 1.91a ± 0.01 2.00a ± 0.03
Liquid nitrogen 72.03B ± 0.16 6.02Y ± 0.39 1.03C ± 0.26 1.90ab ± 0.01 1.94a ± 0.03
Traditional 71.40C ± 0.16 5.77Y ± 0.39 2.01B ± 0.26 1.86b ± 0.03 1.87b ± 0.03
A,B
Means within a column with the same letter are similar (P < 0.01).
Y,Z
Means within a column with the same letter are similar (P < 0.001).
a,b
Means within a column with the same letter are similar (P < 0.05).

eggs were not equally distributed throughout a repli- (Table 2) was greater (P < 0.05) for the cryogenically
cate, which suggests that the GN was not delivered at cooled treatments than the TC eggs. The increased defor-
a consistent pressure. Redesign of the cooling tunnel mation of the vitelline membrane indicates an increase
specifically for shell eggs could reduce the percentage in elasticity in the vitelline membrane, which could con-
of cracked eggs seen in the GN treatment. tribute to fewer broken yolks when cracked out by con-
The number of loss eggs was greatest (P < 0.01) in the sumers or egg-breaking plants.
GN treatment, and the LN treatment maintained the
lowest (1.03%) overall percentage (Table 2). The higher Experiment 2
percentage of loss eggs in the GN treatment was due to
the higher percentage of stuck yolks. This finding might The GC eggs had a significantly (P < 0.001) lower
have been related to the cold temperature of GN and intercept value and steeper slope in the average cooling
the small contact area for cooling at the large end of the curves as compared to the TC eggs (Table 1). The average
egg, which may have caused the migration of the yolk egg cooling curves for the two treatments are illustrated
away from the extreme temperature. This migration led in Figure 3. The GC eggs initially dropped to an average
to a high percentage of yolks sticking to the shell mem- temperature of 12.8 C within the first hour after leaving
brane. In contrast, the LN was dripped on top of the the cooling tunnel. The TC eggs had an average tempera-
eggs, which led to pooling in the bottom of the carton ture of 33 C within 1 h of being packaged into cases.
and enhanced heat transfer around the entire egg The GC eggs therefore had a greater loss of heat post-
surface. processing compared to TC eggs.
The GN treatment required the greatest (P < 0.05) For this experiment, the HU values were analyzed
overall force (1.91 g) to rupture the vitelline membrane by periods. The two periods were analyzed separately
with the LN eggs being intermediate and the TC eggs because of the differences in the source of eggs used for
having the lowest vitelline membrane strength (Table each period. The eggs used in the first period were from
2). The force needed to rupture the vitelline membrane older hens (70 wk of age, premolt), which produced
decreased (P < 0.01) over the 9-wk storage (Table 3) with eggs of poorer quality, including decreased HU scores
the maximum force required being 2.17 g during Week (Curtis et al., 1985). This lower initial quality can be
1. After 9 wk of storage, the membranes began to deterio- observed (Figure 4) with the HU values of the TC eggs
rate beyond the lower limits (< 1.0 g) of the instrument, from the first period, which were in the A grade range
which could not consistently detect a measurable force. (HU ≤ 72) throughout storage. The initial values for the
For this reason, the results for 9 wk only are presented. GC eggs, from the same flock, were 80.70 (grade AA).
The deformation of the vitelline membrane at rupture This trend of higher HU values for the GC treatment

TABLE 3. Storage time effect on vitelline membrane breaking strength in both experiments

Storage time (wk) Experiment 1 (g) Experiment 2 (g)


1 2.17A
± 0.02 2.14A ± 0.04
2 2.02B ± 0.02 1.96BC ± 0.04
3 1.98BC ± 0.02 1.98B ± 0.04
4 1.93CD ± 0.02 1.87BCD ± 0.04
5 1.89DE ± 0.02 1.89BCD ± 0.04
6 1.83EF ± 0.02 1.86BCD ± 0.04
7 1.75F ± 0.02 1.85CDE ± 0.04
8 1.78F ± 0.02 1.76DEF ± 0.04
9 1.67G ± 0.02 1.73EF ± 0.03
10 1.68F ± 0.02
A–C
Means within a column with the same letter are similar (P < 0.01).
EFFECTS OF CRYOGENIC COOLING OF SHELL EGGS ON EGG QUALITY 731
TABLE 4. Effect of processing period on Haugh unit values for Experiment 2

Treatment Period 1 Period 2


Carbon dioxide 74.01Z ± 0.22 74.82A ± 0.22
Traditional 66.71Y ± 0.30 73.64B ± 0.30
A,B
Means within a column with the same letter are similar (P < 0.01).
Y,Z
Means within a column with the same letter are similar (P < 0.001).

TABLE 5. Effect of treatment on percentage of cracked and loss eggs and vitelline membrane
breaking strength and deformation at rupture in Experiment 2

Vitelline Vitelline
membrane membrane
breaking strength deformation at
Treatment Cracked (%) Loss (%) (g) rupture (mm)
Carbon dioxide 6.81 ± 0.30
a
2.17 ± 0.27 1.90a ± 0.01 1.97a ± 0.02
Traditional 5.52b ± 0.42 1.84 ± 0.38 1.85b ± 0.01 1.87b ± 0.03
Means within a column with the same letter are similar (P < 0.05).
a,b

continued for the 12 wk of storage. The GC eggs had a value was not above the allowable level (7% per grade
greater (P < 0.001) average HU value compared to the lot at retail) defined by the USDA. The allowable retail
TC eggs (Table 4). The increased HU value might have percentage was used because a transportation process
been due to carbon dioxide entering the eggs during the was involved to move the eggs to the laboratory from
cooling process and remaining in the albumen, which the processing facility. The approximate 1% increase in
could slow chemical degradation. cracked eggs was due to cooling tunnel design. Redesign
The eggs used during the second period were from of the cooling tunnel could significantly reduce cracked
younger hens (30 wk of age), which produce eggs of eggs. Curtis et al. (1995) also reported an increase in
higher quality. A significant (P < 0.01) difference is seen cracked eggs when subjected to carbon dioxide cooling.
(Table 4) between the GC and TC eggs for this period. They found that once the carbon dioxide snow was pre-
The GC eggs had an average HU value (74.82) that was vented from coming in direct contact with the shell sur-
greater than the TC eggs (73.64), but the difference be- face, cracks decreased. Fajardo et al. (1996) also found
tween these averages was much smaller than those pro- an increased incidence of cracks in shell eggs subjected
duced by the older flock. These data suggest that carbon to forced-air rapid cooling that were produced by 72-
dioxide cryogenic cooling enhances the interior quality wk-old hens compared to those from 31-wk-old hens.
of the egg, but the greater enhancement was observed The vitelline membrane of GC eggs had significantly
for eggs with poorer initial quality. higher breaking strengths (P < 0.05) than traditionally
Both processing periods were combined before analy- cooled eggs (1.90 g and 1.85 g, respectively), as shown
sis of egg grade data. The overall percentage of loss eggs in Table 5. This increased strength was more prominent
was not significantly different between the treatments, for the poorer quality eggs (first period) than with the
as shown in Table 5. The percentage of cracked eggs higher quality eggs (second period). The vitelline mem-
was greater (P < 0.05) for the GC eggs (Table 5), but this brane strength decreased (P < 0.01) with egg age (Table

FIGURE 3. Average cooling curves for each treatment in Experiment FIGURE 4. Treatment and storage time effects on Haugh unit values
2. ◆ Carbon dioxide; 䊐 traditional. for Period 1 in Experiment 2. ◆ Carbon dioxide; 䊐 traditional.
732 JONES ET AL.

which could explain the decrease in vitelline membrane


strength during storage seen in this study.
A new prototype commercial shell egg-cooling tunnel
that uses GC has been designed. The new cooling tunnel
exposes the individual eggs to the cryogen before pack-
aging into the carton. A faster rate of cooling can be
achieved with the new design (Figure 5). Product testing
indicates that fewer cracks are produced compared to
the prototype tunnel. These results show that cooler
redesign eliminated many of the problems associated
with the JE-U4 cooler.

ACKNOWLEDGMENTS
FIGURE 5. Average cooling curve for prototype commercial egg The authors acknowledge the following contributors
cooling tunnel utilizing carbon dioxide.
to this study: Praxair, Inc., Chicago, IL; US Poultry and
Egg Association, Tucker, Georgia; Simpson Eggs, Mon-
roe, North Carolina; and the North Carolina Department
3). The GC eggs also had significantly higher (P < 0.05) of Agriculture, Raleigh, North Carolina.
membrane relative deformation at rupture than tradi-
tionally cooled eggs (Table 5). Therefore, GC treated
eggs had vitelline membranes that were stronger and
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