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Pasteurization of Eggs in the Shell

Article  in  Poultry Science · October 1996

DOI: 10.3382/ps.0751122 · Source: PubMed

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 Pasteurization of Eggs in the Shel11
w. J. STADELMAN, R. K. SINGH, P. M. MURIANA, and H. HOU
FoodScienceD~rtment, PurdueUn~ity, WestLafayette,Indiana47907-1160

ABSTRACT A small percentageof all eggs may be
contaminated with Salmonella enteritidis (SE). To
eliminate this hazard from the food supply, procedures
for pasteurizingeggs in the shell have beendeveloped.
At least four researchgroups are attempting to devisea
processto achievea pasteurizedshell egg. Only one of
the groups has reported proceduresand results. Sound
shell eggswere washedto removesurfacecontaminants.
(Key words: eggs, pasteurization, Salmonellaenteritidis, egg quality)
The cleaneggswere then inoculatedwith high levels of
SEcells.The inoculatedeggswere then heatedby one of
severalmeansto a yolk temperatureof about 55 C and
held at that temperature for varying periods of time.
The number of surviving cells was determined. It is
possible to obtain a 7 log cycle reduction of SE in
inoculated eggs without a significant change in func-
tional or visual quality of the eggs.
1996Poultry Science75:1122-1125

INTRODUCTION bacterialcells in the yolk are usually more heat resistant

than similar cells in the albumen. Cunningham (1995)
The minimum requirements for pasteurization of summarized earlier reports on the effects of several
liquid egg products have been extensively researched temperatures on functionality of egg albumen. The
during the last 60 yr. No literature was found relative to critical temperature appears to be 57 C. At a 57 C
pasteurizationof intact shell eggs. A possible explana- temperaturefor severalminutes egg albumenbegins to
tion for this is that intact eggsat the time of production losefoaming ability. A patent was issuedto Sourbyet al.
were consideredto be sterile. In the mid-1980s,reports (1971)for a processof pasteurizationof liquid whole egg
of ovarian infection with Salmonella enteritidis(SE)and at temperaturesfrom 52 to 63 C. If liquid egg could be
the deposition of SE in the egg during formation pasteurizedat temperaturesof less than 57 C, why not
appeared.Attempts to eliminate SE from laying flocks shell eggs?
have not been completely effective.For this reasonthe For any minimum pasteurizingprocessto be effective
p~ibility of applying the principles of liquid egg initial bacterial loads must be minimal. Barrow (1993)
pasteurization to intact shell eggs have been inves- suggestedthat shell surfacepathogensmay be equally
tigated. as important as liquid contentscontaminationprior to
On April 10, 1995, the Umer-Barry Price Current ovoposition in the transmissionof SE. The incidenceof
included a short report that Pappettis'organizationhad Salmonellaon the shell surface can be reduced by
enteredinto a licenseagreementwith PasteurizedEggs washing eggs in an alkaline solution at moderate
I. P. of New Hampshire for a system for pasteurizing temperatures(Holley and Proulx, 1986).The incidence
eggs in the shell. No further details of the processare of SE-infectedeggs in an SE-infectedflock has been
available. At the 1995 Institute of Food Technologists estimatedto be about 0.5%with lessthan 100cfu of SE
annual meetingHou et al. (1995)reported on pasteuriza- per egg at the time of production (Humphrey et al.,
tion of shell eggs. At that time it was learned that at 1989).Saeedand Koons (1993)reported rapid growth of
least two other groups were researchingthe area. No SE in artificially inoculated eggs. When 20 cfu of SE
details of any of the systemsexcept that of Hou et al. were inoculatedinto eggsand then stored at 23 C for 2
(1996)were obtainable.Van Uth et al. (1995)reported to 3 d, a stationaryphaseof 109cfu was reached.When
that a hot water (57 C) immersion for 30 min did not similarly inoculated eggs were stored at 4 C there was
destroy all Salmonellaof inoculated eggs. minimal growth of SE during 21 d of storage.Hum-
It is well documented that egg albumen is heat phrey (1990b)reported no growth of SE in inoculated
denaturedat lower temperaturesthan the yolk and that shell eggsstored at 8 C. He found a lag time of over 100
h at 10 C and only 15 h at 15 C. Generationtimes for SE
were about 21 h at 10 C and 3 h at 15 C.
Hopper and Mawer (1988)reported natural infection
Receivedfor publication August 16, 1995.
Acceptedfor publication November 10, 1995. levelsin SEpositive eggsto be lessthan 100cfu/l00 g of
IJoumal Number 14,725 of the Purdue University Agricultural yolk. Humphrey et al. (1989, 1991) confirmed these
Research Program. findings with usually less than 10 cfu of SE per egg.

1122
 SECONDOWENJ.COTTERILLEGGAND EGGPRODUCTS
SYMPOSIUM:
Humphrey et al. (1989) studied location of SE in the
intact egg of naturally infectedflocks.The SEwas found
in both albumen and yolk, with greatestconcentrations
in yolk.
Humphrey (1990a)investigatedthe heat resistanceof
SEin eggsafter storageat 4 C and 8 C for times varying
from 0 h to 12 d. Holding for 8 h ormore at 4 C resulted
in a reduction in heat resistance.Humphrey (1990b)
observedno increasein SE cfu when naturally infected
eggs were held at 8 C. At higher temperatures
generation times for SE were less than those for
Salmonella typhimurium.It was found that heat sensitiv-
ity of SEorganismswas greaterin albumenthan in yolk
by Humphrey et al. (1990).
Barrow (1993) discussed various possibilities for
reduction in incidenceof SEfood poisoningsbut did not
include pasteurizationof eggsin the shell. As there is no
J'ect this pape ts
literature
P ossible sub nz, in
waon thisPasteu ' . r thpresen
h 11 some
y s of g eggs m e s e .
MATERIALS AND METHODS
. units and minimal reduction in yolk index using the
With the abovebackgroundof information regarding
eggsand SE,Hou et al. (1996)researchedthe possibility
of destroying SE in eggsinoculatedwith SE.Only clean
shell eggsthat had beenwashedin an alkaline solution,
above pH 11 w~re used (Holl~y and.Proulx,.1986).The
SEwere grown In egg yolk pnor to inoculation of shell
eggs to minimize the effect of media change when
inoculatedinto the yolk of eggs prior to treatmentsfor
pasteurization.Levelsof inoculation varied from 4 x 105
to 4 x 107cfu per gramof egg contents.Normal large
eggs were heated in air, water or by microwave to
determinetimes neededto obtain a yolk temperatureof
55 C followed by holding times at 55 C.
Pasteurizingtreatmentswere heating of shell eggs in
hot water, hot air or with microwave energy followed
by varying holding times. Reductionin colony-forming
units of streptomycin-resistantSE were determined.
§:
~
i:
~ 20
10
0 0
FIGURE 1. Times required to heat the yolk of intact eggs in hot air,
hot water, and microwave oven.
SYMPOSIUM 1123
Working with uninoculated eggs subjected to thl'
several pasteurization treatments,determination ot In-
terior quality and functional quality changeswere made.
For interior quality, Haugh units and yolk indices were
measured. The only functional quality measurements
were on foam volume and stability of the albumenfoam.
RESULTS
When eggswere placedin an abundanceof water the
yolk center was heatedto 56 C in about 20 min. In air
the time neededwas about 1 h and in a microwaveoven
with less than full power only 2 min were required.
With microwaveheating,the yolk temperaturewas 60 C
and the al~umen was 56 to 57 C (Figure 1).
~e SE,-Inoculated egg~wer~ held at 55 to 57 C for
varyIng t1D\es~fter.heatIng (Flgu~e2), Several proce-
dures and holdIng t1D\esand conditions were evaluated
as t 0 thelr 1ethali ty against the mocuI ated 5 E cells
' ' '
(F19ures3, 4, 5, 6, and 7).
'
The functionality and interior quality of pasteurized
eggSwere evaluated. There was no effect on Haugh
method of Sauteret al. (1951).There were no significant
changein foam volume or stability of the albumenfrom
the pasteurized eggs.
DISCUSSION
Hot air heatingwould be the leastpracticalmethod to
heat shell eggs becauseof the extended time period
(> 60 min) required to reach55 C and representsa poor
mediumfor efficienttransferof heat to the insideof the
egg (Figure 1). Water bath heating is more efficient, but
still requires a heating time of approximately 15 min
(Figure 1) to reachthe critical temperatureof 55 to 56 C
at which maximum bacterialinactivation occurswithout
denaturingthe protein componentsof egg white or yolk.
This difference,in heating efficiency is reflected in the
time required for a 3-10g cycle reduction of SE in
10.QCXI,~ 8Q
'.~.~
'oo.~
.10
4OG
-~
'O.~
I '.~ I
1~
10
1
.10 1~ .. -0
1'-("*')
FIGURE 2. Salmontllll mtmtidis destnJction in relation to time held
at 55 C (from Hou et al., 1996, with pem\i8sion).
1124 STADELMAN ET At.
FIGURE3. Destrudion of SEduring heatingand holding of eggsat
55 C in air (from Hou et al., 1996,with pennission).
artificially inoculated eggs by hot air (> 125 min) vs
water bath (25min) heating(Figures3 and 4). The extent
of bacterial inactivation can be increasedby holding at
this critical temperatureto achievethe desiredmicrobial
reduction.
Van Lith et al. (1995)indicated that heating artificially
inoculatedshell eggsat 57 C for 30 min did not result in
completeelimination of SE and extendedincubation at
this temperaturewould causecoagulationof egg white
proteins. Our results conftnned the observationby van
Lith et al. (1995)of the partial reduction (3-log cycles,
Figure 4) of the inoculated cells during water bath
heating and of protein denaturation of egg proteins
during extended incubation at this temperature.
However,by transferringshell eggsfrom the 57 C water
bath to a slightly lower temperature(i.e.,hot air oven at
55 C) once the critical temperature was achieved, we
were able to maintain the quality of the egg as well as
an exponential reduction of Salmonella to over
7-log cycles (Figure 5).
100,a- -
10,a,a
1,000.000 -
e.
[iJ
100,000
I 10,000 I 10,tXXI
1.000
1 10
10 0 10
10 15 20 25 . 31
1"-(-)
FIGURE 4. Destructionof SE during heating of eggs in a water
bath.
FIGURE5. DestructIonof SEduring heatingof eggsin 57 C water
and holding of eggs at 55 C in air (from Hou et aI., 1996,with
permission).
In an effort to further reduce the time required to
achieve a 7-log reduction in SE, we implemented a
microwave heating step as the primary method to
rapidly achieve a come-up temperature close to the
target of 55 C. A combination microwave-hot air or
microwave-water bath heating regimen significantly
reducesthe come-up time and provided a 5-log kill in
less time than was required to achieve a 3-log kill by
either water bath or hot air heating alone (Figures6 and
7). The benefit with microwave heating is that it
preferentially heats egg yolk more than egg white,
which is strategically better becauseegg yolk is more
resistant to heat denaturation than egg white whereas
external conductive heating may denature egg white
before lethal temperaturesare reachedwithin the yolk.
Considering that naturally infected shell eggs contain
only 10 to 100 du of SE, the levels of destruction
demonstratedherein are sufficient to yield SE-negative
shell eggs in 30 min. Further efforts will be directed to
provide better heat distribution during microwave
100.tXXI.tXXI .
-@]
10,tXXI,tXXI
1.tXXI,tXXI
B
I
100,tXXI
i
1,tXXI F
100 0
0
0 20 40 ~ 8) 100 120 140
The(nn)
FIGURE 6. Desb'Uctionof SE during microwave heating and
holding in air at 56 C.
 SYMPOSIUM:SECONDOWEN J. COfiERILL EGG AND EGG PRODUCTS SYMPOSIUM 1125
~ -+- Hopper, commercial
S. A., andlayerS. Mawer,
flock. Vet.
1988. Rec.
Salmonella
123:351. enteritidis in a

-=-- Hou, H., R. K. Singh, and P. M. Muriana, 1995. Pasteurization

of shell eggs for salmonella reduction using water bath

and hot air oven heating. Proc. Inst. Food Technol. Book of

Abstracts:146.
Hou, H., R. K. Singh, P. M. Muriana, and W. J. Stadelman,
1996. Pasteurization of intact shell eggs. Food MicrobioL

(in press).
Humphrey, T. J., 199Oa. Heat resistance of Salmonella enteriti-
dis phage type 4: the influence of storage temperatures
before heating. J. Appl. Bacteriol. 69:493-497.
Humphrey, T. J., 19~. Growth of salmonellas in intact shell
eggs: influence of storage temperature. Vet. Rec. 126:292.
Humphrey, T. J., A. Baskerville, S. Mawer, B. Rowe, and S.
Hopper, 1989. Salmonella enteritidis from the contents of
FIGURE 7. Destruction of SE during miaowave heating and in~ct ~4 eggs: a study involving naturally Infected hens.
holding in 56 C water. EpldemloL Infect. 103:415-423.
Humphrey, T. J., P. A. Chapman. B. Rowe, and R. J. Gilbert,
1990. A comparative study of the heat resistance of
salmonellas in homogenized whole egg, egg yolk or
heating; it is expected that the use of pilot plant scale albumen. Epidemiol. Infect. 104:237-241.
commercial equipment may provide pasteurized shell Humphrey, T. J., A. Whitehead, A.H.L. Grow~er,. and A.
eggs in even less time. Henley, 1991. Numbers of Salmonella ententidlS In the
contents of naturally contaminated hens' eggs. Epidemiol.
Infect. 106:489-496.

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resistance of Salmonella enteritidis in refrigerated and
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Cunningham,F. E., 1995.Egg product pasteurization.Pages 1951. Methods for measuring yolk index. Poultry Sci. 30:
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Stadelmanand O. J. Cotterill, ed. Haworth Press, Bin- Sourby, J. C., W. F. Kohl, and R. H. Ellinger, 1971. Process of

ghamton, NY. pasteurization of whole eggs. U.S. Patent No. 3,573,935.

Holley, R. A., and M. Proulx, 1986.Use of egg wash water pH Van Uth, L.A.J.T., F. F. Putirulan, and RW.A.W. Mulder, 1995.

to preventsurvival of SalmoneliQat moderatetemperature. Pasteurization of table eggs to eliminate Salmonella.

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