EGGS
Contents
Microbiology of Fresh Eggs
Microbiology of Egg Products
Microbiology of Fresh Eggs
NHC Sparks, SRUC, Scotland, UK
Ó 2014 Elsevier Ltd. All rights reserved.
Eggs are one of the few foods that can pass from the farm
to the consumer with minimum treatment. In some
countries, such as the United Kingdom, even the washing
or sanitizing of the shell is prohibited if the egg is to be
sold as a Grade A product. The ability of the chicken to
produce a food that can be stored for up to 3 weeks
without adverse effects on its eating quality or bacterio-
logical safety is an indication of the complex antimicrobial
systems that have evolved to protect the egg, and in
particular the yolk, from both pathogens and spoilage
organisms. The ability of microorganisms to adapt,
however, as evidenced by the impact of Salmonella enter-
itidis on egg production in the United Kingdom and more
recently in the United States, poses a constant challenge to
the safety of fresh eggs as a food product.
Structure and Composition of Fresh Eggs
The hen’s egg is formed in the ovaries and oviduct (see
Figure 1). The oviduct is some 60 cm in length and for func-
tional purposes is divided into the infundibulum or neck, the
Immature
ova Magnum
(albumen deposition 3 h)
Mature
ova
Infundibulum
Figure 1 Schematic diagram of the reproductive organs of the hen.
610 Encyclopedia of Food Microbiology, Volume 1
magnum, isthmus, uterus or shell gland, and the vagina. The
ova or yolk is formed over a period of approximately 9 days.
The constituents (approximately 16% protein, 34% lipid, 0.1%
carbohydrate, and 1% ash) are transported via the bloodstream
to the ovaries, where the material is taken up and contained
within the perivitelline membrane. Following its release, the
yolk should be guided into the oviduct by the infundibulum
and from there begins its passage down the oviduct.
Immediately after its entry into the oviduct, the second
vitelline membrane is deposited and then, on entry to the
magnum, albumen deposition begins. The albumen is laid
down in three distinct layers: the inner and outer, thin albumen
differing from the more viscous middle, thick albumen in the
amount of the protein ovomucin; the percentages of ovomucin
are approximately 1.2% and 7.5% in the thin and thicker
albumens, respectively. With this exception, the different
albumen layers are similar in composition, consisting of
approximately 88% water, 10% protein, 0.03% lipid, 0.6%
carbohydrate, and 0.5% ash. The egg spends approximately 3 h
in the magnum before moving on to the isthmus, where the
sheet-like limiting membrane is deposited, followed by two
fibrous shell membranes. The fibers lie parallel to each other
Shell gland
(shell formation 20 h)
Vagina
Cloaca
Isthmus (shell membrane
formation 1 h)
http://dx.doi.org/10.1016/B978-0-12-384730-0.00089-6
 EGGS j Microbiology of Fresh Eggs 611

Figure 2 Radial section of the fibrous egg shell membranes showing the relative thin fibers of the inner membrane and the thicker fibers of the outer
membrane.

and are arranged in a random manner within the tangential

plain (see Figure 2).
The fibers of the inner membrane, which oppose the
limiting membrane, differ from those in the outer-shell
membrane only in that they are thinner (<2 microns
cf <3.6 microns) and more tightly packed. The inner
membrane is approximately 20 microns thick, whereas the
outer membrane is thicker, at approximately 50 microns.
Towards the end of the hour that the egg spends in the isthmus,
water is taken up by the albumen. This process, called
‘plumping’ continues throughout the early stage of the shell
formation in the shell gland (or uterus).
The egg spends some 18 h in the uterus, that is, approxi-
mately 75% of the total time it spends in the oviduct. Once the
initial layer of shell has formed across the surface of the outer-
shell membrane, the plumping process ceases. The shell
consists of 98% calcium carbonate in the calcite form and 2%
organic matrix (see Figure 3). Traversing the shell are between
7000 and 17 000 trumpet-shaped pores that are approximately
10 microns in diameter. These pores are essential in the fertile
egg for the exchange of respiratory gases. Immediately before
oviposition, the organic cuticle is deposited. This process forms
a relatively thin (0.5–13 microns) layer over the shell that is
normally 300–400 microns thick. Where the cuticle bridges the
mouth of a pore canal, it forms a loose plug, rather like a loose
cork in the neck of a bottle.

Antimicrobial Defense Systems

Physical Defense
The egg’s antimicrobial defense mechanisms are both physical
and chemical in nature. If we consider bacteria located on the Figure 3 Radial section of hen egg shell showing the cuticle (C), pore
surface of the shell, the cuticle presents the first line of defense. canal (PC), and shell membranes (SM).
612 EGGS j Microbiology of Fresh Eggs
Figure 4 Salmonella on the inner surface of the shell’s limiting
membrane.
Immediately following oviposition, the cuticle has a fragile,
spongelike, moist structure. While in this condition, any
bacteria that come into contact with the surface of the shell will
be rapidly translocated by the water associated with the moist
cuticle and underlying pores, through the shell to the shell
membranes (see Figure 4). Normally, however, the cuticle
would have dried before bacteria come into contact with it.
Under these circumstances, the bacteria would tend to be
confined to the relatively dry and hostile environment of the
shell surface. Because of this environment, Gram-positive
bacteria are found more commonly on the shells of eggs (e.g.,
Micrococcus, Bacillus, Escherichia, and Staphylococcus) although
Gram-negative organisms are also routinely isolated (e.g.,
Aerobacter, Cytophaga, and Flavobacterium).
Once the cuticle has dried, probably the most common
cause of bacteria being drawn through the shell is the presence
of water on the shell and in the pore canals. This can come
about either through condensation forming on the shell (so-
called ‘sweating’) or as a result of the egg being washed or
sanitized.
Fungal growth on the shell tends to occur only when the
eggs are held at relatively high levels of humidity (>80% RH).
The following species have been reported to be associated with
shell eggs: Aspergillus, Penicillium, Cladosporium, Rhizopus, and
Mucor. Once fungi have colonized the shell’s surface, the pores
can be penetrated relatively easily by the hyphae.
Although the shell remains intact, microorganisms are
forced to traverse the pore canals; however, once the shell is
cracked, it may provide very little protection and, consequently,
gross contamination of the egg contents can be extremely rapid.
The fibrous shell membranes that form the foundation for,
and hence are crucial to, the correct formation of the overlying
shell offer relatively little defense against microorganisms.
Studies have shown that bacteria can grow within the
membranes, the environment favoring Gram-negative over
Gram-positive organisms. Ultimately, the growth of contami-
nants in the membranes is limited by a combination of the
presence of the limiting membrane and the bacteriostatic
nature of the albumen. If contamination of the albumen is to
occur, bacteria must pass through the limiting membrane.
Whether this is achieved by organisms degrading the limiting
membrane or passing through naturally occurring holes in the
membrane is uncertain; however, once the organisms have
Number (log10) cfu/ml albumen
5
4.5
4
pH 8.54
3.5 pH 9.61
3
2.5
2
0 5 10 15 20 25 30
Time (h)
Figure 5 The effect of albumen pH on the growth of S. typhimurium
when incubated in vitro, at 37.5  C.
passed through the limiting membrane, they are presented with
the hostile environment of the albumen, which separates the
yolk (which is rich in nutrients and has little, if any, inherent
antimicrobial properties) from the shell.
The albumen’s viscosity, or physical defense, is the result of
the interaction between the proteins ovomucin and lysozyme
at neutral pH. However, during the days that follow oviposi-
tion, the loss of carbon dioxide from the albumen by diffusion
brings about an increase in the pH. As the pH rises, the inter-
action between ovomucin and lysozyme decreases, and the
viscosity is lost. This is important in the fertile egg for the
successful development of the embryo. Although the antimi-
crobial benefits of the high viscosity are lost, the increased pH
increases the efficacy of the chemical defense provided by the
numerous antimicrobial proteins in albumen (see Figure 5)
These are discussed in the following sections.
Chemical Defense
Evidence is emerging that the cuticle of chicken eggs and
probably the cuticle of the eggs of at least a related species of
bird have antimicrobial chemical properties and not just the
more commonly recognized physical antimicrobial properties.
For example, lipophilic compounds that have been extracted
from the cuticle are active against Gram-positive and Gram-
negative bacteria. Similarly, porphyrins in the cuticle have been
associated with the photoinactivation of Gram-positive
(Staphylococcus aureus, Bacillus cereus) organisms.
It has long been recognized that the albumen contains
a large number of antimicrobial proteins. More recently,
similar proteins have been identified in the shell and shell
membranes. For example, lysozyme has been isolated from the
sheetlike limiting membrane that forms a barrier between the
fibrous shell membranes and the underlying albumen. Simi-
larly, lysozyme has been identified in the fibrous shell
membranes, the shell, and the cuticle. Other proteins that may
have antimicrobial proprieties have been isolated from the
shell of hens’ eggs include ovotransferrin and ovocalyxin-36.
Although the lysozymes are probably the best known of the
albumen’s antimicrobial proteins, they may be less efficacious
than the protein ovotransferrin. Lysozyme acts on the beta-
(1-4) glycosidic bond between N-acetyl glucosamine and
N-acetylmuramic acid in the water-insoluble peptidoglycan of
eubacterial cell walls, whereas ovotransferrin, as the name
suggests, chelates a number of metal ions, including iron. By

making iron unavailable to bacteria, the ability of microor-
ganisms to replicate is restricted. The importance of ovo-
transferrin’s ability to bind the available iron within the
albumen is exemplified by experiences in the United States.
There, eggs that had been washed and sanitized were rotting in
relatively large numbers when held in store. Upon investiga-
tion, it was shown that the increased incidence of rots resulted
from the eggs being washed in water containing relatively high
levels (>4 ppm) of iron. The wash water was penetrating the
shell and providing sufficient iron to negate the effect of
ovotransferrin.
Other proteins, such as ovomucoid, ovoinhibitor, ovo-
flavoprotein, and avidin will inhibit trypsin, inhibit proteases,
chelate riboflavin, and chelate biotin, respectively.
The proportions and efficacies of the proteins in albumen
vary according to the species. Thus, it has been shown that
while ovotransferrin and ovalbumin were present in the
albumen of the chicken, turkey, duck, and goose, c-type lyso-
zyme was not present in the goose-egg albumen. The higher
concentrations of ovotransferrin and the broad-acting c-type
lysozyme resulted in the albumen of the chicken being more
antimicrobially effective than that of the goose.
Under normal production and storage conditions, the phys-
ical and chemical defense systems combine to delay the growth of
contaminants for about 21 days. Even when abused, for example,
by inoculating bacteria onto the shell membranes and incubating
the egg at 37  C, the egg’s antimicrobial systems prevented (see
Figure 6) gross contamination for more than 12 days.
The mechanisms that result in this delay are, however, the
subject of debate. It is generally agreed that the quiescent
period is terminated when the contaminants make contact with
the nutrients originating from the yolk. Although some
researchers contend that growth occurs following penetration
of the vitelline membrane by contaminants, others postulate
that it is the leeching of iron and nutrients from a deteriorating
membrane that allows the onset of a rapid growth of the
contaminants.
Contamination of Eggs with Salmonellae
Pathogens recovered from eggs in the past have included
species of Aeromonas, Campylobacter, Listeria, and Salmonella.
12
Number (log10) cfu/membrane
10
or ml of albumen
8 secondary outbreaks.
4
Membranes
2 Albumen
0
0 5 10 15 20
Time (d)
Figure 6 The growth of a mixed culture in the shell membranes and
subsequent growth within the albumen of an egg incubated at 37.5  C.
EGGS j Microbiology of Fresh Eggs 613
However, in terms of reported outbreaks of illness attrib-
uted to eggs only Salmonella is of significance. Shells of eggs
have been reported to be contaminated with a range of
Salmonella spp., including S. anatum, S. bareilly, S. enteritidis,
S. derby, S. essen, S. heidelberg, S. montevideo, S. oranienburg,
S. thompson, S. typhimurium, and S. worthington. The normally
dry condition of the surface of the ‘nest-clean’ (i.e., free of
visible contamination) shell means that in practice most
Salmonella spp. die relatively soon after they contaminate
the shell.
Until the 1980s, salmonellosis associated with hens’ eggs
was relatively infrequent. Duck eggs had long been implicated
in salmonellosis outbreaks, presumably because of the envi-
ronment in which they were produced. Therefore, concerns
were raised in the United Kingdom when in the late 1980s an
increase in the incidence of salmonellosis was attributed to
hens’ eggs and specifically an increase in outbreaks due to
S. enteritidis. In the last 3 weeks of November 1988, for
example, this organism accounted for 1167 or 57.2% of the
salmonellae identified in reports, although eggs were not
implicated in all outbreaks caused by S. enteritidis. Of these,
890 reports were of outbreaks that involved S. enteritidis type 4
(PT4). In 1997, more than 32 000 salmonella infections were
reported in England and Wales, an increase of 11% from the
previous year. During the same period, S. enteritidis PT4
infections rose by more than 2000 (16%), and infections
associated with other S. enteritidis phage types rose by 2500
(48%); and infections associated with S. typhimurium and
other salmonellas fell by 16% and 9%, respectively. More
recently, eggs accounted for most of the 3578 cases of S.
enteritidis acquired from foods reported in the United States
between May 1 and November 30, 2010. As of 2011, the US
Department of Health and Human services had noted that
‘one in 10 000 eggs may be contaminated with Salmonella
inside the egg shell’.
It has been suggested that, by adapting to the conditions
found in the oviduct or ovaries, S. enteritidis PT4 has managed
to circumvent many of the egg’s natural antimicrobial systems;
unlike, for example, S. enteritidis PT13A, which is more
commonly associated with fecal contamination. However,
studies have shown that the correlation between the number of
hens infected with S. enteritidis and the number of infected eggs
laid is variable. For example, in one study of infected flocks, the
fraction of eggs whose contents tested positive ranged from
0.1–1.0%. Furthermore, because Salmonella spp. are commonly
associated with both red and white meats and dairy products,
as well as eggs, cross-contamination can occur postproduction
and, in particular, in the home. Poor hygiene can also result in
Implications for Human Health
The common clinical features of salmonellosis are diarrhea,
vomiting, and fever, but infection may result in symptoms
ranging from mild gastroenteritis to septicaemia or death.
Although salmonellae are transmitted predominantly in
foodstuffs, cooking usually kills the organisms. The rise in the
United Kingdom in the late 1980s in the reported numbers of
infections attributed to salmonella in eggs or egg products
614 EGGS j Microbiology of Fresh Eggs
culminated in the chief medical officer advising consumers to
stop eating raw eggs and food containing uncooked eggs.
Furthermore, it was recommended that those who could be
considered vulnerable, such as the sick, elderly, pregnant
women, and babies, should only eat eggs when they had been
cooked sufficiently to solidify the yolk and albumen. At that
time, the dominant causal organism was S. enteritidis. Data
for the period July to September 1998 show that S. enteritidis
accounted for 80.4% of a total of 353 outbreaks attributed to
salmonellas. Of the outbreaks caused by S. enteritidis, 60.9%
of these were due to S. enteritidis PT4. S. typhimurium
accounted for 44 of the 69 outbreaks caused by salmonellas
other than S. enteritidis. Although eggs were not identified as
the suspect vehicle of infection in all of the outbreaks caused
by S. enteritidis, foods incorporating eggs, such as mayon-
naise, egg sandwiches, egg fried rice, or mousse are listed
frequently. Part of the UK egg industry’s response to the rapid
rise in salmonella infections linked to eggs was the intro-
duction of a Salmonella vaccination program for laying hens.
This had a marked effect on the number of eggs testing
positive for Salmonella. For example, by 2011, UK (England
and Wales) data showed that although S. enteritidis still
accounted for most of the 1020 reported cases of salmonel-
losis in August of that year, it was only 29.4% of the isolates;
and of the S. enteritidis isolates, only 13.3% were S. enteritidis
PT4. In contrast to the situation in the late 1990s,
S. typhimurium accounted for 28.7% of the 1020 reported
cases of salmonellosis in August 2011. A somewhat similar
split between these serotypes was reported for US isolates in
2009, by the US Centers for Disease Control and Prevention,
with S. enteritidis accounting for 17.5% of the nearly 50 000
isolates, the next nearest and S. typhimurium being 15% of
the total.
Reducing Infection of Flocks and the Risks in Storage
Eggs may become contaminated with microorganisms through
either the vertical (i.e., infection of the ovaries or oviduct) or
horizontal (i.e., cross-contamination due to dust, fecal mate-
rial, etc.) routes.
Although the vertical transmission of viruses (e.g., Onco-
viridae, paramyoviruses, picornavirus) and Mycoplasma spp.
(e.g., M. meleagridis, M. gallisepticum, M. synoviae, or M. iowae)
can have a major impact on poultry production, these organ-
isms do not affect the human population. The vertical trans-
mission of food-poisoning bacteria has been largely restricted
to S. enteritidis, although S. typhimurium serotypes have infected
the ovaries.
Organisms associated with the contamination of eggs by
horizontal transmission are far more numerous. Spoilage
organisms that have been recovered from eggs include species
of Pseudomonas, Aeromonas, Acinetobacter, Alcaligenes, Cit-
robacter, Cloaca, Escherichia, Hafnia, Proteus, and Serratia. Path-
ogens recovered from shells include a wide range of
salmonellas (e.g., S. heidelberg, S. montevideo, S. typhimurium,
S. enteritidis, S. bareilly), Campylobacter spp., Listeria spp., and
Aeromonas spp. However, in the past 20 years it is the upsurge of
infections resulting from S. enteritidis that has been notable,
with S. enteritidis PT13A being more often associated with fecal
contamination of the shell than infection of the ovaries, and so,
probably, often being transmitted horizontally.
Control measures designed to reduce the risk of product
contamination must therefore encompass two approaches.
First, they should ensure that replacement laying hens are free
of the microorganisms that would be of concern and, secondly,
the risk of infection of the housed birds or cross-contamination
of the product must be minimized.
To understand the control measures, it is necessary to
consider the operation of the commercial production process.
In brief, day-old chicks hatched in a dedicated layer hatchery
will normally be reared either on the floor (the majority of UK
birds are reared in this way) or in cages. Birds will be reared at
dedicated rearing sites until they are about 16 weeks old, when
they are approaching sexual maturity. The bird are then referred
to as being at ‘point-of-lay’, and will be transferred to a laying
farm.
In Europe, eggs are produced using a number of systems,
including cage, barn, free range, and organic. These systems of
production have remained relatively unchanged for decades.
However, from 2012 European regulations require that hens
no longer be housed in the system of choice for most egg
producers, the conventional barren cage. If producers want to
continue to house hens in cages, then they have to replace the
conventional barren cage with the so-called enriched or
modified cage. This cage design differs from that of the barren
cage in a number ways, including the requirements for
provision of a nest box area, scratch mat area, perches, and,
generally, more space (vertical and horizontal) per bird. In
practice, the colony size has also increased from 4 to 6 up to
60, or in some cases, 80 birds per cage. Although many
producers have or will convert from conventional to enriched
cages, a considerable number will have converted to free-range
production by 2012. For example, in the United Kingdom, in
the year 2000, the typical recorded percentages of table eggs
produced from cage, barn, free-range, and organic systems
were, respectively, 74%, 8%, 18%, and <1%. Comparable
figures for 2011 were 48%, 4%, 44%, and 4%, respectively. In
contrast, in the United States, approximately 95% of laying
hens are housed in cages; other countries also have little or no
alternative to the cage-laid egg.
Irrespective of the production system used, the pullet will be
stimulated into lay by increasing the number of hours of light
that the bird is exposed to in a 24 h period. Once in lay, hens
will typically be kept until they are 70–76 weeks old. Then, the
housing will be depopulated and cleaned before being
restocked.
Measures aimed at reducing the risk of contamination of
the product are often targeted at salmonellae, these being
particularly high-profile organisms as far as egg products are
concerned. In Europe, the control of Salmonella in laying hens
(and some other farmed species) is being coordinated at the
level of the European Union. For example, Regulations (EC)
No. 2160/2003 and (EC) No. 1168/2006 are designed to
ensure coherent action to reduce Salmonella serotypes consid-
ered to be of human health significance (S. enteritidis and
S. typhimurium) across the member nations of the European
Union.
In the United Kingdom, the related National Control Pro-
gramme (NCP) for Salmonella in laying hens was implemented

on February 1, 2008. To minimize the risk that eggs could
present to public health, the NCP required that,
from 1st January 2009, eggs originating from flocks infected with
Salmonella Enteritidis or Salmonella Typhimurium cannot be sent for
human consumption unless they are treated in a manner that will
guarantee the elimination of Salmonella (i.e. pasteurisation/heat
treatment).
The UK NCP is supported by other legislation and codes
of practice aimed at reducing the opportunity for Salmonellas
spp. to enter the production unit. For example, there are
codes and legislation that cover the production and testing
of chicks, feed, and the control of vermin and, in particular,
rodents.
It is advisable that replacement pullets should be vaccinated
against S. enteritidis PT4. Before day-old chicks are placed in the
rearing house, the house should be checked for S. enteritidis,
with the area being resanitized if a positive result is obtained.
Standard biosecurity measures should be adopted, including
the use of footbaths, operation of an effective rodent control
program, and the wearing of protective clothing by all
employees. The risks associated with either people, vehicles, or
materials coming on site and acting as vectors for microor-
ganisms, such as S. enteritidis are substantial. Therefore, the
number of visitors to the site should be minimized, and those
who do visit should wear protective clothing. Any vehicle
coming on to the site should be cleaned externally, and the
wheels and lower portion of the vehicle sprayed with a sani-
tizer. The feed should be treated to minimize the risk of
S. enteritidis contamination. This can be achieved in a number
of ways – two of the more common techniques being heat
treatment of the feed (mash) or the addition of an organic acid.
The use of heat (e.g., 85  C for 3 min or 75  C for 6 min) can
achieve a total kill of Enterobacteriaceae and molds when
either group of organisms is initially present at a level
of 106 cfu g1.
Before the point-of-lay pullets can be transferred from the
rearing to the laying farm, a statistically valid number of birds
should be tested for S. enteritidis by taking cloacal swabs. Once
the laying house has been tested and shown to be negative for
S. enteritidis, the point-of-lay pullets can be housed. Strict bio-
security is imperative as most commercial sites are multiage –
that is, the poultry houses on a site will contain flocks, each
in a separate house, that range in age from approximately 16–76
weeks. Measures such as those outlined earlier for rearing sites
should be adopted to minimize the risk of cross-contamination.
Depending on the system, eggs may be laid in a range of
environments. Cage eggs can be laid onto an inclined wire floor
that causes the egg to roll away to the front or rear of the cage,
away from the bird. The eggs would normally roll onto a belt,
which conveys the egg, via a series of lifts and belts, to the egg
store or packing station. Eggs that are produced on barn or free-
range systems are normally laid into a nest box, the require-
ment in Europe being that there be ‘one nest for every 7 birds or
1 square meter of nest space for every 120 birds’. Depending
on the design of the nest box, eggs may be collected manually
or, as in the cage systems described earlier, automatically. If
collected manually, the eggs are normally laid on to either
EGGS j Microbiology of Fresh Eggs 615
white wood shavings or similar material, or plastic turflike
matting. Automated systems can also use plastic matting or
a similar material, the main criteria being that the eggs will roll
over the surface and that the matting is not lost from the nest
box as the egg moves on to the belt.
At the moment the egg emerges from the bird, it is warm
(w41  C) and moist. The moisture is due to the cuticle, which
at this stage has an ‘immature structure’ (see section on
bacterial defense). In essence, the presence of water within the
cuticle, combined with the open structure, allows bacteria to
penetrate the egg, to the level of the membranes, in relatively
large numbers. It is therefore essential that the environment
into which the egg is laid contains as few pathogens and
spoilage organisms as possible.
The move from cages to the extensive systems of egg
production is being led by member countries of the Europe
Union, but it is likely to be adopted in other countries in years
to come. Although the pressure for conventional cages to be
banned in the European Union was driven by welfare
concerns, it has been noted that the move could have a dele-
terious effect on the microbiological quality of table eggs.
Although the barren cage does not fulfill the needs of the
laying hen, it does enable rapid removal of the egg from the
environment in which the hen lives and thus minimizes,
relative to other systems of production, opportunities for
cross-contamination to occur following lay. This argument has
been examined by a number of researchers. Although it has
been reported that ‘contamination of eggshells with aerobic
bacteria is generally higher for nest eggs from non-cage
systems compared to nest eggs from . cages’ it is commonly
reported that the differences in contamination are greater
when the comparison is made using hens housed in experi-
mental facilities, rather than hens housed in commercial
production units. In the limited studies that have been con-
ducted to assess whether, compared with cage systems,
extensive systems pose a greater risk to the laying hen of
Salmonella infection the evidence has been reassuring. That is
to say, within the limitations of the studies, there was no
evidence that the risk of salmonella infections increased if
birds were housed in extensive systems. This said, whether or
not the move from cage to extensive systems of egg produc-
tion, such as free-range, will present a greater challenge to the
bacterial defense mechanisms of the table egg.
Once laid, the risk of cross-contamination from other hens
or other eggs should be minimized by removing the egg as
soon as is feasible from the bird, and moving the egg to either
a store or the packing station. The main contaminants isolated
from the shell of hen’s eggs have been shown to be species of
Micrococcus, Achromobacter, Aerobacter, Alcaligenes, Arthrobacter,
Bacillus, Cytophaga, Escherichia, Flavobacterium, Pseudomonas,
and Staphylococcus. These bacteria are associated with dust,
feces, and soil and reflect the relatively dry environment of the
shell. To minimize the incidence of these contaminants, staff
handling eggs need to wash their hands before and after col-
lecting eggs; segregate (and handle separately) ‘nest clean’ and
dirty, cracked, or broken eggs; and collect eggs on to visibly
clean trays.
Whether eggs are collected from egg stores and taken by
road to the packing station or conveyed directly from the
poultry house to the packing station, care must be taken to
616 EGGS j Microbiology of Fresh Eggs
ensure that the temperature that the eggs are exposed to
remains constant and above 5  C but below 20  C. This is
important as it is a means of controlling the growth of organ-
isms within the egg and because it reduces the risk of
condensation forming on the shell. In the egg industry
condensation, or ‘sweating’ as it is referred to colloquially, can
occur on the shell when eggs are moved out of cool stores into
a warmer environment. Water on the shell is of particular
concern because of the ease with which bacteria, in the presence
of water, can move through the pores of the shell. If conden-
sation is allowed to remain on the shell for prolonged periods,
the risk of fungal (e.g., Cladosporium spp.) growth on the shell
becomes significant.
Although the washing of Grade A eggs is forbidden in the
United Kingdom, egg washing or sanitizing is common practice
in other parts of the world. If eggs are to be sanitized, it is
important that certain criteria are met, because water can
facilitate the movement of bacteria through the shell. These
criteria include ensuring that the wash water is maintained at
a constant temperature of w42  C; the temperature of the eggs
is less than that of the wash water; the difference between the
egg and water temperatures is not greater than w35  C, as
a greater temperature difference will increase the incidence of
shell cracks; and that the sanitizing solution always contains
sufficient active sanitizer.
Recommended conditions for the storage of table eggs on
the farm or at the packing station are <20  C (typically 15  C)
and approximately 75% RH. If they are to be stored on the
farm, it is good practice to ensure that eggs are transported to
the packing station as soon as possible after lay and within
a maximum of 3 days.
Once in the packing station, the eggs are graded. As of 2011,
eggs sold in the European Union were classified as either Grade
A or B.
Grade A eggs are the highest grade. They are naturally clean, fresh
eggs, internally perfect with shells intact and the air sac not exceeding
6 mm in depth. The yolk must not move away from the center of the
egg on rotation. Grade A eggs are sold as shell eggs. Grade B eggs are
broken out and pasteurized. Industrial eggs, which are for nonfood
use only, are used in products such as shampoo and soap.
Grading consists of removing those with visible signs of
contamination on the shell; ‘candling’, that is, shining a bright
light through the egg to allow an operator to detect and remove
eggs with inclusions, cracked shells, and other imperfections;
and sorting according to weight, stamping, and packing. All
Class A eggs are stamped or marked with a code that defines
the farming system (i.e., 0 ¼ organic, 1 ¼ free range, 2 ¼ barn,
3 ¼ cage), country of origin, and production unit. Following
packing and boxing or film-wrapping on a pallet, the eggs are
held in store (as described) and dispatched as rapidly as
possible. Among other information, such as the packing station
details, the packaging should show the ‘Best before date’. This
date is a maximum of 4 weeks from the time of lay.
See also: Eggs: Microbiology of Egg Products; Natural
Antimicrobial Systems: Lysozyme and Other Proteins in Eggs;
Salmonella: Salmonella Enteritidis.
Further Reading
Anon, 2001a. Second Report on Salmonella in Eggs. FSA, London.
Anon, 2011b. Summary of Lion Quality Code of Practice. British Egg Industry Council,
London. http://www.lioneggs.co.uk/files/lioneggs.co.uk/pdfs/LionCodeSummary.
pdf (accessed at 20.05.11.).
Board, R.G., 1966. Review article. The course of microbial infection of the hen’s egg.
Journal of Bacteriology 29, 319–341.
Board, R.G., Fuller, R. (Eds.), 1994. Microbiology of the Avian Egg. Chapman and Hall,
London.
Board, R.G., Sparks, N.H.C., Tranter, H.S., 1986. Antimicrobial defence of the avian egg.
In: Gould, G., Rhodes-Roberts, M.E., Charnley, A.K., Cooper, R.M., Board, R.G. (Eds.),
Natural Antimicrobial Systems. Bath University Press, Bath, pp. 82–96.
Duguid, J.P., North, R.A.E., 1991. Eggs and salmonella food-poisoning: an evaluation.
Journal of Medical Microbiology 34, 65–72.
Gantois, I., Ducatelle, R., Pasmans, F., Haesebrouck, F., Gast, R., Humphrey, T.J., Van
Immerseel, F., 2009. Review article. Mechanisms of egg contamination by
Salmonella enteritidis. FEMS Microbiology Reviews 33, 718–738.
Holt, P.S., Davies, R.H., Dewulf, J., Gast, R.K., Huwe, J.K., Jones, D.R., Waltman, D.,
Willian, K.R., 2011. The impact of different housing systems on egg safety and
quality. Poultry Science 90 (1), 251–262.
Humphrey, T.J., 1994. Contamination of egg shell and contents with Salmonella
enteritidis: a review. International Journal of Food Microbiology 21, 31–40.
Van Hoorebeke, S., Van Immerseel, F., Haesebrouck, F., Ducatelle, R., Dewulf, J.,
2011. The influence of the housing system on salmonella infections in laying hens:
a review. Zoonoses and Public Health 58 (5), 304–311.