289

J. Milk Food Techno/. Vol. 39, No. 4, Pages 289-296 (April, 1976)
Copyright © 1976, International Association of Milk, Food, and Environmental Sanitarians

Public Health Aspects of

Cream-filled Pastries. A Review
FRANKL. BRYAN
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U.S. Department Health, Education and Welfare, Public Health Service

Center for Disease Control, Bureau of Training
Atlanta. Georgia 30333

(Received for publication September 8, 1975)

ABSTRACT Other foods

In the United States food borne disease outbreaks for which cream- and mixtures*
filled pastry was identified as the vehicle have declined from 17.8% in Egg and egg products
Journal of Milk and Food Technology 1976.39:289-296.

the 1930's to 2.3o/oin the 1970's. Cream fillings or cream-tilled pastries

Milk and milk
were usually contaminated with staphylococci and Salmonella typhi by
products
workers and with salmonellae by ingredients such as eggs and milk.
These contaminants multiplied as a result of favorable nutrients, water Potato and
activity, temperature, and pH; and they survived the effects of macaroni salad Beef
competing organisms and processes. Prevention and control of such Pork
outbreaks have been based on formulating the product so it will not
mpport bacterial growth, using pathogen-free ingredients, thorough Cream-filled Combinations
cooking and reheating, sanitary handling of fillings and finished pastry, pastry
rapid cooling and storing at low temperature, establishing Chicken Turkey
microbiological standards for the finished products, training
*59 outbreaks in which the incriminated food was not determined
food-processing and food-service personnel, and educating the have been om1tted.
consumer to refrigerate products after purchase.
Figure 1. Foods incriminated in staphylococcal food poisoning
outbreaks reported from 1961 to 1971.
EPIDEMIOLOGY
TABLE 2. Diseases conveyed by contaminated cream-filled pastry in
Cream-filled pastries have a notorious history of being the United States (selected periods from 1938 to 1972 in which
vehicles of food borne illnesses, particularly staphylococ- surveillance data was available and outbreaks reported in literature
cal food poisoning (16, 18, 44). If this history is examined from 1916)
Number of
for years in which records are available, a decreasing Disease Outbreaks Percent
percentage of outbreaks in which cream-filled pastries Staphylococcal intoxication 374 65.3
were vehicles occurred during each successive decade Salmonellosis (caused by various
serotypes) 55 9.6
(fable 1)_ From 1961 to 1971, for instance, cream-filled 6 1.0
Typhoid fever
Enterococcal gastroentritis 3 0.5
TABLE 1. Percent of foodborne disease outbreaks in which 1 0.2
Viral hepatitis
cream ;tilled pastries were vehicles in reported outbreaks from I 938 to
Food borne illness of unknown
1973a 134 23.4
etiology
Outbreaks Total 573
Years Number Total Pereent
1938,1939 42 236 17.8 losis, a few outbreaks of typhoid fever and enterococcal
1941-1949 430 2702 15.9
1950,1952-1959 149 2064 7.2
gastroenteritis, and one outbreak of viral hepatitis were
1960-1969 111 2601 4.3 also attributed to these vehicles_ A number of outbreaks
1970-1973 30 1284 2.3 were classified as unknown etiology. Many of these
aoata for 1940 and 1951 unavailable. reports gave clinical pictures typical of staphylococcal
blncludes outbreaks in which vehicles were and were not detected. intoxication, but they contained insufficient laboratory
pastries were vehicles in only SO (9.So/o of) reported confirmation to classify the disease.
outbreaks of staphylococcal intoxication (Fig. 1).
FACTORS CONTRIBUTING TO OUTBREAKS
Whereas in previous decades they were usually the most
commonly reported vehicles of this disease (J 8). Conditions necessary for cream-filled pastries to
For the years covered in Table 1, cream-filled pastries become vehicles for foodborne pathogens and to allow
were frequently vehicles of staphylococcal intoxication these pathogens to multiply to such an extent that illness
outbreaks (fable 2). A number of outbreaks of salmonel- results when they are ingested are: (a) pastries or their
 290
ingredients become contaminated with pathogens; (b)
they contain nutrients which support growth of
pathogenic bacteria; (c) the filling or the cake or crust has
a water activity that is high enough to permit growth of
pathogenic bacteria or the water activity differential of
these causes migration of water to create pockets of
moisture that permit such growth; (d) pH of the filling is
such that pathogenic bacteria can survive and can
multiply; (e) oxidation-reduction potential of the filling
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or topping is within a range so that pathogenic bacteria
can initiate growth; ~1 temperatures at which the filling
or the finished pastries are held are within a range that
pathogenic bacteria multiply for sufficient time to permit
development of large numbers of these bacteria or
elaboration of enterotoxins; (g) pathogenic bacteria can
successfully compete with non-pathogenic microbial
flora in the product; and (h) pathogenic bacteria (or
toxins) must survive all operations to which they are
exposed.
Journal of Milk and Food Technology 1976.39:289-296.
If these conditions are met and the cream-filled pastry
is ingested by susceptible persons, foodborne illness will
result. The likelihood of the eight conditions occurring
can be assessed by looking at each in greater detail.
Sources of contamination
Foodborne pathogens that reach cream filling or
pastry made from such filling come from two major
sources~workers and foods of animal origin. The
relative importance of sources of contamination of
cream-filled pastry as indicated by outbreak
investigations is shown in Table 3. Enterotoxogenic
TABLE 3. Factors contributing to 367 outbreaks in which
cream-jilled pastries were vehicles (covers periods from 1920's to 1972)a
Inadequate n"n"'"ra1nnn
Infected worker 91
Prepared a day or more before serving 82
Insanitary plant 27
Workers with poor personal hygiene handling
food 19 5.2
Inadequately cleaned equipment 17 4.6
Contaminated raw ingredients (eggs and milk) 15 4.1
Cooking or reheating failures 12 3.3
Rodent contamination(?} 5 1.4
construction 4 1.1
2 0.5
a Many reports did not give complete information of the factors that
contributed to the outbreak, and laboratory analysis was often not
done.
strains of Staphylococcus aureus are usually introduced
into cream fillings by infected workers after the pastry
has been cooked. The workers may have infected burns
or cuts on their hands or they may have boils; but usually
they have no lesions, they just carry the staphylococci in
their nares (23, 34). In a few outbreaks reported before
1950, staphylococci were introduced into fillings when
raw milk was added.
Salmonellae have frequently entered cream fillings or
custards with raw ingredients. Broken, cracked, or
BRYAN
checked eggs and unpasteurized frozen and dried eggs
have been the main sources. Other raw ingredients such
as cocoa, dry milk, or coconut, however, may also be
contaminated with salmonellae. Cross contamination of
cream from contaminated dried eggs was suggested as
the source of Salmonella typhimurium in creamfilled
sponge cakes that were epidemiologically and laboratory
incriminated during an outbreak investigation (15).
In reports made in the 1920's and 1930's, rodents were
presumed to be sources of salmonellae; but these reports
appeared in a period when presence of certain serotypes
of Salmonella in foods was attributed to rodents by some
investigators whether or not there was epidemiologic or
laboratory evidence to support such a hypothesis. This
hypothesis has not been substantiated in recent years.
Hepatitis-A virus and Salmonella typhi have been
introduced into cream fillings after cooking during
handling by workers.
Nutrients
Cream fillings used in pastries may be made of eggs,
milk, shortening, sugar, cornstarch or flour, salt, vanilla,
and water or of just a "synthetic'' mix consisting of
homogenated vegetable oil, emulsifying agents, sugar,
salt, and water. If the water activity is high enough, the
first type of filling and some brands of the second type of
filling will support growth of S. aureus (13), Salmonella.
and other foodborne pathogenic bacteria. S. aureus
requires up to eleven amino acids, and thiamine and
nicotinic acid to grow, but salmonellae only require
simple sugars and inorganic nitrogen compounds to
grow. When water was substituted for milk when
reconstructing dry-mix pudding, S. aureus growth was
inhibited (13). When milk, eggs, or butter was added to
synthetic cream fillings, staphylococcal growth was
enhanced (13, 17, 22).
Water activity
Availability of water in a food or medium to
microorganisms is known as water activity <aw). The
water activity value is the point where the relative
humidity of an atmosphere around a food neither gains
nor loses water. Thus, the two humidity values are in
equilibrium, and the vapor pressure of water in the food
is the same as that in the atmosphere. A more detailed
description of water activity can be found in papers by
Scott (39) and Troller (45).
Water activity is decreased by substances that dissolve
in water. Items of high molecular weight, such as flour,
eggs, and milk have relatively little effect on reducing
water activity because their molecules are large and the
number dissolved in a unit of water is small. Sucrose can
appreciably decrease water activity because its molecular
size is relatively small. The same amount of dextrose will
reduce water activity even more because its molecule is
about half the size of the sucrose molecule. The same
amount of sodium chloride will decrease water activity
even more because of the small size of its molecule and
consequently more surface area. Solutes decrease vapor
 PUBLIC HEALTH ASPECTS OF PASTRIES
pressure so that fewer water molecules go into the air
above a solution. Thus, the air above such a solution has
a lower relative humidity than the air above pure water.
Because of the amount of sugar that is added to cream
filling, the water activity is relatively low; too low to
support growth of many microorganisms. A water
activity of below 0.945 will prevent growth of Salmonella.
A water activity below 0.86 will prevent growth of S.
aureus and below 0.90 will prevent enterotoxin
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production by this organism.
Fillings made of cooking fat, emulsifying agents,
sugar, and salt (no protein) did not support growth of S.
aureus (22). When water only was added to some brands
of synthetic fillings, however, the fillings supported
growth of S. au reus (17. 32). When these fillings were put
in pie crusts, S. aureus grew profusely at the interface
between the crust and the filling (17). Silliker and
McHugh (41) observed that S. aureus could grow
neither in the crumb portion of devil's food cake nor in
Journal of Milk and Food Technology 1976.39:289-296.
butter-cream fillings containing as low as 1.8 parts
sucrose to one part water. Water activity in both was low
enough to inhibit growth of S. aureus. But staphylococci
grew in cream fillings containing as much as 2.7 parts
sucrose, dextrose, or invert sugar to one part water when
these fillings were put between layers of the devil's food
cake. This growth was attributed to migration of water
from the cake to the interface of the cake and filling and
to creation of localized areas of high water activity.
Rolfes (37) found that staphylococci grew in inoculated
fillings of chocolate cup cakes when the sugar to water
ratio was 1.83:1 or lower but not at 2.20:1 and of sponge
cake fillings when the sugar to water ratio was 1.53:1 but
not as 1.83:1.
There is marked dehydration on the top surface of
custard pies. Top surface inoculum of S. aureus showed a
24-h lag before growth commenced (36). Cut surfaces
also showed dehydration, but this caused less inhibition.
In general, it is difficult to predict whether or not
particular fillings, icings, or toppings will support
staphylococcal growth. because migration of water can
result in creating areas of higher water activity than that
of either of the components (40).
pH
The optimum pH for growth of salmonellae and
staphylococci is near 7. The pH of commercial custard
mixes used by bakeries is close to the optimum (5.84-6.6)
for these organisms (12). Growth of staphylococci is
prevented at pH 5, and growth of salmonellae is
prevented at a pH of 4.5.
Oxidation-reduction potential
Staphylococci and salmonellae are aerobic, facultative-
ly anaerobic in regard to their oxygen needs. Thus, the
oxidation-reduction potential of cream fillings should be
within a suitable range for these pathogens to initiate
growth.
Temperature
The temperature range for which staphylococci can
291
grow in custard is 46 to 114 F (6). Salmonellae did not
grow in custard between 40 and SO F, but they grew at
114 F (6). Optimal temperature for multiplication of
these pathogens is near 100 F.
Surkiewicz (43) reported that coliform, coagulase-posi-
tive staphylococci, and aerobic colony counts increased
greatly when imitation-cream pies were stored at room
temperature for 24 and 48 h. Post et al. (35) reported that
S. aureus increased in cream filling to between 10 5 to
107/g when stored under conditions to simulate delivery
temperaturt: for 10 h.
If cream-filled pastries or their fillings are left in the
temperature range in which foodborne pathogens can
grow for sufficiently long periods, these pathogens
multiply and in the event of enterotoxigenic strains of S.
aureus produce enterotoxin. Inadequate cooling of
cream fillings or inadequate cold storage of cream-filled
pastries are the factors that contribute to most reported
food borne outbreaks (fable 3). Another important factor
associated with inadequate cooling is to prepare
cream-filled pastries a day or more before serving during
which time pastries or their fillings are improperly
stored.
Competition
Many microorganisms compete with and outgrow
staphylococci in the ingredients that go into cream
fillings; but after these ingredients are blended and
cooked, competing organisms as well as staphylo-
cocci are killed. Staphylococci can be readily
reintroduced if the cooked fillings are handled by
infected workers after cooking, and these organisms will
subsequently grow without competition from other
organisms. The ratio of competitive organisms to
pathogen in the mix and the phase of growth that
contaminating organisms are in when they reach the
product will, along with the other factors mentioned,
determine which organisms will predominate.
Survival
Cooking and reheating failures have permitted
pathogens to survive in cream fillings and toppings
(fable 3). Browning (heat treatment of approximately
450 F for about 6 min) of meringue topping, for instance,
offers too little heat treatment to kill bacteria except
those in the top layer. Meringue is an excellent insulator
because of air bubbles entrapped in egg white foam.
Experiments conducted by the American Institute of
Baking (3) revealed that the temperature attained at the
meringue-filling interface was less than 112 F during
browning.
EXAMPLES OF OUTBREAKS
Circumstances leading up to two outbreaks in which
either cream-filled pastry or meringue-topped cream pies
were vehicles are presented below. Although both
outbreaks occurred several years ago, similar patterns
have repeated with monotonous regularity; and, un-
fortunately will be repeated as long as cream-filled
pastries are mishandled by uninformed or careless bakers,
 292
food-service operators, and consumers.
Cream-filled eclairs which were implicated in an
outbreak of staphylococcal intoxication (16) were
prepared in a bakery in the following manner. Cream
filling was made of milk, sugar, starch, eggs, salt, and
vanilla. (A blend which would readily support rapid and
progressive grmvth of bacteria.) A mixture of milk and
sugar was boiled. Then other ingredients were added.
This mixture was poured into several 2-gal. pots which
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were placed on the floor of an unheated room to cool for
4 h. Of contamination had occurred during the transfer,
staphylococci would have probably passed from their lag
phase and begun exponential growth.) Then the cream
filling was poured into a mechanical cream-puff filler.
Prepared pastry shells were filled one at a time by
pushing the shell upon the nozzle of the filler by hand.
This process took about an hour. (During the
investigation, it was observed that parts of the filler
which were not easily accessible for cleaning had not
Journal of Milk and Food Technology 1976.39:289-296.
been cleaned.) After filling, a chocolate covering was
sprayed over the shells. Eclairs were left at room
temperature for S h until they were delivered. Delivery
took up to S more h. (If contamination had taken place
during filling, there would have been ample time for
staphylococcal growth and toxin production during
holding and delivery.) Nose and throat cultures of most
of the employees showed S. aureus. This organism was
also isolated from a purulent infection on a finger of a
worker who poured cream filling into the filler and
handled each eclair during filling. It was also isolated
from the nozzle and base of the filling machine as well as
from samples of the cream filling. Emetic responses were
observed in kittens tested. (This epidemic occurred
before immunogel-diffusion tests for enterotoxin in food
and phage typing of isolates from cultures of specimens
and samples were available.)
Chocolate and banana-cream pies were incriminated
as vehicles in Salmonella outbreaks arising from meals
served at two separate food service establishments (2).
The incriminated cream pies were manufactured at a
local pie bakery. The chocolate- or banana-flavored
pudding made of dried skimmed milk, sugar. water, salt,
cornstarch, and flavoring was boiled; then unpasteurized
dried egg white (a likely source of Salmonella) was folded
into the mixture. Pie shells were filled and a meringue
made from unpasteurized frozen egg white (a likely and
suspected source of Salmonella), sugar, agar stabilizer,
and water was added by hand. Meringue-topped pies
were browned in an oven for S min at 450 F. (Hardly
enough time to kill Salmonella.) Pies were not
refrigerated while stored at the bakery or during delivery.
This practice provided ample time and suitable
temperature conditions to allow salmonellae to
proliferate.
About a year later, lemon meringue pies baked in the
same bakery were vehicles in a second outbreak. This
time frozen egg whites were considered the source of
Salmonella for the pies.
BRYAN
CONTROL
Prevention of foodborne illness is based on
preventing or limiting contamination, killing pathogens,
and preventing multiplication of bacteria. These
principles must be applied at appropriate steps of
cream-filled pastry manufacture, distribution, and
storage.
Product formulation and ingredients
Synthetic cream fillings have been formulated to
alleviate the inherent problem of supporting growth of
pathogens and to prolong product shelf life. Without
protein, staphylococci are unable to grow; without eggs
the likelihood of contamination by salmonellae is
lessened. Staphylococci can grow in some brands of
synthetic cream fillings when just water has been added.
Growth was enhanced, however, by the addition of milk,
eggs, or butter.
Control of water activity is the most important factor
to consider when formulating creams so that they will
prevent growth of microorganisms. But even in creams
that are formulated to have water activity values too low
for growth to occur, water may migrate and form pockets
of moisture which can allow bacterial growth. The
pockets form particularly at the interface of cream and
pastry.
Acid ingredients such as lemon may slow bacterial
growth, but buffering properties of milk and eggs require
that an excessive amount of acids are needed to lower the
pH of a tilling to a value that would prevent growth of
pathogens (13, 38). Lemon, orange, pineapple, apricot,
raspberry, peach, and strawberry pure fruit fillings
inhibited growth of salmonellae and staphylococci (13,
38). Chocolate or cocoa also inhibited staphylococcal
gro\'iih in cream fillings (12). This inhibition was
attributed to nonfat components of chocolate and to pH.
Certain additives have inhibited bacterial growth in
cream-filled pastries. Castellani (10) showed that
DL -serine had bacteriostatic action on staphylococci (but
not salmonellae) in cream-pastry fillings. Both coconut
and cocoa, however, neutralized the bacteriostatic effect
of serine on staphylococci (II). Subtilin and terramycin
prevented growth of bacteria in cream fillings (21), but
their use is prohibited. Hydrogen peroxide has been
effectively used to inhibit bacterial growth in synthetic
creams (22). Preonas et al. (36) reported that 80 mg of
undissociated sorbic acid per gram in combination with
100 mg of undissociated propionic acid per gram
prevented growth of S. aureus on top surfaces of custard
pies.
Eggs are a potentially hazardous ingredient in
cream-filled pastry. Broken or checked eggs and
unpasteurized frozen or dried eggs have been the source
of salmonellae in these products (Table 3). Only eggs that
have been pasteurized or otherwise treated so as to
destroy all salmonellae should be used in fillings.
As new developments in processed foods occur,
changes take place in formulation of fillings and other
 PUBLIC HEALTH ASPECTS OF PASTRIES
components of cream-filled pastry. These new
ingredients sometimes permit incorporation of more
water. High ratio shortenings, for example, permit
incorporation of more water in a cake batter than was
previously possible. If this increase in water is ·not
accompanied by a similar increase in sugar, the resulting
cake may not be safeguarded from growth of pathogens.
Changes in formula should only be made after effects of
changes on safety of the product have been evaluated (.5).
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Cooking and reheating
Foodborne pathogens that have caused cream-filled
pastry associated outbreaks are killed by routine
methods of cooking cream fillings. Dack et al. (19) found
that when sponge cakes were heated to temperatures
above 170 F, staphylococci inoculated in the cake were
destroyed. Cathcart et al. (14) observed that S. aureus
and Salmonella were killed by the proper baking of
custards and that bringing custard to a boil after adding
thickening ingredients killed these organisms. Husseman
Journal of Milk and Food Technology 1976.39:289-296.
and Tanner (24) reported that 10 8 staphylococci/g were
killed when heated in cream filling to a temperature of
167 F. Temperatures of 185 to 199.4 F rendered
puddings and custards containing eggs free of S. aureus,
but this organism survived at the minimum temperature
for eggs to coagulate (25). In observations of commercial
bakery operations a temperature of at least 180 F was
attained in the center of custard when 9-inch pies were
baked at 425 F for 25 to 30 min (3). Angelotti et al. (7)
reported that 53 to 59 min were required to kill 10 7
staphylococci/gin custard heated at 140 F and that 5.2
to 6.6 min were needed to kill the same number when this
product was heated at 150 F. They also reported that
from 19 to 78 min at 140 F were required to kill the same
number of two serotypes of Salmonella in custard and
that 3.5 to 11.5 min were needed to kill them when this
product was heated at 150 F. An internal temperature of
165 F in a cream mix should be adequate to kill any
expected levels of contamination of S. aureus or
Salmonella in less than a minute. The American Institute
of Baking (4) recommends that pie shells be filled wtth
cream fillings after the filling has been cooked and while
it is still hot.
The hot process of making meringue causes a marked
reduction of bacteria (3). This method consists of adding
hot sugar syrup to whipped egg whites and whipping
until the desired consistency is reached. Browning has
not been effective in killing pathogens.
At one time, reheating cream"filled pastry after filling
was recommended (20, 42). It was suggested that cream
puffs or eclairs be put into a pan, covered with an
inverted pan, and heated in an oven at a temperature of
420 F for 20 min. Although this procedure was effective
in killing salmonellae and staphylococci (and preventing
staphylococcal intoxications if it was used before
enterotoxin was formed), it was objected to by industry
because of the fear of overcooking, and it became
antiquated as refrigeration became more readily
available and more frequently used.
293
Handling
Because man is a reservoir of S. aureus and principal
sources are his nose, hands, clothing, and lesions,
attempts to exlude S. aureus from environments where
cream-filled pastry is processed are impossible and
attempts to prevent contamination of foods are extremely
difficult. Because animals are frequent reservoirs of
salmonellae, as well as staphylococci, they and
unpasteurized foods produced by them or manufactured
from their products can harbor these pathogens and
transport them to food processing and preparation estab-
lishments.
Dack et al. (19) showed that cooking killed
staphylococci in cream filling and baking killed these
organisms in sponge cakes. but contamination occurred
after cooking. Therefore, workers who have open lesions.
recurrent boils, acute sinus infections, diarrhea, or
jaundice should not handle cooked fillings or prepared
pastries. Regulations that prohibit ill or infected persons
from handling food are difficult to enforce, and they do
not entirely solve the problem because healthy people are
just as apt to carry S. aureus and contaminate
cream-filled pastry.
Thorough washing can effectively remove transient
organisms-those that are acquired from touching the
nose or other body parts and from handling food-from
hands, but washing is ineffective at removing resident
staphylococci (29, 30). The use of disinfectants after
handwashing unfortunately does not yield dramatic
results in the control of S. aureus (9. 28). Gloves act as a
barrier between contaminated hands or infected lesions
and food, but they can become as contaminated with
transient organisms as hands are if they are worn very
long or while handling contaminated foods. Bacteria
multiply rapidly on hands that are covered by gloves and
hands so covered perspire freely so that punctures and
tears in gloves, which readily occur, result in leakage of
large numbers of bacteria, including resident
staphylococci. Rubber gloves are seldom washed as
frequently as hands or as well as other pieces of
equipment at the end of the day's operation. Use of
disposable plastic gloves or holding pastry between
waxed paper, however, may be valuable in limiting
contamination of cream-tilled pastry by contaminated
hands during packaging. Their use should be limited to
their intended purpose, and they should be changed if
unrelated tasks are done or if they become soiled or torn.
So even with the best intentions of personal hygiene and
hygienic handling of fillings and pastry, contamination
still occurs.
Although adequate cooking will kill vegetative
bacterial pathogens that may be in the filling or on pastry
shells, there is a possibility of incorporating Salmonella
into products such as meringue topping which are not
adequately cooked. Such contamination can occur via air
currents; by use of equipment used consecutively for
unpasteurized products and then for cooked products;
and by handling of unpasteurized products and then
touching cooked cream filling, meringues, or finished
 294
pastries. However, if unpasteurized or particularly
broken eggs are used in a bakery, they should be used in
an area separate from cooked cream filling or meringue
and should be handled only by workers who do not have
access to areas where cooked cream filling or finished
pastries are handled or stored. Their use should be
limited to items that get thoroughly cooked. cans
should not be used to store any food product other than
the eggs originally packed in them. They are not
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designed for reuse. Organisms may lodge in the inner
seam and be difficult to remove by washing. Frozen eggs
should be thawed either in a refrigerator for several days
or in a tank with cold running water for approximately
18 h.
During mixing of batters or whipping of eggs, very fine
droplets are produced. These aerosols may be carried by
air currents to other areas and contaminate other
products (4). Also, dust is generated from powdered
ingredients. This dust may settle across a room and, if
Journal of Milk and Food Technology 1976.39:289-296.
contaminated, spread pathogens. Ventilation should,
therefore, be designed so that flow of filtered air is from
finished product area to production area.
Eclair filling machines should be constructed of easily
cleanable materials and be so designed as to permit easy
access for cleaning. These machines as well as storage
pans, spoons, scoops, spatulas, ladles, and other utensils
that touch the tilling should be washed with hot water
and detergent. rinsed, and disinfected after use.
Equipment sanitation is more effective if a cleaning
schedule (which defines cleaning responsibility,
frequency, time, and method) is followed.
In a survey of 12 plants and 453 samples of imitation
cream pie and 350 line samples, frozen pies produced in
plants operating under good sanitary conditions (as
determined by Food and Drug Administration
inspections) had fewer than 3 Escherichia coli per gram,
fewer than 50 coliforms per gram, fewer than 25,000
aerobic .Plate colonies per gram, and no coagulase-posi-
tive staphylococci in 0.1-gram portions (43). Good
sanitary conditions included freedom from gross sanitary
deficiencies, periodic and thorough cleaning and
disinfection of equipment. and use of hand sanitizing
dips. Plants operating under poor sanitary conditions
produced pies that had as many as 15 E. coli per gram,
1,100 coliforms per gram, 2,700,000 aerobic plate
colonies per gram, and coagulase-positive staphylococci
were found in 0.01-gram portions.
In conclusion to a study of the bacteriology of
cream-filled pastry, Abrahamson et al. (J) stated that the
keystone of control rests in proper sanitary technique
and that refrigeration is a secondary consideration. (Per-
haps the order should have been reversed, but the two
most important control measures were emphasized.)
Other control measures stated were adjustment of pH
and reheating of finished bakery products, But they felt
that these methods were not as well accepted by industry
because of consumer rejection.
BRYAN
Storage
Contemporary practices of personal hygiene and
sanitation of bakeries do not ensure that foodborne
pathogens will be kept out of cream-filled pastries.
Therefore, foods must be treated as if they are
contaminated by at least staphylococci if not by other
foodborne pathogens. In an early report on the control of
foodborne illness from cream-tilled pastry. the need for
refrigeration in bakeries and homes was emphasized (48).
The most crucial procedure to prevent bacterial
foodborne diseases is to keep pathogenic bacteria from
multiplying. This can only be done by: (a) altering cream
fillings to make them unable to support growth of
pathogenic bacteria, (b) allowing filling or cooked
products to remain within the temperature range at
which pathogenic bacteria can grow for such time that
these organisms stay in the lag phase, (c) rapidly lowering
temperatures of foods and storing them at temperatures
at which pathogenic bacteria cannot grow, or (d) holding
hot foods above temperatures that allow pathogenic
bacteria to grow. The first method has already been
discussed, and the last is a preventive measure that is
probably not practicable for storage of cream-filled
pastry. Discussion will, therefore, be on the second and
third listed methods.
Bulk cream filling or cream-tilled pastry should not be
held within the temperature range 42 to 126 F that
permits growth of foodborne disease bacteria for more
than 3 cumulative hours, including chilling time. This
objective is difficult to meet unless special procedures are
taken to cool fillings rapidly because custard and similar
fillings cool slowly. If cream fillings are stored for less
than 3 days, they should be kept at temperatures of 45 F
or below (46). If they are stored for a longer time,
temperatures of 40 F or less should be used.
Prompt cooling of cream filling is essential for
preventing gro"Wih of pathogenic bacteria. Batches of
cream tilling should never be cooled to room temperature
before being refrigerated. In this period. considerable
bacterial gro"Wih can occur. Cooked fillings which are to
be used at some later time should be put in a refrigerator
within a half hour after cooking. Black and Lewis (8)
observed that custard cooled faster when immediately
refrigerated (at 170 F) than when allowed to cool to room
temperature before refrigerating. Very high bacterial
colony counts were observed in custards held at room
temperature before cooling, but only a small increase was
noted in custard that was put in a refrigerator
immediately after cooking. The time it takes filling to
cool to temperatures at which food borne pathogens cease
multiplication is increased as the time is extended at
which fillings are held at room temperature before
refrigeration (27).
The size and shape of the container and its fill greatly
influence cooling time. The farther heat must travel from
the center of a food to the food surface or container wall
where it is taken up by the cooling medium, the longer it
takes the food to cool. The internal temperature of food
 PUBLIC HEALTH ASPECTS OF PASTRIES
cooled in shallow pans falls faster than that of foods
cooled in large, deep containers. For instance, McDivitt
and Hammer (31) observed that cornstarch pudding
cooled slower and S. aureus grew in it when it was
stored in 100-serving quantities in 20-quart and 14-quart
stock pots in a refrigerator (40 F), but it cooled relatively
rapidly and no bacterial growth occurred when it was
stored in a shallow pan at the same temperature.
Cooling rate is also affected by the material of which
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containers are made and by the method of cooling. Miller
and Smull (33) reported that 3 gal. of pie filling cooled
faster in enamel pans than in earthenware crocks. This
filling cooled faster in refrigerators than at room
temperature; it cooled faster in ice or water baths than in
either refrigerators or freezers. Agitation and stirring
also enhanced the rate of cooling cornstarch pudding (31)
and custard (26).
Some companies and health agencies have advocated
discontinuing preparation of cream-filled pastry during
Journal of Milk and Food Technology 1976.39:289-296.
the warmer months. Such a practice, however, does not
offer a high degree of safety because bakeries, food serv-
ice establishments, and homes are relatively warm year
round and if cream filling or cream-filled pastries are left
at room temperature (winter or summer) bacterial
contaminants will multiply. Proper refrigeration can
prevent this from happening. The practice of
discontinuing manufacture of cream-filled pastry in the
summer seems to be an antiquated control measure left
over from a period before refrigerated storage
equipment, refrigerated trucks, or synthetic fillings were
readily available.
Microbiological standards
Microbial standards of quality for frozen ready-to-eat
banana. coconut, chocolate, or lemon cream-type pies
have been proposed by the Food and Drug
Administration (47). These standards have been based on
a survey of samples from manufacturers of such
products. The standards are that the geometric mean of
10 representative samples of a lot be equal to or less than
50,000 aerobic plate count per gram, and equal to or less
than SO coliform count per gram. Lots falling below this
standard must be labeled with the statement "Below
standard in quality-contains excessive bacteria." Such
standards should assist in providing incentive to keep
contamination to a minimum level, to maintain a
reasonable level of plant sanitation, and to have good
operational procedures.
Training
Prevention of foodborne disease from cream-filled
pastry must be based on training and education.
Training of professional public health workers,
managers of bakeries, and employees and supervisors of
baking and food service operations is necessary. They
should be informed about specific disease hazards
associated with preparation of cream-filled pastry, of
factors that have contributed to outbreaks, and of critical
control points of the operation. They should develop
295
skills in their specific preventive roles whether it be
teaching, inspection of operations, purchasing safe
ingredients, managing operation, cooking cream filling,
filling eclairs, or storing prepared fillings or pastries.
And they should be motivated to perform these skills so
that a good, safe, profitable product is produced.
For prevention of staphylococcal intoxication, for
instance, food workers and their supervisors must not
only know that staphylococcal contamination results
primarily from infected (but usually healthy) workers
touching foods, but that foods so contaminated must be
handled in a way that will prevent staphylococci from
multiplying and, thus from elaborating enterotoxin.
They must know that unpasteurized egg products,
cracked and checked eggs, and the egg shell itself may
harbor salmonellae which end up in finished products as
a result of inadequate cooking or from cross
contamination. They must know that foodborne disease
outbreaks can be prevented by application of the
following three food protection principles: (a) preventing
contamination by purchasing safe foods, by careful
handling of foodstuffs, by personal hygiene, and by
cleaning and disinfection of kitchen equipment; (b)
killing pathogens by thorough cooking; and (c)
preventing bacteria from multiplying by processing foods
rapidly while bacteria are in a lag phase, by rapidly
cooling foods, and by holding foods at temperatures at
above or below those at which pathogens multiply. The
aim of training is to provide habitually good day-to-day
operational procedures in the production of cream-filled
pastry.
Education of the purchaser so that he will not abuse
cream-filled pastry by letting the small numbers of
bacteria that will invariably be in it multiply is a
necessary part of a cream-filled pastry protection
program. Tapes or labels on boxes informing the
purchaser to refrigerate cream-filled pastry have assisted
in obtaining this goal.
SUMMARY
Achievements by industry, research institutions, and
official food protection agencies in developing an
awareness of the problem and in devising and applying
preventive measures are notable. Few foodborne diseases
transmitted by specific vehicles (other than milk) have
shown such a marked decline in the last four decades.
Disease surveillance with appropriate follow up,
microbiological testing, and training and education are
the approaches that will prevent cream-filled pastry from
becoming vehicles of food borne disease outbreaks in the
future.
ACKNOWLEDGMENTS
Presented at the Annual Meeting of the New York State Association
of Milk and Food Sanitarians, September 20, 1974.
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