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Department of Food Science and Nutrition, College of Home Economics, University ofthe Philippines, Diliman JIO], Quezon City,
Philippines
The microbiology of kwek-kwek as a Philippine emerging streetfood made from boiled quail eggs, which
have been battered and fried was studied. The process of water-cooling and manual peeling of the boiled shell
eggs were shown to increase the TPCs, and coliform and staphylococci counts of the product. The batter was
also shown to contribute to microbial contamination of the product. The microbial profile of ready-to-eat
kwek-kwek during vending was: I04-106 cfu/g TPC; ~ I02 MPN/g coliform count; ~ I04 MPN/g coagulase-
positive staphylococci count; and presence of Salmonella sp. per 25 g sample. The flour-based sauces of kwek-
kwek were found to contain higher microbial contaminants than the vinegar-based sauce. It was recommended
that good manufacturing procedures within the boundary of streetfood trade economics be fully considered
in the preparation and vending of the product.
Physical characteristics Table I shows the physical and staphylococci (Longree and Armbruster, 1996). The
properties of the raw ingredients and other food samples insufficiency of the frying process for kwek-kwek to reach
obtained from different stages of preparation and vending the prescribed internal temperatures for adequate cooking
of kwek-kwek. The temperature of fresh raw materials to may be explained by the very arbitrary indicators used by
the peeled boiled quail eggs ranged from 26-28'C. This the vendors to determine doneness of the food being
temperature range of the egg samples reflects the temper- cooked. It was established that the level of browness of the
ature of the surrounding environment where food was batter coating or the visibly crunchy appearance of the
prepared and stored. Ambient temperature in the Philippines products served as the primary indicators of the cooking
was reported to be 28'C based on prevailing Philippine suff iciency.
normal climatological conditions (PAGASA, 1999). Fresh The samples during re-frying, recorded internal temper-
eggs were reported to be best stored at temperatures ~ 10'C atures below the required food temperatures for cooked
(Clay and Board, 1991; Dolman and Board, 1992). At foods to render it microbiologically safe. Typical re-frying
ambient temperatures, the total quality of fresh eggs were process used also utilize flash heating which does not
reported to deteriorate rapidly (Clay and Board, 1991; normally achieve adequate heating of the cold points of the
Longree and Armbruster, 1996). food especially in the presence of very thick batter coating
used for this test streetfood. It was previously cited that
Table 1. Physical characteristics of street-vended fried quail eggs pre-cooked ham croquettes, that were batter-coated and
(kwek-kwek) obtained from various stages of preparation, vending and fried for 2 min at oil temperature of about 191'C, only
(a)
storage . attained internal temperatures of about 56.1-62.8'C
Sampling Point Temperature aw pH (Deskins and Hussemann, 1954). The final brown color of
('C) the batter coating was also reported to have been used to
1. Fresh quail eggs 26-28 0.92-0.94 7.20-7.77 indicate doneness of the re-heated ham croquettes. The
2. Pre-processed quail eggs temperatures of flour- and vinegar-based sauces used as
a water-soaked boiled eggs 27-28 O.91-0.93 7.72-8.34 condiments for kwek-kwek during the 8-1 2 h hold-on display
b de-shelled boiled eggs 27-28 0.92-0.96 7.55-7.90
4.65-6.22
at ambient conditions were in the range of 26-38'C. The
3. Batter mixture 27-29 0.92-0.93
4. Fried kwek-kwek
temperatures of the sauces coincide with the ambient con-
a newly fried kwek-kwek 60-67 0.90-0.95 7 .37-7 .9 1 ditions of the vending environment.
b re-fried kwek-kwek 26-55 0.91-0.93 7.53-8.25 A11 samples obtained from various stages of food prepa-
5. Sauces for kwek-kwek ration operations prior to frying recorded a~ readings
a flour-based sweet and
ranging from 0.9 1-0.96 indicating high perishability of the
sour sauce (O h) 26-38 0.90-0.93 4. 1 9-4. 80
food samples (Table 1). Water activity levels within the range
b flour-based sweet and
sour sauce (8 h) 26-32 0.90-0.96 4.29-4.77 of 0.86-0.95 permit growth of most bacteria, specifically
c spiced vinegar sauce (O h) 26-30 0.92-0.99 2.84-3.54 those of the foodborne pathogens like Salmonella,
d spiced vinegar sauce (8 h) 26-32 0.92-0.94 2.83-3.66
Staphylococcus aureus and Vibrio parahaemolyticus
(a) Analyses were conducted m 3 tnals (Roberts, 1992). With batter-coating and subsequent frying
and refrying processes, the a~ range of the fried samples
Hard-boiled egg samples, which have been soaked in the in this study did not drop to lower ranges. In related studies,
cooling water, and consequently de-shelled, also recorded frying generally caused a considerable reduction in the a~
temperatures ranging from 27-28'C. Holding of cooked of some deep-fried food commodities attributed to the des-
foods at this temperature range, which is within the danger iccating effect of the procedures (Azanza and Gedaria,
zone of 7.2-60'C (FDA, 1978), is critical to its microbial 1998a; Azanza et al., 2001). In this study, the anticipated
quality (Longree and Armbruster, 1996). Further, de-shelled reduction in the a~ of the fried kwek-kwek samples was not
cooked eggs may be considered more susceptible to spoilage realized perhaps due to insufficiency of the cooking steps
since the natural barrier offered by the shell and its to take effect in the thick batter coating of the eggs. The
membrane no longer protects the food materials. Oblinger inner layers of the batter-coating and the egg itself may have
and Angalet ( 1 974) established that low temperature storage just been lightly heated during frying despite apparent
of hard-boiled eggs at 5'C successfully retarded bacterial doneness of the outer surface of the batter. The a~ of both
spoilage even after 21 d of storage. The batter mixture used flour- and vinegar-based sauces were in the range 0.90-0.99
for coating boiled egg products during hold-on was estab- (Table I ). Previous studies on both starch-based and vinegar
lished to likewise have temperature readings of 27-29'C. sauces used for street-vended grilled chicken intestines
Warm temperature holding of the batter mixture during similarly recorded a~ range values between 0.91-0.96
vending in streetcarts was established to be as long as (Azanza and Gedaria, 1998b).
12 h. Egg samples, including fresh shell eggs, hard-boiled
Newly fried kwek-kwek samples were found to have eggs, and fried and re-fried battered egg samples had pH
internal temperatures of between 60-67'C (Table 1). Internal readings in the range of 7.20-8.34 (Table 1). Fronning et
temperatures of cooked foods must reach at least al. (1992) reported that pH of blended yolk and white of
73.9-76.7'C during the cooking process for an effective shell eggs varies between 7.0-7.6. The pH values estab-
reduction or even elimination of pathogens like Salmonella lished for both flour- and vinegar-based sauces were
,
Microbiotogy of Kwek-Kwek 337
4. 19-4.8 and 2.83-3.66, respectively. Reported pH values fresh potable water to ensure adequate safety.
for starch-based sweet and sour sauces for other Philippine The manual de-shelling of the soaked eggs may have
street-vended foods were 3.5-4. I and 2.8-4.2, respective- inevitably contributed to the recontamination of the boiled
ly (Azanza and Gedaria, 1998a; 1998b). Vinegar normally eggs. Peeling of soaked eggs was manually done by the
has pH of about 3.0-4.0 (Jay, 1992). vendors with unprotected hands. Foodhandlers were estab-
lished transvectors of microorganisms of public health sig-
Microbial characteristics nificance including Escherichia coli and staphylococci to
Totalplate and cohform counts The TPCs and coliform food (Azanza and Gedaria, 1998b). Swab test conducted
counts of fresh quail eggs samples were recorded to be in on the hands of some streetfood vendors in the Philippines
the range of <101_102 cfu/g and ~ 101 MPN/g, respective- indicated that vendors are major agents of microbial con-
ly (Table 2). These counts were considerably lower than tamination of local street-vended foods (Azanza and
the normal microbial counts reported for fresh chicken eggs Gedaria, 1998b).
which were around 102-104 cfu/g (Mossel et al., 1995; The batter mixture analyzed was found to have TPCs and
NAS, 1985) and lO]-l03 MPN/g (Mossel et al., 1995) for coliform counts in the range of about 105-107 cfu/g and
TPC and coliform count, respectively. Fronning et al. ( 1992), 103-104 MPN/g, respectively. Batter-coated egg-based
however, reported that TPC of fresh eggs > 102 cfu/g already
dishes have previously been reported to be one of the most
indicates possible microbial penetration through the porous common type of foods implicated in the increasing food-
egg shell. The raw eggs used in the study generally were borne epidemiological cases in United Kingdom (Sharp,
inherently of low quality since these are leakers. 1992). The aerobic plate and coliform guideline values for
Soaking in cooling water and subsequent manual peeling batters were reported to be about 105 cfu/g and 102 MPN/g,
of the boiled eggs were found to have increased the TPCs respectively (NAS, 1985). The overall microbial quality of
and coliform counts of egg samples by 2-4 and 1-3 Iog the batter blends used by vendors of kwek-kwek may be
units, respectively. The deterioration of the microbial quality attributed to the microbial quality of the main components
of egg following the boiling, soaking and peeling proce- of the mixture including flour, water and spices. Commercial
dures may be attributed to possible contamination from the spices were cited to be heavily contarninated with insect
soaking water used to cool the boiled eggs and contact with fragments and microorganisms (Julseth and Deibel, 1974;
the foodhandler. In the study, cooling of the freshly boiled Powers et al., 1975). Spices have also been reported to
eggs was done by batch soaking in a container using non- normally have TPC of about 105-1 06 cfu/g (Marshall, 1986),
flowing tap water for about 30 min. Although hard-cooked and coliform counts of 102 MPN/g (Wehr, 1982). Grain-
eggs are generally considered safe from microorganisms based products, Iike flour, are commonly associated with
(Licciardello et al. , 1965), this does not preclude the possible
several types of microbial contaminants, in particular
recontamination of the cooked eggs during subsequent Bacillus cereus which is capable of releasing enterotoxins
handling (Merrill et al., 1984). Ideally, wash water of hard- (Longree and Armbruster, 1996).
boiled eggs must be kept at about 10'C warmer than the The frying process was able to reduce the microbial con-
hot eggs to prevent aspiration of possibly contaminated tamination of the streetfood relative to its ingredients by
water into the porous shell and membrane of the eggs upon about 2 Iog units and 1 Iog unit for TPC and coliform
contraction of the hot eggs contents during cooling process counts, respectively. Reduction of microbial counts of fried
(Longree and Armbruster, 1996). For cooling, it has been kwek-kwek samples, however, was still not enough to lower
suggested that hard-cooked eggs must be cooled only in it to acceptable levels for TPCs and coliform counts reported
Table 2. Microbiological quality profile of street-vended fried quail eggs (kwek-kwek) obtained from various stages of preparation, vending and
(a)
storage .
to be about 104 cfu/g and 10 MPN/g for ready-to-eat meals, prepared meals (Marshall, 1986).
respectively (Marshall, 1986). The insufficiency of the With hold-on display at ambient conditions for about
frying procedure to effectively lower the TPCs and coliform 8 h, re-fried kwek-kwek samples were found to have staphy-
counts to recommended acceptable levels may be related 10cocci counts of up to 104 MPN/g. These levels of staphy-
to the low internal temperature attained by the food during lococci pose risk to consumers due to potential enterotox-
the frying process. Color and appearance of the cooked batter in production if staphylococci concentrations increase to
coating were found to be the primary indicators of doneness levels of about ~ 105 cfu/g during prolonged period of hot-
used by the vendors. However, sensory indicators were holding (Mossel et al., 1995). Flour- and vinegar-based
earlier established to be poor indices of adequacy of cooking sauces sampled during vending operations of kvvek-kwek
foods (Deskins and Hussemann, 1954). Re-fried kwek-kwek were found to have coagulase-positive staphylococci counts
samples, which were held for a maximum of 8 h vending of 100_102 MPN/g and 100_101 MPN/g, respectively.
at ambient conditions recorded 104-106 cfu/g TPC, and ~ Presence and survival of staphylococci contaminants in
102 MPN/g coliform counts. Re-working of kwek-kwek these sauces may be explained by their ability to tolerate
samples was also established to cause further increase in very wide pH range. For example, growth of S. aureus was
microbial count by 1-2 Iog-units. reported to be optimum at slightly alkaline conditions
The TPC and coliform range values of the sauces for (7.0-7.5) but can tolerate pH conditions within the range
kwek-kwek at the point of sale were: ( 1) flour-based sauces, 4.2-9.3 (Ash, 1997).
104-l07 cfu/g and 101_102 MPN/g; and (2) vinegar-based Presence ofSalmonella spp Salmonella sp. contam-
sauces, 103-105 cfu/g and 101 MPN/g, respectively (Table ination was recorded for almost all of samples tested includ-
2). Freshly prepared sauces of both types had TPC values ing fresh and cooked egg, batter mixture and sauces (Table
within acceptable levels reported for sauces of 104 cfu/g 2). Salmonella is considered to be ubiquitous in eggs (Gast
(Marshall, 1986). After 8 h of use and hold-on at ambient and Beard 1992). Eggs and poultry meat are among the most
condition, an increase of up to 3-4 Iog-units in the TPCs common food vehicles of salmonellosis to humans (St.
for both sauces was established. These increases in the Louis et al., 1988; Longree and Armbruster, 1996). Presence
TPCs of the sauces, however, may be attributed to the of Salmonella in water-cooled and peeled boiled quail egg
growth of surviving heat-resistant organisms and the samples may indicate either the possible survival of ini-
acquired contaminants upon use and hold-on of the sauces tially present contaminant during cooking or acquired
during vending operations. through contamination during water-soaking and subse-
Staphylococci counts Coagulase-positive staphylo- quent manual de-shelling procedures. Licciardello et al.
cocci counts of fresh and water-soaked boiled quail eggs (1965) established that the normal cooking times recom-
were recorded to be ~ 101 MPN/g which increased by 3- mended for hard-cooked eggs was adequate to destroy 4
10g units after manual peeling. The staphylococci count of serotypes of Salmonella. However, the ability of Salmonella
the peeled boiled quail eggs already exceeded the safety to survive soft boiling of eggs has been reported (Humphrey
guideline value set for cooked meals or snacks which was et al., 1989). Studies have shown that any form of cooking
reported to be 102 cfu/g (Marshall, 1986). The most likely where all or some of the yolk remains liquid can permit the
source of additional staphylococci contamination was the survival of Salmonella enteritidis PT4 even from a very
hands of the vendors in contact with the egg samples during miniscule inoculum (Stadelman, 1995). Post-process con-
manual peeling since the organism is commensal to the tamination has also been established to be a significant route
human skin (Eley, 1992). It has even been demonstrated by which cooked foods can be contaminated by Salmonella
previously that S. aureus are able to enter the shell of (Bryan, 1974). The presence of Salmonella in the newly
cooked eggs since these are no longer protected by their fried and re-fried kwek-kwek samples suggests that the deep
natural resistance to microbial contamination (Harbrecht and frying process applied to the batter-coated eggs was not
Bergdoll, 1980; Merrill et al., 1984). effective in destroying the contaminant initially present in
About 1-10g unit decrease in the coagulase-positive the samples. Varnam and Evans ( 1 996) reported a minimum
staphylococci counts of the newly fried kwek-kwek samples lethal temperature of 74'C for Salmonella to be complete-
was observed. Staphylococci organisms are heat-sensitive, ly destroyed in high a~ foods such as the test streetfood.
and its vegetative cells can be destroyed with heating at Unfortunately, internal temperatures recorded for fried and
temperature of about 60-65'C for 0.2-50 min, depending re-fried kwek-kwek samples were just ~ 67'C.
upon the food or suspending media employed (Roberts, Salmonella contamination of kwek-kwek sauces may have
1992; Ash, 1997). The addition of starch-based thick batter likely been introduced through cross-contamination from
coating may have, however, provided protection to the ini- contaminated raw and other pre-cooked food products. The
tially present staphylococci contaminants in the batter and presence and survival of Salmonella in these sauces could
the peeled boiled eggs. Generally, heat resistance of micro- very well be supported by the favorable extrinsic condi-
biological cells was reported to be affected by the presence tions to which the sauces were exposed to during vending
of protective substances such as protein, fats and colloidal operation in particular, the prolonged holding at warm tem-
matter (Longree and Armbruster, 1996). Fried kwek-kwek peratures. It was also established that the addition of freshly
samples had staphylococci counts ~ 103 MPN/g, which is cut ingredients such as onions and chili was usually done
still beyond the normally reported S. aureus counts for after pre-cooking and pre-preparation of sauces for kwek-
Microbiology of Kwek-Kwek 339
kwek. Gravies were earlier cited to have become contami- foods. Food and Nutrition Research Institute-Department of Science
nated with Salmonella through the addition of contaminat- and Technology (FNRI-DOST), Taguig, Metro Manila, Philippines.
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tions during 0-8 h vending operations had the following Institute of Food Science and Technology (AIFST) Ltd. NSW
microbial profile: TPC of 104-106 cfu/g; coliform count of Branch, Food Microbiology Group, NSW, Australia, pp. 253-286.
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Acknowledgements This study has been made possible through the Gast, R. and Beard, C.W. (1992). Detection and enumeration of
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