Professional Documents
Culture Documents
ABSTRACT
INTRODUCTION
1
Author for correspondence. TEL: (632) 920-5473; 920-5301 loc. 6552, FAX: (632) 920-2091;
926-1449; 926-2813; EMAIL: ma_patritia.anzanza@up.edu.ph
sworth 1994). Although formally registered food services that cater to RTE
take-away foods do exist in the Philippines, these are greatly outnumbered by
informal establishments that also provide RTE foods at more affordable
prices. Unfortunately, increasing numbers of local foodborne diseases con-
tinue to be implicated with food service institutions that prepare and sell
Philippine RTE foods (Dayrit et al. 1993; Dayrit 1994; Dayrit et al. 1996a,b;
Roces et al. 1996; Roque et al. 1996; Dayrit et al. 1997; Roces et al. 1998a,b;
Roces et al. 1999a,b,c, 2000a,b; Roces et al. 2001). Steps to improve local
surveillance of quality and safety of RTE foods are needed to help ensure
public health. The benefits in cost and convenience derived from RTE take-
away foods should always be coupled with safety assurance.
Although the microbial quality of many RTE foods has been the subject
of numerous investigations in more developed countries (Van Kampen et al.
1998; Kaneko et al. 1999; Nichols et al. 1999), in the Philippines there is a
paucity of information on the microbial quality and safety of this type of food
products. In developing countries like the Philippines, where effective food
safety controls by concerned regulatory agencies are yet to be realized, eval-
uation of food microbial hazards and their indicators would help provide
criteria for setting functional microbial guideline values.
Among the more popularly used nonpathogenic microbiological indica-
tors of food quality is the Aerobic Plate Count (APC) (Vandereit 1985; FEHD
2001; FSAI 2001). It is generally used for descriptive evaluation of microor-
ganisms on nonselective media under mesophilic and aerobic conditions of
incubation (Swanson et al. 1985; FEHD 2001; FSAI 2001). This plate method
serves as an indicator of food quality and as a measure of the effectiveness
and maintenance of procedural integrity of food preparation protocols
(Shapton and Shapton 1991).
It is generally believed that high APCs in foods indicate greater risks of
pathogens being present in consumable products, poor implementation of
sanitation procedures or problems in process controls to which a test food
item has been subjected (Miskimin et al. 1976). The recommended reference
value for the APC of RTE foods was cited in several studies to be <105 cfu/g
(Solberg et al. 1990; Shapton and Shapton 1991; Jay 1996). The Japanese
local prefectural government similarly defined RTE foods with <5.0 log cfu/
g as safe (Kaneko et al. 1999). The Malaysian Food Act of 1983 and the
Malaysian Food Regulation of 1985 both set a more lenient APC guideline
for RTE meat products at 106 cfu/g (Seng and Badji 1993). Miskimin et al.
(1976) much earlier reported that it is unrealistic to have APC values for RTE
foods set at <103 cfu/g.
The present study was done to establish the APCs of some popular
Philippine RTE foods from take-away premises sampled at the point of sale.
The information presented in this study was envisioned to contribute to the
82 M.P.V. AZANZA
much needed baseline data necessary to set some microbial guideline values
for RTE take-away foods in the country.
Sampling Procedure
A total of 125 samples consisting of 34 different types of take-away RTE
food samples were collected and analyzed in the food laboratory of the
Department of Food Science and Nutrition, College of Home Economics,
University of the Philippines, Diliman, Quezon City, Philippines. The take-
away foods were purchased at the point of sale from registered and informal
food service establishments within the vicinity of Diliman, Quezon City,
Philippines for the period of March 1998–October 2002. The types of take-
away RTE foods sampled included: meat, fish/fishery, vegetable, sandwich,
beverage, beverage-like (sweetened beverage with significant amount of solid
particulates included), rice and pasta food products. The various test products,
in their original packaging materials with net weight of ≥150 g, were pur-
chased and transported to the laboratory within 1 h from sampling for micro-
bial analyses.
Meat Products
The APCs of some Philippine RTE meat products from take-away food
service premises in Diliman, Quezon City, Philippines are presented in
Table 1. Some of the APCs of the grilled and fried meat product analyzed
TABLE 1.
THE AEROBIC PLATE COUNTS (APCs) OF READY-TO-EAT MEAT PRODUCTS FROM TAKE-AWAY PREMISES IN DILIMAN, QUEZON CITY,
PHILIPPINES
Local product name/ Trial APC Local product name/ Trial APC Local product name/ Trial APC
description (cfu/g) description (cfu/g) description (cfu/g)
exceeded the typical guideline APC value set at <105 cfu/g for RTE food
products (Solberg et al. 1990; Shapton and Shapton 1991; Jay 1996; Kaneko
et al. 1999). Fried beef jerky appeared to be the sample that recorded relatively
higher APC values among the samples tested. Traditionally, this meat product
is cooked instantaneously by panfrying in very hot oil for the shortest time
possible to avoid toughening of meat and excessive caramelization of the
sugar ingredient of the product that may lead to unavoidable surface charring.
Johnston and Tompkin (1992) cited that the combination of drying and frying
should have a synergistic effect on the lowering of the total microbial counts
in jerky products. However, the local beef jerky samples, as dried commodities
sold in local retail markets intended to be fried, may have also been exposed
to substantial post-drying contaminants that were not fully inactivated during
the typical flash heating steps used for local cooking of the product.
Other test fried RTE products that have counts exceeding the recom-
mended APC value included: fried chinese meat roll and sweet nitrite-cured
pork slices. The chinese meat roll could be described as an emulsified product,
which mainly constitutes minced meat and seasonings with various starches
as binders and extenders. Fried chicken croquettes, which closely resemble
the chinese meat roll in terms of formulation and cooking procedures, have
been similarly reported to have APC values as high as 106 cfu/g (Seng and
Badji 1993). Simmonds and Lamprecht (1985) cited that starch-based blended
formulations that may contain minced meat, starch, herbs, spices, eggs and
other extenders were regarded as risky food commodities because of increased
chances of contamination from its food ingredients and the highly manual
mode of preparation.
Fried sweet nitrite-cured pork slice samples, which were processed and
sold in local provincial markets, have been previously cited to contain high
APC values (≥105 cfu/g) (Azanza and Rustia 2003). The microbial contami-
nation of local sweet nitrite-cured meat samples was previously attributed to
the following factors: (1) the use of leftover cut meats from local fresh meat
retailers as raw material, (2) on-market site preparation, fermentation and
storage of the products where necessary hygienic facilities and utilities needed
for safe food processing were lacking or unavailable and (3) the utilization of
curing and seasoning ingredients that have been repacked also under the rather
unhygienic conditions of the local retail market (Azanza and Rustia 2003).
Fortunately, it has also been reported that nitrite-cured pork slices prepared
by small- to medium-scale food processing industries have lower microbial
counts (<105 cfu/g APC) (Azanza and Rustia 2003) as what was also shown
in the results of some samples analyzed in the study.
Some grilled meat products analyzed were also shown to have counts
≥105 cfu/g like the grilled pork slices sampled. Similarly, grilled chicken
kebabs (sate ayam) were earlier reported to have APCs as high as 107 cfu/g
AEROBIC PLATE COUNTS OF READY-TO-EAT FOODS 85
(Seng and Badji 1993). Burnt surfaces of grilled meat products have been
reported to significantly hamper heat transfer in the food and eventually
prevent further cooking of the inner portions of meat pieces being heated (Jay
1996). Having grilled meat products that are overcooked on the surface yet
undercooked inside may be a result of the immediate oxidation of proteins
and fats on the surface of the food that are exposed to high temperature at the
start of the grilling procedure (Azanza and Gedaria 1998a). Other grilled meat
products including the exotic local dishes, chicken intestine kebabs and
chopped spicy pork jowls or pig masks, did not exceed the generally accept-
able recommended APC value for RTE food products. Fortunately, although
these dishes utilize nontraditional meat cuts, the dishes are commonly pre-
pared using precooking steps that involve boiling in acidified brines. The
precooking step for chicken intestine kebabs, which involves boiling in brine
with vinegar, was previously cited to significantly lower the APCs of the test
product (Azanza and Gedaria 1998a).
Among the meat products that were shown to have APC values within
the generally recommended guideline value for APC of RTE foods set at
<105 cfu/g (Solberg et al. 1990; Shapton and Shapton 1991; Jay 1996; Kaneko
et al. 1999) were meat stews, fried native coarse pork sausages and deep-fried
battered/breaded pork chops. Stewing of osso bucco usually involves slow
boiling of meat and vegetable ingredients in local crock-pot to attain the tender
texture of meat sought by its consumers (Olney 1978; Abiva and Subida
1994). Similarly, the pork and vegetable sour stew is traditionally boiled for
several hours to attain the very soft to almost disintegrating condition of the
meat that local consumers better prefer (Abiva and Subida 1994; Morris and
Hsiung 2001). Deep-fried battered/breaded pork chops are cooked in a very
hot vegetable oil that may significantly eliminate microbial contaminants in
the products.
TABLE 2.
THE AEROBIC PLATE COUNTS (APCs) OF READY-TO-EAT FISH/FISHERY AND
VEGETABLE PRODUCTS FROM TAKE-AWAY PREMISES IN DILIMAN, QUEZON CITY,
PHILIPPINES
Fish/Fishery
Ginisang bagoong 1 5.00 ¥ 104
Sautéed fermented shrimp paste 2 3.10 ¥ 104
3 3.00 ¥ 104
4 1.90 ¥ 103
Mean 2.82 ¥ 104
Pritong alumahan 1 1.41 ¥ 105
Fried striped mackerel 2 7.15 ¥ 104
3 1.25 ¥ 104
Mean 7.50 ¥ 104
Pritong bangus 1 5.50 ¥ 104
Fried milkfish 2 1.25 ¥ 104
3 1.05 ¥ 104
Mean 2.6 ¥ 103
Pritong fishballs 1 1.22 ¥ 104
Fried fishballs 2 9.86 ¥ 103
3 9.85 ¥ 103
4 6.05 ¥ 103
5 5.90 ¥ 103
6 5.10 ¥ 103
Mean 8.16 ¥ 103
Vegetable
Ginisang munggo 1 1.42 ¥ 104
Stir-fried mungbeans 2 1.25 ¥ 104
3 6.00 ¥ 103
Mean 1.09 ¥ 104
Lumpiang sariwa 1 1.60 ¥ 106
Fresh spring roll with sautéed vegetable filling 2 1.60 ¥ 105
3 2.50 ¥ 103
4 2.10 ¥ 103
Mean 4.41 ¥ 105
wrapper and the manual wrapping of the rolls without the benefit of subse-
quent final cooking process may help explain the elevated APC levels of some
of the samples analyzed.
Fried fish was previously reported to have an acceptable APC guideline
value of 104 cfu/g (Wehr 1982). The Food and Environmental Hygiene Depart-
ment of Hong Kong and the Food Safety Authority of Ireland more recently
and realistically set a guideline value of <106 cfu/g (FEHD 2001) and
<105 cfu/g (FSAI 2001), respectively, for RTE cooked fish. Although fried
foods are generally expected to have lower microbial counts because of the
AEROBIC PLATE COUNTS OF READY-TO-EAT FOODS 87
frying process, the elevated APC value of one sample of fried fish analyzed
in the study could perhaps be attributed in part to some post-cooking contam-
inations during extended hold-on display of the product under warm, ambient
conditions. It has been reported in the Philippines that fried milkfish held on
display for 6 h at 28–30C during vending recorded APCs as high as 106 cfu/
g (Azanza et al. 2001). Seng and Badji (1993) similarly reported elevated APC
values of fried fish from hawker stalls to as high as 107 cfu/g.
For fermented foods, like sautéed shrimp paste, specific APC guideline
values are yet to be established because existing microbiological data were
said to be insufficient to warrant recommended guideline values (FEHD 2001;
FSAI 2001). Lee (1989) reported APC values of 105 cfu/g for fermented
anchovy, where the counts were mainly attributed to the total concentration
of lactic acid bacteria.
Studies on microbial contamination of fishballs are uniquely important
for Philippine consumers because it is a very popular RTE food in the country
to date. This food product has already been implicated in one cholera food-
borne outbreak and in a hepatitis A outbreak in the Philippines (Dayrit et al.
1993; Dayrit 1994). Azanza and Gedaria (1998b) cited that some of the factors
that render this RTE food potentially hazardous were: (1) deterioration of raw
fishballs kept under ambient conditions during vending, (2) unhygienic prep-
aration and use of fishball sauces and (3) temperature abuse of the cooked
product during vending. Fortunately, frying temperatures, which can reach as
high as 120C, were shown to adequately lower the APC values of fishballs to
a range of 103-104 cfu/g as a result of the destruction of the vegetative cells
of a wide range of microorganisms, including those that are of public health
significance (Azanza and Gedaria 1998b). It was also previously recom-
mended that fishballs be consumed when freshly fried and using vinegar-based
sauce (Azanza and Gedaria 1998b). All the fried fishballs analyzed in this
study recorded APC values that fell within this previously reported APC range
(103-104 cfu/g).
Local product name/ Trial APC Local product name/ Trial APC
description (cfu/g) description (cfu/mL)
Sandwich Beverage/Beverage-like
Chicken 1 1.00 ¥ 106 Inuming buko 1 1.70 ¥ 104
Bread slices filled with 2 4.30 ¥ 104 Grated young coconut 2 9.60 ¥ 103
mixture of flaked boiled 3 2.90 ¥ 104 meat with coconut 3 6.10 ¥ 103
chicken meat, chopped onion, 4 1.70 ¥ 104 liquid endosperm Mean 1.09 ¥ 104
seasonings and mayonnaise 5 4.10 ¥ 103
6 1.35 ¥ 103 Sago gulaman 1 2.38 ¥ 107
7 8.00 ¥ 102 Tapioca pearls and 2 2.18 ¥ 106
Mean 1.56 ¥ 105 gelatin in light syrup 3 1.40 ¥ 106
4 1.87 ¥ 106
Hamburger 5 1.22 ¥ 106
Bread buns filled with fried 1 1.00 ¥ 106 6 1.04 ¥ 106
and/or grilled beef patties, 2 6.60 ¥ 104 7 3.45 ¥ 105
M.P.V. AZANZA
either as raw or cooked components, which were then mixed with some
dressing matrices without the benefit of final cooking steps. Tuna and chicken
sandwiches sold in the Philippines normally utilize fillings that fall under the
salad-type category.
Relatively higher APC range (105-107 cfu/g) was established for the
hotdog sandwiches analyzed in the study. Higher levels of APCs in hotdog
sandwiches may be attributed mainly to the quality of sausage component of
the food unit. Shapton and Shapton (1991) cited an APC of 105 cfu/g for
cooked sausage. Microbial APC criterion for uncooked pork sausage was
reported to be 107 cfu/g (Wehr 1982). Hotdog is essentially a type of sausage
containing emulsified meat extenders and curing agents combined in food
grade casings (Hoogenkamp 1998). The meat component and extender for
hotdogs usually consists of low priced meat trimmings and other meat by-
products including mechanically deboned meat (MDM), pork rind emulsion
and the like (Babji and Yusof 1995). Some nontraditional meat components,
like MDM, unfortunately carry high microbial loads. Thus, high APC values
in the food product are not unexpected. Likewise, RTE hotdogs are usually
served with dressing including mustard, mayonnaise and catsup that may
equally contribute to the flora of the final RTE sandwich. In the Philippines,
hotdog has been implicated in some foodborne disease outbreaks (Roces et al.
1998b; Roces et al. 1999c).
Tapioca pearl and gelatin in light syrup (sago gulaman) beverage samples
recorded higher APC values relative to other beverage and beverage-like
products analyzed that fell in the range of 105-107 cfu/mL. Azanza and
Gedaria (1997) in an earlier work similarly reported APCs for sago gulaman
beverage to be in the range of 106-107 cfu/mL. The APCs of all sago gulaman
samples analyzed in this study were not within the reported APC values of
£104 cfu/mL for syrups and flavored syrups (Wehr 1982). Microbial contam-
ination of sago gulaman was previously attributed to the cross-contamination
during vending, mixing of leftovers with new batch preparation of the product
and extended hold-on display of the product at ambient conditions (Azanza
and Gedaria 1997). In the Philippines, sago gulaman was also previously
implicated in a foodborne disease outbreak involving 27 morbidities (Roces
et al. 1998a).
The local beverage consisting of solid and liquid endosperms of young
coconut (Cocos nucifera Linn.), which are sold as a chilled commodity
(Azanza et al. 2003), recorded APC values of 103-104 cfu/mL. These values
were lower than the typical guideline APC value of <105 cfu/g for RTE food
products (Solberg et al. 1990; Shapton and Shapton 1991; Jay 1996; Kaneko
et al. 1999). The mesophlic count for this type of product was expected to be
low because the beverage samples were stored at 10–15C during vending.
However, separate studies by Azanza et al. (2003), Pagurigan et al. (2000)
90 M.P.V. AZANZA
and Torres (1997) previously reported that the APC values of the beverage
were as high as 106 cfu/mL. The previously reported higher APC values of
the food commodity may be, in part, attributed to the unscrupulous practices
of some vendors of extending the product shelf life and possible lapses in
temperature control during the vending of the product.
All soft bean curd in light syrup (taho) samples analyzed had APCs in
the range of 103-104 cfu/mL. These values were lower than the general rec-
ommended guideline value of <105 cfu/mL for RTE foods (Solberg et al.
1990; Shapton and Shapton 1991; Jay 1996; Kaneko et al. 1999). The Food
and Environmental Hygiene Department of Hong Kong has recently placed
bean curd under the savory food group but still without any applicable
microbial criterion for aerobic colony count (FEHD 2001). Similarly, the
Food Safety Authority of Ireland has grouped bean curd under a food cate-
gory for which guideline value for aerobic colony count is not yet applica-
ble (FSAI 2001). The APC values of local samples analyzed in this study
were initially expected to be higher than what was actually obtained consid-
ering that this RTE food is produced mainly by local micro and small-scale
businesses. As such, it was assumed that the control of hygiene during man-
ufacturing of the product was less stringent. Likewise, the traditional prac-
tice of employing daily contracted vendors, who do not necessarily have the
appropriate knowledge of the fundamentals of food hygiene, was also
expected to exacerbate the potential microbial contamination of the product.
However, manufacturers of taho generally claim that the soft bean curd
product will not solidify if there are contaminants in the curd. Therefore, it
is also possible that self-imposed stringency in processing procedures is
actually being implemented by the local producers, as further supported by
low APC values of the product obtained in the study. Furthermore, both
curd and syrup of the product are exposed to high temperatures during
cooking, which may also cause significant inactivation of mesophilic aero-
bic flora inherent in the commodity.
TABLE 4.
THE AEROBIC PLATE COUNTS (APCs) OF READY-TO-EAT RICE AND PASTA PRODUCTS
FROM TAKE-AWAY PREMISES IN DILIMAN, QUEZON CITY, PHILIPPINES
et al. 1999). Indonesian RTE fried rice, Nasi goreng, was similarly shown to
have APCs as high as 107 cfu/g (Van Kampen et al. 1998). Gilbert et al. (1996)
reported that an APC value as high as 106 cfu/g was given a satisfactory
microbial rating for RTE fried rice samples analyzed.
The reported high levels of microbiological contamination of boiled rice
and its association with incidences of food poisonings have been linked with
the commercial practice of bulk preparation of the product in food service
establishments in anticipation of subsequent need, as well as its storage at
room temperature for long periods of time prior to reheating (Nichols et al.
1999). Bryan et al. (1992) earlier cited that this practice in handling cooked
rice is particularly common in Asian countries, like the Philippines, where
rice is staple food. High microbial contamination of fried rice can be attributed
to the fact that it is generally acceptable to use leftover rice as starting material
92 M.P.V. AZANZA
for the dish variant together with some other ingredients like meat and
vegetables, which may also be leftovers. Likewise, because fried rice is based
on the use of cooked material, only flash heating is traditionally required to
end up with a finished fried rice dish. Both fried rice and boiled rice were
previously implicated in reported foodborne disease outbreaks in the Philip-
pines (Roque et al. 1996; Roces et al. 1999a).
Spaghetti was shown to have the most number of samples exceeding the
general recommended guideline value for RTE foods of <105 cfu/g (Solberg
et al. 1990; Shapton and Shapton 1991; Jay 1996; Kaneko et al. 1999). The
result obtained in the study was a validation of previous reports associating
the dish with a number of local foodborne disease outbreaks (Dayrit et al.
1996a,b; Dayrit et al. 1997; Roces et al. 1999a,b; Roces et al. 2001). An
understanding of how culturally distinct spaghetti is cooked, handled and
stored in the Philippines should be considered to better appreciate why this
supposedly microbiologically benign product is recording high levels of
microbial contamination and causing foodborne disease outbreaks. The pasta
dish is now part of the typical local festive household menus and is also
commonly sold in almost all food service institutions. As such, the dish has
been indigenized in formulation and in manner of handling. Just like boiled
rice, bulk preparation of the spaghetti noodles and its sauce is typically done
(Azanza et al. 2001). Likewise, the dish is usually subsequently stored at
ambient conditions for long periods of time until batch reheating is required,
depending on demand. The dish is therefore subject to potential cross-
contaminations and temperature abuse.
The APC values of rice noodles with thick sauce topped with flaked
smoked fish, boiled egg and spring onion (palabok) were within the general
recommended guideline value for RTE foods of <105 cfu/g. Considering that
this product contained toppings, which were manually handled as raw ingre-
dients, the APC values of the samples were unexpectedly low. The general
view of the populace that the product is highly perishable perhaps may have
provided the imposed necessary margin of safety needed in the preparation of
the dish with the food handlers becoming more cautioned of the product
perishability, particularly those sold commercially.
In summary, the study for the first time analyzed and consolidated APC
values of at least four major groups of local RTE foods with the intent of using
the information in the development of local microbial guideline values for
Philippine RTE foods. The APC values of most of the food samples analyzed
were within the generally recommended APC guideline value for RTE foods
of <105 cfu/unit of food sample. Although the APC values of some RTE foods
analyzed were ≥105 cfu/unit of food sample, these were still considered
acceptable because none of the food samples analyzed in the study were
implicated in any foodborne disease outbreaks.
AEROBIC PLATE COUNTS OF READY-TO-EAT FOODS 93
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