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Food Microbiology 36 (2013) 57e62

Contents lists available at SciVerse ScienceDirect

Food Microbiology
journal homepage: www.elsevier.com/locate/fm

Short communication

Microbiological quality of chicken- and pork-based street-vended


foods from Taichung, Taiwan, and Laguna, Philippines
Lydia S. Manguiat a,1, Tony J. Fang a, b, *
a
b

Department of Food Science and Biotechnology, National Chung Hsing University, 250 Kuokuang Road, Taichung 402, Taiwan, ROC
Department of Nutrition, China Medical University, No.91 Hsueh-Shih Road, Taichung 40402, Taiwan, ROC

a r t i c l e i n f o

a b s t r a c t

Article history:
Received 1 July 2012
Received in revised form
31 March 2013
Accepted 11 April 2013
Available online 25 April 2013

The microbiological quality of chicken- and pork-based street-food samples from Taichung, Taiwans
night markets (50) and Laguna, Philippines public places (69) was evaluated in comparison to a microbiological guideline for ready-to-eat foods. Different bacterial contamination patterns were observed
between hot-grilled and cold cooked/fried food types from the two sampling locations with hot grilled
foods generally showing better microbiological quality. Several samples were found to be unsatisfactory
due to high levels of aerobic plate count, coliform, Escherichia coli, and Staphylococcus aureus. The highest
counts obtained were 8.2 log cfu g1, 5.4 log cfu g1, 4.4 log cfu g1, and 3.9 log cfu g1, respectively,
suggesting poor food hygiene practices and poor sanitation. Salmonella was found in 8% and 7% of Taichung and Laguna samples, respectively, which made the samples potentially hazardous. None of the
samples was found to be positive for Listeria monocytogenes and E. coli O157, but Bacillus cereus was
detected at the unsatisfactory level of 4 log cfu g1 in one Laguna sample. Antimicrobial resistance was
observed for Salmonella, E. coli, and S. aureus isolates. Food preparation, cooking, and food handling
practices were considered to be contributors to the unacceptable microbiological quality of the street
foods. Hence, providing training on food hygiene for the street vendors should result in the improvement
of the microbiological quality of street foods. The data obtained in this study can be used as input to
microbial risk assessments and in identifying science-based interventions to control the hazards.
2013 Elsevier Ltd. All rights reserved.

Keywords:
Street food
Ready-to-eat food
Food pathogens
Microbiological quality
Microbial hazard
Antimicrobial resistance

1. Introduction
Street foods are popular because of their accessibility, low cost,
variety, and nutritional value, but sometimes they are perceived as
unsafe because of the unsatisfactory handling practices of food
servers. Most foods are prepared and distributed in mobile and
temporary shops that lack the primary facilities and infrastructure
required to guarantee safe preparation of the foods (WHO, 1996). In
addition, reports have shown that street vendors are generally unaware of basic food-safety issues, lack knowledge about food hygiene, and have little education (WHOeINFOSAN, 2010; WHO,1996).
The proliferation of street-food vendors continues to increase
because the business is very protable and requires very low
capitalization (Cho et al., 2011; WHOeINFOSAN, 2010), and

* Corresponding author. Department of Food Science and Biotechnology, National


Chung Hsing University, 250 KuoKuang Rd., Taichung 402, Taiwan, ROC. Tel.: 886 4
22840385x3010.
E-mail address: tjfang@nchu.edu.tw (T.J. Fang).
1
Department of Science and Technology IV-A, Jamboree Road, Timugan, Los
Baos, Laguna 4030, Philippines.
0740-0020/$ e see front matter 2013 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.fm.2013.04.005

controlling their number and the quality of food they offer is


becoming a challenge. The contribution of the street-vending industry to socio-economic growth is enormous (Von Holy and
Makhoane, 2006). This emphasizes the importance of placing a
priority on assisting them in understanding the importance and the
requirements of food safety. Doing so will protect public health and
simultaneously improve the image of the street vending industry.
Various reports have identied the risks associated with
consuming contaminated street-vended foods that have high levels
of coliform bacteria and the presence of pathogenic bacteria, such
as Escherichia coli, Salmonella spp., Staphylococcus aureus, Bacillus
cereus, Clostridium perfringens, and Vibrio cholerae (Cho et al., 2011;
Hanashiro et al., 2005; Mankee et al., 2005). These reports clearly
indicate that people who patronize the vendors of ready-to-eat
(RTE) street foods might be putting their health at risk. In addition, the prevalence of multi-drug resistance among important
microorganisms, such as Salmonella, E. coli, and S. aureus has been
increasing and poses a real threat to public health (Guven et al.,
2010; Harakeh et al., 2005) because street foods could possibly
become a medium by which these antimicrobial-resistant pathogenic bacteria are transmitted to people.

58

L.S. Manguiat, T.J. Fang / Food Microbiology 36 (2013) 57e62

Chicken- and pork-based street foods are commonly found in


Taiwan and in the Philippines. In both countries, it is very common
to use poultry (chicken/duck) and pork entrails and other parts that
typically are not used for food, including intestines, blood, anal
base, feet, neck, head, skin, heart, liver, gizzard, and proventriculus.
Inherently, these parts are unclean and therefore require additional
and careful cleaning procedures to be acceptable for human consumption. These meat-based street foods are usually available in
Taiwan night markets in grilled form, while in the Philippines, they
are sold in many public places, such as bus terminals, parks, and day
markets.
This study was undertaken to obtain data on the microbiological
quality of chicken- and pork-based street-vended foods in Taichung, Taiwan, and Laguna, Philippines. The data provide information on the microbial hazards present in the street-vended food
category and can be used as inputs to microbiological risk assessments. The results of the risk assessments provide the basis for the
development of science-based interventions to control the hazards
and to implement and improve food-safety management systems
for the street-food vending industry. In addition, in the study, we
attempted to determine the antimicrobial resistance of the resulting microbial isolates, the results of which may offer valuable information on the potential of street foods to contribute to the
spread of multidrug-resistant microorganisms.
2. Materials and methods
2.1. Sample collection
Street-vended food consisting of chicken- and pork-based
samples, mostly grilled and fried, were obtained in two cities, i.e.,
Taichung, Taiwan, and Laguna, Philippines. From October 2010
through September 2011, 50 samples were taken from four night
markets in Taichung, and 69 samples were taken from public places
in three cities in Laguna. Each sample consisted of approximately
200e250 g, and the samples were collected from the point-of-sale
in packages provided by the vendors, just as a consumer would do.
The packed samples were placed in a cooler and immediately
transported to the laboratory and stored at 4  C until they were
analyzed; the holding time did not exceed 16 h. The samples to be
tested were grouped into hot-grilled and cold-cooked or fried
categories, and the specic types of food includes hot-grilled
chicken (hgc), hot-grilled pork (hgp), cold-cooked chicken (ccc),
cold-cooked pork (ccp), and cold-fried chicken (cfc). The chickenbased samples included heart, skin, intestines, buttocks, bits, riceblood cake, neck, feet, gizzard, proventriculus, and kwekekwek
(chicken egg). The pork-based samples included sausage, intestines,
wieners, bits, liver, and head.
2.2. Microbiological analysis
Samples were analyzed for Aerobic Plate Count (APC), coliform
bacteria, E. coli, B. cereus, S. aureus, Salmonella spp., E. coli O157, and
Listeria monocytogenes. With some modications, the test procedures basically were conducted in accordance with the requirements of the Bacteriological Analytical Manual (BAM Online).
Twenty-ve grams of each sample were mixed with 225 ml of
sterile, buffered, phosphate water in a sterile lter bag (Whirl-Pak,
Nasco, Wisconsin, USA) and macerated for 2 min (Stomacher,
Seward, Florida, USA). Serial dilutions up to 106 were prepared
using 0.1% peptone water, and samples were placed on pour plates
in duplicate using Plate Count Agar (Difco BD, New Jersey, USA) for
aerobic plate count (APC). The plates were incubated at 37  C for
24e48 h. Simultaneous enumeration of coliform bacteria and E. coli
was done by pour plate in duplicate using Chromucult Coliform

Agar (Merck, Darmstadt, Germany). The plates were incubated at


37  C for 24e48 h. E. coli BCRC 11634 and ATCC 25922 were used as
reference strains. Dark-blue to violet colonies were counted as
E. coli, and salmon-to-red colored colonies were counted as coliforms. The total of all of the dark-blue-to-violet colonies were
considered to be the total coliform count. The presence of E. coli was
conrmed by the Indole test using Kovacs reagent. For the
enumeration and isolation of B. cereus, 0.1 ml of the sample suspension (101 dilution) was inoculated onto the surfaces of B. cereus
selective agar plates (Oxoid, Hampshire, England) by the spreadplate method. The plates were incubated at 37  C for 24e48 h.
Presumptive identication of B. cereus was conrmed by the Rapid
Conrmatory Staining Procedure (Oxoid). B. cereus ATTC 10876 was
used as the reference strain.
For S. aureus, 225 ml of nutrient-enriched broth with 7% NaCl
were added to 25 g of each sample in a sterile lter bag (WhirlPak, Nasco), and the resulting mixture was homogenized/macerated for 2 min (Stomacher, Seward, USA). One milliliter of diluted
(101) sample suspension was separated into quantities of 0.4, 0.3,
and 0.3 ml and distributed on three Baird Parker Agar plates
(Merck, Darmstadt, Germany) plates by spread plating. The plates
were incubated at 37  C for 48 h. The presence of typical S. aureus
colonies was conrmed by the coagulase test using Bactident
coagulase (Merck) or Staphylase test kit (Oxoid) and by polymerase
chain reaction (PCR) using an S. aureus DAS detection kit (Los
Baos, Philippines). The catalase test and gram-staining also were
conducted. S. aureus ATCC 25923 and BCRC 12653 were used as
reference strains.
For Salmonella detection, 25 g of each sample were placed in a
sterile lter bag (Whirl-Pak, Nasco), mixed with 225 ml of
buffered peptone water, and incubated at 37  C for 20e24 h. From
the enriched sample, 0.1 ml was added to Rappaport Vassiliadis
broth (Merck) and 1 ml was added to Tetrathionate broth (Merck),
and the two were incubated for 24 h at 42  C and 37  C,
respectively. Then, the enriched solutions were streaked on
Xylose Lysine Desoxycholate agar (Difco BD, Madison, USA), Bismuth Sulte Agar (Merck), and Hektoen Enteric Agar (Merck),
after which they were incubated at 37  C for 24 h. Presumptive
positive results were conrmed biochemically according to the
Biochemical Identication of Salmonella and Shigella Using
Abbreviated Panel Tests (WHO, 2010) and by PCR using a Salmonella DAS detection kit. Microscopic examinations of Gramstained cells also were conducted. Salmonella enterica ATCC
10749 and ATCC 9842 were used as reference strains. For serotyping, the Salmonella isolates were submitted to the Antimicrobial Resistance Surveillance Reference Laboratory of the Research
Institute for Tropical Medicine in the Department of Health in
Manila, Philippines.
The presumptive presence of E. coli O157:H7 was conrmed
using modied Tryptic Soy Broth with novobiocin (mTSB, Merck) as
selective pre-enrichment (37  C, 24 h) and streaked on Sorbitol
MacConkey Agar plates (Pronadisa, Madrid, Spain), Fluorocult
E. coli O157:H7 agar plates (Merck), and CHROMagar O157 plates
(Paris, France) as selective/differential media (37  C, 24 h).
Biochemical tests were conducted using Triple Sugar Iron agar (TSI),
Indole, Urea, lysine iron agar (LIA), and PCR using an E. coli O157
DAS detection kit. E. coli O157:H7 BCRC 15377 was used as the
reference strain.
CHROMagar (Paris, France) Listeria plate was used for the
detection of L. monocytogenes in the food samples. For enrichment,
25 g of sample were placed in 225 ml of Demi Frazer Broth (Acumedia, Michigan, USA) with ferric ammonium citrate and incubated at 37  C for 24 h. The enriched solution was streaked to
CHROMagar Listeria agar plate and incubated at 37  C for 24 h.
L. monocytogenes BCRC 14848 was used as the reference strain.

L.S. Manguiat, T.J. Fang / Food Microbiology 36 (2013) 57e62

2.3. Antimicrobial susceptibility testing


The antimicrobial susceptibility proles of Salmonella, E. coli,
and S. aureus isolates were determined by the disk diffusion
method on Mueller-Hinton agar (Scharlau, Barcelona, Spain) as
described by the WHO Global Foodborne Infections Network (2010)
and by the European Committee on Antimicrobial Susceptibility
Testing (EUCAST) Disk Diffusion Method for Antimicrobial Susceptibility Testing e Version 2.1 (2012). The following antibiotic
disks (Oxoid Antimicrobial Susceptibility Discs, Mastdiscs, Merseyside, UK) were tested: ampicillin (10 mg), chloramphenicol
(30 mg), ciprooxacin (5 mg), ceftriaxone (30 mg), amoxicillin/clavulanic (30 mg), nitrofurantoin (300 mg), ceftaxidime (30 mg), nalidixic acid (30 mg), oxacillin (1 mg), clindamycin (2 mg), fusidic acid
(10 mg), gentamicin (10 mg), oaxacin (5 mg), streptomycin (10 mg),
sulphamethroxazole/trimethoprim (23.75 and 1.25 mg), penicillin
(10 mg), erythromycin (15 mg), and vancomycin (30 mg). E. coli ATTC
25922 was used as the control strain to ensure the validity of the
susceptibility testing. Results were recorded after 18e20 h of incubation at 37  C and interpreted according to the breakpoints of
each antibiotic as described in the EUCAST Clinical Breakpoint
Table v.2.0, valid from 01/01/2012.
2.4. Statistical analysis, comparison, and evaluation of results
Results were analyzed as randomized complete block design
with food types as treatments and locations of sampling within a
country as replications. Analysis of variance (ANOVA) and orthogonal group comparisons were conducted using the SAS System for
Windows, Version 9. Data on bacterial cell counts were rst
transformed to log (base10) before the ANOVA. Furthermore, the
results of the microbiological tests were compared with available
microbiological guidelines for ready-to-eat foods, since street foods
are considered to be a part of this category. In this study, the
microbiological guidelines for RTE foods (FSANZ, 2001) served as
the bases for the evaluation of the microbiological quality of street

59

foods. The guidelines assign categories of microbiological quality of


RTE food as satisfactory (S), marginal (M), unsatisfactory (US), and
potentially hazardous (PH) or unacceptable based on standard or
aerobic plate counts, levels of indicator organisms, and the presence and numbers of pathogens.
3. Results and discussion
3.1. Hot-grilled chicken- and pork-based street foods
The microbiological quality of hot-grilled chicken and porkbased street foods, according to the FSANZ (2001) microbiological
guide, is presented in Table 1. Unsatisfactory levels of APC were
higher in Laguna hgc (33%) and hgp (20%) samples than those of
Taichung hgc (11%) and hgp (17%) samples. The mean APC counts of
hot-grilled samples ranged from 3.5  1.5 to 4.0  0.7 log cfu g1
(Table 2), and no signicant differences were observed between
Laguna and Taichung hgc and hgp samples (p 0.531). The highest
APC value of 8.2 log cfu g1 was observed in the Laguna hgp sample
(pork head). As compared to previous studies, the mean APC values
obtained in this survey were lower than those reported by Cho et al.
(2011) for various street foods, including hot meals in Korea with
the value of 4.71  1.53 log cfu g1. In the study reported by
Ologhobo et al. (2010), an APC value of 6 log cfu g1 was obtained
for Nigerian chicken roasted suya. Unsatisfactory levels of coliform
likewise were observed in Laguna hgc (13%) and hgp (12%).
Remarkably, no sample from Taichung was found unsatisfactory for
coliforms (Table 1). The mean coliform count ranged from 1.9  0.9
to 2.0  1.2 log cfu g1 (Table 2), and the highest coliform count of
5.4 log cfu g1 also was observed in Laguna hgp (pork liver). The
APC and coliforms are indicators of sanitation and could signify
unhygienic conditions during food handling and preparation.
E. coli, S. aureus and B. cereus were all detected in Laguna samples with unsatisfactory levels of 13%, 17%, and 4%, respectively, for
hgc samples, and 8%, 12%, and 4%, respectively, for hgp samples. The
results were greater than those obtained in Korean street food

Table 1
Microbiological quality of food types according to Guidelines for Microbiological Examination of RTE Foods, FSANZ (2001).
Microbiological guide

% Microbiological quality
Food types,a Taichung, Taiwan

Category

Aerobic plate count


S
M
US
Coliforms
S
M
US
E. coli
S
M
US
S. aureus
S
M
US
B. cereus
S
M
US
a

Food types,a Laguna, Philippines

Limit,

hgc

hgp

ccc

ccp

hgc

hgp

cfc

cfu g1

n 18

n 12

n 14

n6

n 24

n 25

n 20

<104
<105
105

50
39
11

42
42
17

0
0
100

0
0
100

50
17
33

76
4
20

75
10
15

102
102e104
104

61
39
0

75
25
0

0
36
64

0
50
50

21
67
13

40
48
12

50
50
0

<3
3e100
100

100
0
0

100
0
0

29
43
29

100
0
0

83
4
13

92
0
8

100
0
0

102
102e103
103e104

100
0
0

100
0
0

43
36
21

83
0
17

79
4
17

88
0
12

95
5
0

102
102e103
103e104

100
0
0

100
0
0

79
21
0

83
17
0

96
0
4

96
0
4

100
0
0

Food type: hgc hot-grilled chicken; hgp hot-grilled pork; ccc cold-cooked chicken; ccp cold-cooked pork; cfc cold fried-chicken.
Category: S Satisfactory, results indicate good microbiological quality; M Marginal, results are borderline in that they are within limits of acceptable microbiological
quality but may indicate possible hygiene problems in the preparation of the food; US Unsatisfactory, results are outside of acceptable microbiological limits and are
indicative of poor hygiene or food handling practices.
b

60

L.S. Manguiat, T.J. Fang / Food Microbiology 36 (2013) 57e62

Table 2
Bacterial counts of chicken- and pork-based street foods from Taichung, Taiwan and Laguna, Philippines.
Food typea

Sample size, n

Taichung
hgc

18

hgp

12

ccc

14

ccp

Laguna
hgc

24

hgp

25

cfc

20

a
b
c
d

Mean bacterial counts (log cfu g1)


APCb

Coliform

E. coli

S. aureus

B. cereus

4.0 (0.7)c
(2.1e5.1)d
3.8 (1.1)
(1.3e5.1)
5.7 (0.6)
(5.1e6.5)
5.6 (0.5)
(5.1e6.4)

1.9 (0.9)
(<1.0e3.52)
1.5 (0.9)
(<1.0e3.4)
4.3 (0.7)
(3.1e5.4)
3.9 (0.5)
(3.1e4.4)

<1.0 (0.0)

<1.0 (0.0)

<10.0 (0.0)

<1.0 (0.0)

<1.0 (0.0)

<10.0 (0.0)

2.2 (1.3)
(<1.0e4.7)
<1.0 (0.0)

1.8 (0.9)
(<1.0e3.4)
1.3 (0.9)
(<1e3.1.0)

2.0 (0.2)
(<2.0e2.5)
2.2 (0.5)
(<2.0e3.2)

3.5 (1.5)
(1.0e5.6)
3.5 (1.6)
(1.4e8.2)
2.8 (1.3)
(1.0e5.4)

2.0 (1.2)
(<1.0e4.4)
1.9 (1.4)
(<1.0e5.4)
1.4 (0.8)
(<1.0e3.4)

1.4 (0.9)
(<1.0e4.4)
1.3 (0.8)
(<1.0e4.4)
1.2 (0.4)
(<1.0e2.0)

1.2 (0.6)
(<1.0e3.0)
1.3 (1.0)
(<1.0e3.9)
1.4 (0.7)
(<1.0e2.4)

2.0 (0.4)
(<2.0e3.9)
2.0 (0.4)
(<2.0e4.0)
<2.0(0.0)

Food type: hgc hot grilled chicken; hgp hot grilled pork; ccc cold cooked chicken; ccp cold cooked pork; cfc cold fried chicken.
Aerobic plate count.
Numbers in parentheses indicate standard deviation.
Numbers in parentheses indicate range of bacterial counts.

samples, i.e., 3%, 9%, and 3%, respectively (Cho et al., 2011). In
another study, E. coli was detected in 5 of 43 (11.6%) of grilledchicken samples from street vendors in Mexico, while S. aureus
was detected in 4 of 43 (9.3%) of such samples (Diaz-Lopez et al.,
2011). In contrast, these pathogens were not detected in any of
the Taichung hot-grilled samples (Table 1), which had a 100%
satisfactory rating.
Salmonella was detected in one of the 25 (4%) Laguna hgc
samples (intestines) and in three of the 25 (12%) Laguna hgp
samples (liver, meat, head, and sausage). The pathogen was also
detected in three (17%) Taichung hgc samples (heart, intestine,
blood) and one (8%) hgp samples (sausage) (data not shown). The
detection of Salmonella spp. in a 25-g sample is considered
potentially hazardous or unacceptable according to the microbiological guide that was used. The Salmonella isolated from the positives samples were serotyped as Salmonella Typhimurium. The
prevalence of Salmonella in RTE and street foods has been reported
in various studies. Diaz-Lopez et al. (2011) reported a higher
prevalence of Salmonella in grilled chicken from street vendors than
in retail outlets. Yan et al. (2010) reported that 81 Salmonella isolates were recovered in 20.9% of retail foods, including chicken and
pork meats. The presence of this pathogen has been associated with
inadequate cooking, cross-contamination from an unhygienic
environment, and food handlers.
L. monocytogenes and E. coli O157 were not detected in any of the
hgc and hgp samples from any sampling sites, signifying the adequacy of the grilling process. These ndings agree with those reported by Diaz-Lopez et al. (2011), wherein L. monocytogenes and
E. coli (shiga toxin and enterotoxin producer) were not detected in
any of the 43 samples of grilled chicken.
Appropriate food preparation, including sufcient cooking, is a
critical contributor to the safety of food. In this survey, the streetfood samples had undergone cooking, such as grilling for hgc and
hgc, boiling for ccc and ccp, and frying for cfc, as heat treatments
and kill steps to destroy the microorganisms in the food. Prior to
consumption, perishable, uncured meats should be cooked fully to
an internal temperature of at least 70  C to eliminate vegetative
infectious pathogenic bacteria (ICMSF, 2005). Although hgc and
hgp were cooked or heated before selling, some samples were still
found unsatisfactory and unacceptable because they had bacterial
counts above the microbiological limits established by FSANZ. Like
any other street foods, poor food preparation and handling and

inadequate cooking can result in unsatisfactory microbial quality.


The high bacterial counts and presence of some pathogens suggested that grilling was sometimes inadequate to destroy microorganisms in some hgc and hgp samples. Under-grilling is
sometimes done intentionally to minimize food shrinkage. Also, the
poor microbial condition of the raw materials may contribute to the
unsatisfactory quality of the grilled food. No analyses were done for
the raw foods in this study, but raw chicken and pork and their
entrails are known to have high microbial loads due to their compositions, which favor the growth of microorganisms (ICMSF, 2005;
Van Nierop et al., 2005; Yan et al., 2010).
Aside from inadequate grilling, contamination in hot-grilled
foods may come from uncooked and contaminated ingredients,
such as condiments and spices (e.g., pepper and chili) that usually
are added after grilling. While sufcient grilling destroys the bacteria, cross contamination by these ingredients is very likely.
Nonetheless, overall results showed that many of the Taichung and
Laguna hot-grilled, street foods were satisfactory and safe for
consumption.
3.2. Cold-cooked chicken- and pork-based street foods
These types of foods were those that were prepared and cooked
earlier and brought to the street vending stores to be sold. In this
study, samples from Taichung were the stewed-moist type (ccc and
ccp), while those from Laguna were the fried-dry type (cfc). As a
usual practice, no further cooking of these types of food occurs at
the point of sale. The foods are held and sold at ambient temperature, which promotes the growth of mesophilic microorganisms
and most pathogens (Jay et al., 2005).
The quality of ccc and ccp samples, according to the microbiological guide, was rated 100% unsatisfactory for APC in all samples
(Table 1), because these samples all had APC counts of >5 log
cfu g1 (Table 2). Nine (64%) ccc and 36 (50%) ccp samples were
found to be unsatisfactory based on their coliforms counts, which
were >4 log cfu g1. E. coli was detected in 10 (72%) of the ccc
samples, four of which (29%) (skin, buttocks, neck, and feet) were
found to be unsatisfactory because they had counts that were >2
log cfu g1 (Table 2). However, E. coli was not detected in any of the
ccp samples. The high levels of contamination were a clear indication of poor hygiene and sanitation. The cold-cooked food type,
although thoroughly cooked, may have been contaminated during

L.S. Manguiat, T.J. Fang / Food Microbiology 36 (2013) 57e62

handling and storage since it is held at ambient temperature.


S. aureus was detected in 8 (57%) of the ccc samples, 3 (21%) of
which (neck, feet, and skin) were found unsatisfactory with counts
>3 log cfu g1 (Table 1). The pathogen was also detected in one ccp
sample (sausage) with an unsatisfactory rating.
Although high in APC and coliform counts, Salmonella, E. coli
O157 and L. monocytogenes were not detected in any of the ccc and
ccp samples (Table 3) from Taichung, an indication that no cross
contamination from these pathogens had occurred during
handling. Nevertheless, monitoring of the quality of street food as a
precautionary measure should be conducted regularly because
handling conditions and situations vary and can compromise the
foods microbial safety and quality.
For the cfc food type collected from Laguna, 3 samples (15%) had
unsatisfactory ratings for APC. No unsatisfactory rating was noted
for coliforms (Table 1). E. coli, B. cereus, L. monocytogenes, and E. coli
O157 were not detected in any of the samples. However, S. aureus
was detected in one sample with a mean count of 2.4 log cfu g1.
One sample (chicken intestine) was found to be positive for Salmonella and also was serotyped as Typhimurium.
3.3. Comparison of hot-grilled and cold-cooked or fried samples
Hot-grilled street foods (hgc, hgp) collected in Taichung had
better microbiological quality than the cold-cooked samples (ccc,
ccp) for almost all parameters tested (p 0.001), except for Salmonella, which was detected in 3 hgc samples and 1 hgp sample.
Similarly, hot-grilled pork (hgp) and cold-cooked pork (ccp)
showed that the hgp samples exhibited better quality. Comparison
of means between bacterial counts of hot-grilled and cold-cooked
food types revealed highly signicant differences for APC, coliforms, E. coli, and S. aureus (p 0.001), with the cold-cooked
samples having higher levels of contamination. There could be
several reasons for the unsatisfactory levels, including cross
contamination from unsanitary raw ingredients and contact with
contaminated surfaces, improper handling of the food, vendors
inadequate knowledge of food hygiene, and inadequate or unavailable cold storage. Improper handling and holding the cooked
food at ambient temperature were observed in all stores. In addition, cooked foods were left uncovered and exposed to microbial
contaminants during the entire selling period.
Comparison of the microbiological qualities of the hgc and cfc
samples collected from Laguna revealed no signicant differences
in APC, coliforms, E. coli, and S. aureus counts. However, signicant
difference was noted for the B. cereus count (p 0.023), with hgc
having a higher mean count.

61

3.4. Antimicrobial susceptibility of bacterial isolates


In this survey, the antimicrobial susceptibility proles of S.
Typhimurium, E. coli, and S. aureus isolated from various street-food
samples were determined. Four S. Typhimurium isolates from
chicken (3) and pork (1) exhibited multi-resistance to ampicillin,
amoxycillin/clavulanic, and chloramphenicol; they also exhibited
intermediate resistance to tetracycline, but they were found to be
susceptible to other antimicrobial agents (data not shown). Previous studies also have revealed the prevalence and antimicrobial
resistance of Salmonella isolated from retail and street restaurants
(Yan et al., 2010; Dione et al., 2009; Harakeh et al., 2005).
Four E. coli isolates from chicken were found resistant to ampicillin, six isolates (ve chicken, 1 pork) to tetracycline, two isolates
(chicken) to sulphamethoxazole/trimethroprim, and one isolate
(chicken) to chloramphenicol. Two E. coli isolates from chicken
exhibited multi-resistance to four antimicrobial agents (ampicillin,
tetracycline, chloramphenicol, and sulphamethoxazole/trimethroprim). S. aureus isolates from two chicken samples and one pork
sample were found to be resistant to fusidic acid. An isolate from
pork was found resistant to oaxacin and tetracycline. Studies
conducted by Guven et al. (2010) and Rhee and Woo (2010) revealed
that several strains of S. aureus isolated from meat, dairy, and food
products were resistant to some antibiotics. Likewise, in Taiwan, Lin
et al. (2009) found 207 S. aureus strains isolated from pork and
chicken carcasses to be resistant to several antimicrobial agents.
It is a major concern to obtain information on the antimicrobial
susceptibility proles of bacteria isolated from foods, because these
foods could be public health hazards by act as vehicles for many
antimicrobial-resistant pathogenic organisms. Salmonella spp. and
S. aureus are considered health risks and are leading causes of
foodborne infections (Guven et al., 2010; Harakeh et al., 2005). As
the prevalence of multi-drug resistance Salmonella strains and the
methicillin-resistant S. aureus (MRSA) increases, these bacteria
have the potential for becoming worldwide health threats. The
results from this study revealed that some of the E. coli, S. aureus,
and Salmonella isolated from chicken- and pork-based street foods
exhibited antimicrobial resistance.
4. Conclusions
The results showed that several hot-grilled and cold-cooked
street foods that were included in the study exhibited unsatisfactory and unacceptable microbiological quality that posed health
risks for consumers. In addition, some microorganisms that were
isolated from the samples showed antimicrobial resistance, which

Table 3
Pathogenic microorganisms detected in chicken- and pork-based street foods collected from studied areas in Taichung, Taiwan and Laguna, Philippines.
% Pathogenic microorganism detected
Taichung

Escherichia coli
Staphylococcus aureus
Bacillus cereus
Salmonella spp
Listeria monocytogenes
Escherichia coli O157
a
b
c
d
e

hgc hot-grilled chicken.


hgp hot grilled pork.
ccc cold-cooked chicken.
ccp cold-cooked pork.
cfc cold-fried chicken.

Laguna

hgca

hgpb

cccc

ccpd

n 18

n 12

n 14

n6

n 24

n 25

n 20

nd
nd
nd
17
nd
nd

nd
nd
nd
8
nd
nd

72
57
21
nd
nd
nd

nd
17
17
nd
nd
nd

17
21
4
4
nd
nd

8
12
4
12
nd
nd

25
5
nd
5
nd
nd

hgc

hgp

cfce

62

L.S. Manguiat, T.J. Fang / Food Microbiology 36 (2013) 57e62

further increases the risks associated with these foods. Therefore,


there is a need to continuously educate street-food vendors on food
hygiene and sanitation, and the microbial quality of street foods
should be assessed on a regular basis to acquire sufcient data for
use in conducting microbial risk assessments.
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