Food Control 44 (2014) 203e207

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Food Control
journal homepage: www.elsevier.com/locate/foodcont

Antimicrobial resistance of Escherichia coli and Staphylococcus aureus

isolated from food handler’s hands
S.L. Tan a, H.Y. Lee b, N.A. Mahyudin a, b, *
a
Department of Food Service and Management, Faculty of Food Science and Technology, Universiti Putra Malaysia, 43400 UPM Serdang, Selangor Darul
Ehsan, Malaysia
b
Department of Food Science, Faculty of Food Science and Technology, Universiti Putra Malaysia, 43400 UPM Serdang, Selangor Darul Ehsan, Malaysia

a r t i c l e i n f o a b s t r a c t

Article history: The aim of this study was to determine the antimicrobial resistance of Escherichia coli and Staphylococcus
Received 11 October 2013 aureus isolates from food handlers’ hands at primary schools in Hulu Langat district, Selangor (Malaysia).
Received in revised form Disc diffusion methods were used to examine the antimicrobial resistance of the bacteria by using ten
2 April 2014
types of antibiotic discs with different concentrations. The results show that the prevalence of S. aureus
Accepted 3 April 2014
Available online 13 April 2014
(65.88e74.12%) was far higher than the prevalence of E. coli (9.41e14.12%). The percentage isolates of
E. coli that were resistant to the antibiotics was 85.71% Penicillin and Chloramphenicol, 57.14%
Sulfamethoxazole-Trimethoprim, Ampicillin and Trimethoprim, 28.57% Kanamycin and Tetracycline and
Keywords:
Antibiotic discs
14.29% Ciprofloxacin. All of the isolates had shown susceptible to Gentamicin and Nitrofurantoin. For
Escherichia coli S. aureus, the percentage isolates that were resistant to the antibiotics was 72.30% Ampicillin, 53.38%
Food handlers’ hands Penicillin, 4.73% Nitrofurantoin,1.35% Chloramphenicol and Trimethoprim and 0.68% Kanamycin and
Multidrug resistant bacteria Tetracycline. None of the isolates had shown resistant to Ciprofloxacin, Sulfamethoxazole-Trimethoprim
Staphylococcus aureus and Gentamicin. Multidrug resistant Escherichia coli represented a high percentage (85.71%) of the total
positive strains revived whereas multidrug resistant S. aureus strains were only 5.41% of the total positive
strains. The existence of multidrug resistant bacteria is quite worrying as they may pose serious threat to
the patients. Hence, the microbiological quality of food handlers’ hands from foodservice operations
should be maintained in a good condition to reduce the existence of multidrug resistance bacteria.
Ó 2014 Elsevier Ltd. All rights reserved.

1. Introduction their mechanisms of action: inhibit cell wall synthesis, inhibit

Antimicrobial resistant bacteria are a serious issue as they could
pose a serious threat to the patients. Antibiotics are antimicrobial
agents that are produced naturally by microorganisms to inhibit or
destroy microbial growth in the infected host. They are members of
an extremely diverse group of metabolic products known as sec-
ondary metabolites, which are complex organic molecules that are
not essential for normal cell growth and reproduction and are
produced only after an organism has established itself in its envi-
ronment. The ideal antibiotics to treat an infection must be readily
available, inexpensive, chemically stable, easily administered, non-
toxic and non-allergenic to human (Bauman, 2004; Cowan & Talaro,
2009). There are five main categories of antibiotics according to
* Corresponding author. Department of Food Service and Management, Faculty of
Food Science and Technology, Universiti Putra Malaysia, 43400 UPM Serdang,
Selangor Darul Ehsan, Malaysia. Tel.: þ60 3 8946 8375; fax: þ60 3 8942 3552.
E-mail address: norainy@food.upm.edu.my (N.A. Mahyudin).
protein synthesis, alter cell membranes, anti metabolites and
inhibit nucleic acid synthesis. To ascertain the efficacy of antibi-
otics, diffusion susceptibility tests also known as KirbyeBauer
technique, is an agar diffusion test that provides useful data on
antimicrobial susceptibility. This method was widely used on the
determination of antimicrobial resistance of the bacteria isolated
from food or hands of food handlers (Akond, Alam, Hassan, & Shirin,
2009; Albuquerque, Macrae, Sousa, Vieira, & Vieira, 2007; Harakeh
et al., 2005; Miranda et al., 2009; Normanno et al., 2007; Pesavento,
Ducci, Comodo, & Nostro, 2007; Sasidharan, Prema, & Yoga Latha,
2011). In Tan, Bakar, Abdul Karim, Lee, and Mahyudin (2013)
report on food hygiene practices by food handlers in Malaysia
that the least practiced habits were hand washing and the usage of
face mask during food preparation. This would facilitate the
transmission of bacteria such as Staphylococcus aureus into food,
and due to the different background of food handlers, carriers of
multiple resistant S. aureus can contribute to the widespread of
antibiotic resistance of S. aureus. In community-acquired infections,

http://dx.doi.org/10.1016/j.foodcont.2014.04.008
0956-7135/Ó 2014 Elsevier Ltd. All rights reserved.
204 S.L. Tan et al. / Food Control 44 (2014) 203e207

Escherichia coli and S. aureus are the most frequently isolated bac-
teria (Thibaut et al., 2010).
As more bacteria become resistant to traditional antibiotics, this
leads to emergence and re-emergence of multidrug-resistant
pathogens (Abulreesh & Organji, 2011; Acco, Ferreira, Henriques, &
Tondo, 2003; Akond et al., 2009; Albuquerque et al., 2007; Lei
et al., 2010; Platell, Johnson, Cobbold, & Trott, 2011; Simeoni et al.,
2008). This study was performed to determine the antimicrobial
resistance of E. coli and S. aureus isolates from food handlers’ hands
at primary schools in Hulu Langat district, Selangor (Malaysia). Re-
sults of this study may be applicable as useful information related to
multidrug resistant bacteria found on food handlers’ hands.
2. Materials and methods
2.1. Sampling and culturing procedures
A total of 1020 samples were collected from 85 food handlers’ hands
at 38 primary schools in Hulu Langat district. Microbiological analysis
was conducted on food handlers’ hands to test for APC (Aerobic Plate
Count), E. coli/coliform and S. aureus counts. Samples were collected
from the right and left palms of the food handlers in duplicate. The
collection was done during weekdays (06:00e10:00) at the following
intervals; before, during and after preparation of ready-to-eat (RTE)
foods such as ‘nasi lemak’, sandwiches, fried foods and burgers.
Sterile swabs (Premier, China) were removed from pre-coded
test tubes that contained 5 ml of 1  sterile phosphate-buffered
saline with pH 7.4  1 (Oxoid, Basingstoke, UK) and the targeted
areas (palms of food handlers) were swabbed. Sampling was per-
formed by swabbing the areas horizontally, vertically and diago-
nally by using aluminum templates with the size of 2 cm  5 cm.
The whole procedures were done aseptically to minimize the risk of
contamination. Swabs were then placed back into the pre-coded
test tubes. The collected samples were stored and transported in
insulated boxes filled with crushed ice prior to analysis. The storage
temperature was within 0e4  C while the transport duration to the
laboratory was within 15 min to 1 h. Analyses were performed
immediately upon arrival to the laboratory.
Each of the food handlers’ palms was analyzed for APC, E. coli/
coliform and S. aureus counts by using Petrifilm APC, Petrifilm
E. coli/coliform and Petrifilm STX Count Plates respectively (3M
Microbiology, St. Paul, USA). Swab contact method on Petrifilm
plates was used to evaluate APC, E. coli/coliform and S. aureus
counts on food handlers’ palms (Evancho, Sveum, Moberg, & Frank,
2001).
2.2. Isolation and identification of E. coli and S. aureus
Single colony of E. coli and S. aureus for each sample from the
food handlers’ hands were isolated stored at 20  C until further
examinations (Baldwin, Ziegler, Green, & Thomas, 2000; Portle,
2009; StockingerLab, 2001). The colonies were identified through
a series of biochemical (physiological) tests as described in Bergey
and Holt (1994). Before the biochemical tests were held, the isolates
were revived on nutrient agar to obtain fresh cultures. Gram
staining, catalase test and mannitol salt agar were used to identify
suspected S. aureus isolates while Gram staining, oxidase test,
agar (Wikler, 2006). Ten types of antibiotic discs with different
concentrations were used. The antibiotic discs used were Penicillin
(10 mg), Ampicillin (10 mg), Gentamicin (10 mg), Kanamycin (30 mg),
Tetracycline (30 mg), Chloramphenicol (30 mg), Trimethoprim (5 mg),
Sulfamethoxazole-Trimethoprim (25 mg), Ciprofloxacin (5 mg) and
Nitrofurantoin (300 mg). These antibiotics were chosen based on
their different molecular structures and modes of action and must be
effective against both Gram-negative and Gram-positive infections.
The diameters of zones were measured to the nearest whole milli-
meter and the bacteria were categorized into resistant, intermediate
and susceptible as mentioned in Wikler (2007). CLSI 2006 shows the
disc diffusion methods whereas CLSI 2007 shows the susceptibility
of bacteria (resistant, intermediate or susceptible).
2.4. Statistical analysis
Statistical analyses were performed using SPSS Statistics version
19. Frequencies and percentages were calculated for all variables as
appropriate.
3. Results and discussion
3.1. Prevalence of E. coli and S. aureus on food handlers’ hands
Table 1 displays the prevalence of E. coli and S. aureus on 85 food
handlers’ hands before, during and after RTE foods preparation. The
results showed that the prevalence of S. aureus (65.88e74.12%) was
significantly higher (P < 0.05) than the prevalence of E. coli (9.41e
14.12%). The high prevalence of S. aureus among the food handlers
may indicate that they did not maintain good personal hygiene
when handling RTE foods. It also may be due to the contamination
introduced by food handlers through skin lesions or by sneezing or
coughing (Bischoff, Wallis, Tucker, Rebouyssin, Pfaller, Hayden &
Sherertz, 2006). As hygiene practices reported by Tan et al.
(2013), hand washing practices and face mask are not commonly
used by food handlers may cause the higher prevalence of S. aureus
from the hands. Fortunately, the prevalence of E. coli was quite low
compared to S. aureus. For E. coli, they existed most often after the
preparation of RTE foods (14.12%) and they was the same (9.41%) for
both before and during the preparation of RTE foods whereas for
S. aureus, they existed most frequently before RTE foods prepara-
tion (74.12%)and reduced after (70.59%) and during (65.88%) the
preparation of RTE foods. Statistical analyses found there were no
significant (P > 0.05) difference in the mean log cfu/cm2 for E. coli ,
S. aureus and APC on the food handlers’ hands for the three in-
tervals of food preparation. The increased occurrence of E. coli after
food preparation may also due to the cross contamination of the
food to the food handlers’ hands. From observation, some food
Table 1
Mean of E. coli and S. aureus on 85 food handlers’ hands before, during and after RTE
foods preparation.
Intervals E. coli S. aureus Statistical
a difference
Mean Percentage Mean  Percentage
(P < 0.05)
(log10 (%) standard (%)
CFU/cm2) deviation
(log10 CFU/cm2)

lactose fermentation, indole and citrate tests were used to identify Before 0.2b ± 0.4 9.41 0.5a ± 0.7 74.12 F ¼ 8.855;
presumptive E. coli isolates. In addition, culture characteristics of P ¼ 0.003
a
During 0.2 ± 0.4 9.41 0.3 ± 0.5 65.88 F ¼ 3.412;
the bacteria were also observed.
P ¼ 0.066
After 0.2b ± 0.4 14.12 0.4a ± 0.7 70.59 F ¼ 5.317,
2.3. Antimicrobial disc susceptibility tests P ¼ 0.022
a
Data were reported as mean  standard deviation for four replicates (log10 CFU/
Disc diffusion methods were used to examine the antimicrobial cm2).
b
resistance of S. aureus and E. coli isolates on sterile MuellereHinton Significant difference between E. coli and S. aureus.
 S.L. Tan et al. / Food Control 44 (2014) 203e207 205

handlers do not wash their hands while some do not practice
proper handwashing procedures. Although the prevalence of E. coli
inspected from food handlers’ hands were low, attention should be
given as the E. coli due to the frequent association of community/
hospital acquired infections to this bacteria (Ayçiçek, Aydog an,
Küçükkaraaslan, Baysallar, & Başustaog lu, 2004). This finding is in
contrast to Thibaut et al. (2010), where the isolation of E. coli strains
from community acquired infection were very high (90.6%) for
E. coli and 9.4% for S. aureus. In their study, majority of the isolation
of E. coli was from urine samples which are a common cause of
urinary tract infections (UTIs). Since only food handlers’ palms
were swabbed, it is not surprising to find a lower prevalence of
E. coli in this study in comparison to Thibaut et al. (2010). Few
reasons could attribute to this finding whereby practices of food
handlers whereby in (Tan et al., 2013) hand washing after using the
toilet was practiced among 93.5% of the food handlers in their study
or the possible cross contamination of E. coli originated from the
food prepared. Since E. coli can be readily isolated from many food
sources, the practices at the farm level for antimicrobial therapy for
the poultry farms may lead to a cross contamination of resistant
bacteria in food.
Soares, Almeida, Cerqueira, Carvalho, and Nunes (2012) had
reported that during food preparation and distribution of meals in
the schools of Brazil, there was 53.3% of the food handlers’ hands
were detected for coagulase-positive staphylococci. Seventy
percent of S. aureus and 7.8% of E. coli had been isolated from bare
and gloved hands before and during food preparation in a military
training hospital in Turkey (Ayçiçek et al., 2004). Besides, there
were also several other studies that had reported on the occurrence
of E. coli and S. aureus from the food handlers’ hands in the com-
mercial foodservice operations. Akond et al. (2009) had reported
that there were 46% of samples detected with E. coli from the hand
wash of chicken handlers from different poultry markets in
Bangladesh. Sixty percent of the nasal swabs of food handlers from
the food environment in Saudi Arabia were tested positive for
coagulase-positive staphylococci (Abulreesh & Organji, 2011).
S. aureus were present on 88% of the hands of food handlers in a
retail group in South Africa (Lues & Van Tonder, 2007). As a results
obtained from the above studies and also the present study, more
than half of the S. aureus strains were isolated from the food han-
dlers which showed that the personal hygiene of food handlers was
not satisfied and need to be emphasized.
3.2. Antimicrobial disc susceptibility tests for E. coli
Out of 28 isolates of E. coli, only seven isolates were tested
positive for antibiotic resistance. Table 2 demonstrates the
antimicrobial resistance of seven positive isolates of E. coli on food
handlers’ hands. The percentage isolates of E. coli that were resis-
tant to the antibiotics was 85.71% (Penicillin and Chloramphenicol),
57.14% (Ampicillin, Trimethoprim and Sulfamethoxazole-
Trimethoprim), 28.57% (Kanamycin and Tetracycline) and 14.29%
(Ciprofloxacin). A high percentage of E. coli isolated from food
handlers in this study was resistant to Penicillin and Chloram-
phenicol that inhibit cell walls and protein synthesis (elongation
step). All of the isolates had shown susceptibility to Gentamicin and
Nitrofurantoin. Both Gentamicin and Nitrofurantoin were effective
against E. coli by inhibiting protein synthesis (initiation step) and
nucleic acid synthesis respectively. Only 14.29% of the E. coli was
recorded to be intermediate resistant to Penicillin and Ampicillin.
Study from Akond et al. (2009) recorded that none of the E. coli
strains isolated from the poultry sources (included chicken han-
dlers’ hands were either resistant to Gentamicin or sensitive to
Kanamycin, Penicillin and Ciprofloxacin). It had been identified that
51.3% of pathogenic E. coli that were isolated from stool samples of
the food handlers shown resistant to Sulfamethoxazole-
Trimethoprim that inhibit folate synthesis pathway.
Foods that contain high frequency of bacteria (e.g. E. coli) such as
poultry products from Spain (Sáenz et al., 2001) and meat-based
fast food from Lebanon (Harakeh et al., 2005) have higher chance
of transfer onto the hands of food handlers during preparation of
food. This is because Gungor and Gokoglu (2010) and Gorman,
Bloomfield, and Adley (2002) had stated in their studies that
there was a possibility of cross-contamination between food and
food preparation surfaces (such as food handlers’ hands). So, it is
important for the food handlers in the foodservice operations to
maintain good hand hygiene as bacteria may transfer from food to
hand and eventually to the food that school children will be
consumed.
3.3. Antimicrobial disc susceptibility tests for S. aureus
There were 148 out of 179 S. aureus isolates were tested positive
for antibiotic resistance. Table 3 demonstrates the antimicrobial
resistance of selected 148 of S. aureus on food handlers’ hands. The
percentage isolates of S. aureus that were resistant to the antibiotics
was 72.30% (Ampicillin), 53.38% (Penicillin), 4.73% (Nitro-
furantoin),1.35% (Chloramphenicol and Trimethoprim) and 0.68%
(Kanamycin and Tetracycline). None of the isolates had shown
resistant to Ciprofloxacin, Sulfamethoxazole-Trimethoprim and
Gentamicin. The range for S. aureus that had shown intermediate
resistant to the antibiotics was 1.35e4.05%. The percentage isolates
that were susceptible to the antibiotics was 100% (Sulfamethoxa-
zole-Trimethoprim and Gentamicin), 98.65% (Ciprofloxacin and

Table 2
Antimicrobial resistance of seven positive isolates of E. coli on food handlers’ hands.

Antibiotics Resistant Intermediate Susceptible

Positive Zone Positive Zone Positive Zone

strains n (%) diameter strains n (%) diameter strains n (%) diameter
(mm) (mm) (mm)

Penicillin (10 mg) 6 (85.71) 13 1 (14.29) 14e16 e 17

Ciprofloxacin (5 mg) 1 (14.29) 15 e 16e20 6 (85.71) 21
Chloramphenicol (30 mg) 6 (85.71) 12 e 13e17 1 (14.29) 18
Sulfamethoxazole-Trimethoprim 4 (57.14) 10 e 11e15 3 (42.86) 16
(25 mg)
Ampicillin (10 mg) 4 (57.14) 13 1 (14.29) 14e16 2 (28.57) 17
Gentamicin (10 mg) e 12 e 13e14 7 (100.00) 15
Kanamycin (30 mg) 2 (28.57) 13 e 14e17 5 (71.43) 18
Tetracycline (30 mg) 2 (28.57) 11 e 12e14 5 (71.43) 15
Trimethoprim (5 mg) 4 (57.14) 10 e 11e15 3 (42.86) 16
Nitrofurantoin (300 mg) e 14 e 15e16 7 (100.00) 17

Note: Percentage of positive strains obtained was from mean of four replicates.
206 S.L. Tan et al. / Food Control 44 (2014) 203e207

Table 3
Antimicrobial resistance of 148 positive isolates of S. aureus on food handlers’ hands.

Antibiotics Resistant Intermediate Susceptible

Positive strains Zone Positive Zone Positive strains Zone

n (%) diameter strains n diameter n (%) diameter
(mm) (%) (mm) (mm)

Penicillin (10 mg) 79 (53.38) 28 e e 69 (46.62) 29

Ciprofloxacin (5 mg) e 15 2 (1.35) 16e20 146 (98.65) 21
Chloramphenicol (30 mg) 2 (1.35) 12 e 13e17 146 (98.65) 18
Sulfamethoxazole-Trimethoprim e 10 e 11e15 148 (100.00) 16
(25 mg)
Ampicillin (10 mg) 107 (72.30) 28 e e 41 (27.70) 29
Gentamicin (10 mg) e 12 e 13e14 148 (100.00) 15
Kanamycin (30 mg) 1 (0.68) 13 5 (3.38) 14e17 142 (95.95) 18
Tetracycline (30 mg) 1 (0.68) 14 6 (4.05) 15e18 141 (95.27) 19
Trimethoprim (5 mg) 2 (1.35) 10 4 (2.70) 11e15 142 (95.95) 16
Nitrofurantoin (300 mg) 7 (4.73) 14 e 15e16 141 (95.27) 17

Note: Percentage of positive strains obtained was from mean of four replicates.

Chloramphenicol), 95.95% (Kanamycin and Trimethoprim), 95.27%
(Tetracycline and Nitrofurantoin), 46.62% (Penicillin) and 27.70%
(Ampicillin). Antibiotics that were effective against S. aureus were
Sulfamethoxazole-Trimethoprim that inhibit folate synthesis
pathway and Gentamicin that inhibit protein synthesis (similar to
E. coli).
In Kuwait City restaurants, S. aureus isolated from the food
handlers were resistant to Penicillin G, Tetracycline, Trimethoprim,
Kanamycin and Gentamicin within the range of 0.5e82.0% (Udo, Al-
Mufti, & Albert, 2009). Finding from Abulreesh and Organji (2011)
had shown that all of the coagulase-positive staphylococci iso-
lates that were recovered from the nasal mucosa of food handlers
were resistant to Penicillin G. All of the S. aureus strains isolated
from a fish market and from fish handlers were resistant to
Ampicillin (Albuquerque et al., 2007). Seventy percent of the
S. aureus strains isolated from nasal mucosa of food handlers in
Porto Alegre, Southern Brazil were resistant to Penicillin. All of the
strains that were tested positive for S. aureus from nasal mucosa of
food handlers were sensitive to Chloramphenicol and Gentamicin
(similar to the result from this study) (Acco et al., 2003). All of the
S. aureus isolated from a small dairy plant (included food handlers’
anterior nares and hands) in Brazil had shown susceptible to Cip-
rofloxacin and Gentamicin which is supported by the present re-
sults (André et al., 2008).
3.4. Multidrug resistant E. coli
Multidrug resistant E. coli on the hands of food handlers were
shown in Table 4 below. As defined by Gibbs et al. (2006), multidrug
resistant bacteria were those resistant to at least two classes of
antibiotics. Multidrug resistant E. coli represented a high percent-
age (85.71%) of the total positive E. coli strains revived. Only 14.29%
of the E. coli strains did not resistant to any of the antibiotics tested.
According to the table, there was a multidrug resistant E. coli strain
resistant to six antibiotics (P, C, SXT, AMP, TE and W) from three
different antimicrobial classes and another multidrug resistant
E. coli strain resistant to seven antibiotics (P, CIP, C, SXT, AMP, TE and
W) from four different antimicrobial classes.
Comparison of nationality on multidrug resistant E. coli strains
present study, multidrug resistant E. coli had been discovered in all
of the isolates obtained from the food handlers in Bangladesh
(Akond et al., 2009). As a result, precaution should be taken as the
high cases of multidrug resistant E. coli may bring harmful effect to
the consumer, in this case, the school children.
3.5. Multidrug resistant S. aureus
Multidrug resistant S. aureus on the hands of food handlers were
shown in Table 5 below. From the total of positive S. aureus strains,
5.41% of them represented the multidrug resistant S. aureus and
94.59% of the strains did not resistant to all of the antibiotics or only
resistant to one of the antibiotics tested. There was a multidrug
resistant S. aureus resistant to four antibiotics (P, AMP, K and W)
from three different antimicrobial classes and the rest of them
resistant to only two antibiotics from two different antimicrobial
classes. Multidrug resistant S. aureus were detected on five non-
Malaysian food handlers and three Malaysian food handlers.
Exposure to pathogenic S. aureus by non-Malaysian food handlers
was slightly higher than the local food handlers. This outcome
maybe because of the different background of non-Malaysian food
handlers and their exposure to hygiene practices in the country.
Multidrug resistant S. aureus isolated from food handlers had been
described in various studies such like Acco et al. (2003), Abulreesh
and Organji (2011) and Albuquerque et al. (2007). In United States,
52% of the S. aureus isolated from meat and poultry samples were
also resistant to multidrug including Tetracycline, Penicillin and
Ampicillin (Waters et al., 2011).
4. Conclusions
The existence of multidrug resistant bacteria may pose serious
threat to the patients, hence, the microbiological quality on food
Table 4
Multidrug resistant E. coli on the hands of food handlers.
Antibiotics n (%) Nationality
Malaysian Non-Malaysian

showed that the strains were mostly detected (five food handlers) None 1 (14.29) 0 1
on Malaysian food handlers’ hands whereas only one food handler P and C 2 (28.57) 2 0
P, C, SXT, AMP, K and W 2 (28.57) 2 0
which is non-Malaysian had found to have multidrug resistant
P, C, SXT, AMP, TE and W 1 (14.29) 1 0
E. coli on her hand. There was a different exposure of backgrounds P, CIP, C, SXT, AMP, TE and W 1 (14.29) 0 1
to microbes from home country. As in Malaysia, the chances for Total 7 (100.00) 5 2
food handlers exposed to pathogenic E. coli were higher compared Note: n ¼ number of positive E. coli strains, P ¼ Penicillin, CIP ¼ Ciprofloxacin,
to Indonesian food handlers maybe due to their frequency or C ¼ Chloramphenicol, SXT ¼ Sulfamethoxazole-Trimethoprim, AMP ¼ Ampicillin,
method of using the toilet. Besides the high cases obtained from the K ¼ Kanamycin, TE ¼ Tetracycline, W ¼ Trimethoprim.
 S.L. Tan et al. / Food Control 44 (2014) 203e207 207

Table 5 Gibbs, S. G., Green, C. F., Tarwater, P. M., Mota, L. C., Mena, K. D., & Scarpino, P. V.
Multidrug resistant S. aureus on the hands of food handlers. (2006). Isolation of antibiotic-resistant bacteria from the air plume downwind
of a swine confined or concentrated animal feeding operation. Environmental
Antibiotics n (%) Nationality Health Perspectives, 114(7), 1032.
Gorman, R., Bloomfield, S., & Adley, C. C. (2002). A study of cross-contamination of
Malaysian Non-Malaysian
food-borne pathogens in the domestic kitchen in the Republic of Ireland. In-
None 140 (94.59) 80 60 ternational Journal of Food Microbiology, 76(1e2), 143e150.
AMP and C 2 (1.35) 0 2 Gungor, E., & Gokoglu, N. (2010). Determination of microbial contamination sources
AMP and TE 1 (0.68) 1 0 at a Frankfurter sausage processing line. Turkish Journal of Veterinary and Animal
AMP and F 4 (2.70) 2 2 Sciences, 34(1), 53e59.
Harakeh, S., Yassine, H., Gharios, M., Barbour, E., Hajjar, S., El-Fadel, M., et al. (2005).
P, AMP, K and W 1 (0.68) 0 1
Isolation, molecular characterization and antimicrobial resistance patterns of
Total 148 (100.00) 83 65
Salmonella and Escherichia coli isolates from meat-based fast food in Lebanon.
Note: n ¼ number of positive S. aureus strains, P ¼ Penicillin, C ¼ Chloramphenicol, Science of the Total Environment, 341(1), 33e44.
AMP ¼ Ampicillin, K ¼ Kanamycin, TE ¼ Tetracycline, W ¼ Trimethoprim, Lei, T., Tian, W., He, L., Huang, X.-H., Sun, Y.-X., Deng, Y.-T., et al. (2010). Antimi-
F ¼ Nitrofurantoin. crobial resistance in Escherichia coli isolates from food animals, animal food
products and companion animals in China. Veterinary Microbiology, 146(1), 85e
89.
Lues, J., & Van Tonder, I. (2007). The occurrence of indicator bacteria on hands and
handlers’ hands should be maintained in a good condition by aprons of food handlers in the delicatessen sections of a retail group. Food
adhering to GMP and SOP to reduce the existence of multidrug Control, 18(4), 326e332.
Miranda, J., Mondragón, A., Vázquez, B., Fente, C., Cepeda, A., & Franco, C. (2009).
resistance bacteria. Besides, there is also a need in the imple- Influence of farming methods on microbiological contamination and prevalence
mentation of an effective HACCP program in Malaysia school food of resistance to antimicrobial drugs in isolates from beef. Meat Science, 82(2),
service operations. 284e288.
Normanno, G., La Salandra, G., Dambrosio, A., Quaglia, N., Corrente, M., Parisi, A.,
et al. (2007). Occurrence, characterization and antimicrobial resistance of en-
Acknowledgments terotoxigenic Staphylococcus aureus isolated from meat and dairy products.
International Journal of Food Microbiology, 115(3), 290e296.
Pesavento, G., Ducci, B., Comodo, N., & Nostro, A. L. (2007). Antimicrobial resistance
This study was supported by Universiti Putra Malaysia Research
profile of Staphylococcus aureus isolated from raw meat: a research for methi-
University Grant Scheme (RUGS 9329800). Authors would like to cillin resistant Staphylococcus aureus (MRSA). Food Control, 18(3), 196e200.
specially thank the Ministry of Education Malaysia for granting the Platell, J. L., Johnson, J. R., Cobbold, R. N., & Trott, D. J. (2011). Multidrug-resistant
access into the school premise. extraintestinal pathogenic Escherichia coli of sequence type ST131 in animals
and foods. Veterinary Microbiology, 153(1), 99e108.
Portle, S. (2009). Elucidating the connection between cell population heterogeneity and
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