Food Control 127 (2021) 108111

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

The performance of food safety management system in relation to the

microbiological safety of salmon nigiri sushi: A multiple case study in a
Japanese chain restaurant
R.N. Fathurrahman a, Y. Rukayadi a, b, U.Z.A. Ungku Fatimah c, d, S. Jinap a, e, N.
A. Abdul-Mutalib c, e, M. Sanny a, e, *
a
Department of Food Science, Faculty of Food Science and Technology, Universiti Putra Malaysia, 43400, Serdang, Selangor, Malaysia
b
Laboratory of Natural Products, Institute of Bioscience, Universiti Putra Malaysia, UPM, Serdang, Selangor Darul Ehsan, 43400, Malaysia
c
Department of Food Service Management, Faculty of Food Science and Technology, Universiti Putra Malaysia, 43400, Serdang, Selangor, Malaysia
d
Halal Products Research Institute, Universiti Putra Malaysia, 43400, UPM Serdang, Selangor, Malaysia
e
Laboratory of Food Safety and Food Integrity (FOSFI), Institute of Tropical Agriculture and Food Security, Universiti Putra Malaysia, 43400, UPM, Serdang, Selangor,
Malaysia

A R T I C L E I N F O A B S T R A C T

Keywords: The study’s objective was to evaluate the performance of the food safety management system (FSMS) in relation
Microbiological food safety output to the microbiological food safety (FS) output of Salmon Nigiri Sushi in the selected outlets of a Japanese chain
Salmon nigiri sushi restaurant. Two outlets that are FSMS certified with ISO 22000 and two outlets that are FSMS not certified with
Critical sampling locations
ISO 22000 were selected. Microbiological Assessment Scheme was used in the study of evaluating the perfor­
Japanese chain restaurant
Food safety management system
mance of the FSMS, in which samples were collected from the selected critical sampling locations and analysed
for Bacillus cereus, Vibrio parahaemolyticus, Listeria monocytogenes, Escherichia coli, Staphylococcus aureus, Coli­
form, Total Plate Count (TPC), and Yeast and Mould Count. The microbial counts were compared against the
relevant established acceptance criteria to determine FS level and consequently calculate the FS output. The
overall FS output of the two outlets that are non-ISO 22000-certified FSMS was 2–3 (moderate to a good level)
and 2 (moderate level) in contrast to ISO 22000-certified FSMS outlets that was 2–3 (moderate to a good level)
and 1 to 2 (poor to a moderate level). None of the outlets was able to achieve their FS objectives. Bacillus cereus,
Vibrio parahaemolyticus, and Listeria monocytogenes were not detected, and therefore, the FS level was determined
at level 3 (good result) for all outlets. The FS level for TPC and E. coli was determined at level 1 (low result) due
to high E. coli counts (even in filtered tap water), which lead to ineffectiveness in cleaning and sanitation of food
contact surfaces, including hand washing. It appeared the performance of FSMS in relation to the microbiological
FS outputs of Salmon Nigiri Sushi of outlets that are non-ISO 22000-certified FSMS were better than outlets that
are ISO 22000-certified FSMS.

1. Introduction
Foodservice defines those businesses, institutions, and companies
that responsible for any meal prepared outside the home. This industry
includes restaurants, school and hospital cafeterias, and catering oper­
ations (Ortiz et al., 2018). Japanese restaurants are well known for their
sushi, and one of the most famous sushi is Salmon Nigiri Sushi (Lor­
entzen, Wesmajervi Breiland, Cooper, & Herland, 2012). Salmon Nigiri
Sushi consists of cold-cooked vinegared rice shaped into bite-size pieces
and topped with Salmon’s slice (Liang et al., 2016). Food poisoning
outbreaks in sushi in several countries were associated with Vibrio par­
ahaemolyticus, Bacillus cereus, Staphylococcus aureus, and Escherichia coli
and Listeria monocytogenes (Liang et al., 2016; Lorentzen et al., 2012;
NSW Food Authority, 2008). Some ingredients in sushi, such as Salmon,
are fresh raw food, which their consumption exposes consumers to
different pathogenic microorganisms that might lead to simple gastro­
enteritis and fatality (Nespolo, Martineli, & Rossi, 2012). Furthermore,
sushi ingredients are prepared in advance for quick-serve, and this meal
is directly contacted with handlers’ hands and cutting board during its
preparation. These factors lead to an increased incidence of

* Corresponding author. Department of Food Science, Faculty of Food Science and Technology, Universiti Putra Malaysia, 43400, Serdang, Selangor, Malaysia.
E-mail address: s_maimunah@upm.edu.my (M. Sanny).

https://doi.org/10.1016/j.foodcont.2021.108111
Received 16 October 2020; Received in revised form 23 February 2021; Accepted 21 March 2021
Available online 27 March 2021
0956-7135/© 2021 Elsevier Ltd. All rights reserved.
R.N. Fathurrahman et al. Food Control 127 (2021) 108111

cross-contamination with potential foodborne pathogens, especially Table 1

Staphylococcus aureus (Liang et al., 2016).
The International Organization for Standardization (ISO) developed
the standard ISO 22000 that describes requirements for a food safety
management system (FSMS) (Standards Malaysia. 2012). FSMS
complying with the standard ISO 22000 is implemented to assure food
safety (FS) in the entire food supply chain, and the standard is based on
Good Manufacturing Practices (GMPs), the Codex Alimentarius Hazard
Analysis Critical Control Points (HACCP) principles, and some addi­
tional elements existing in quality management systems described in ISO
9001 standard (Luning, Chinchilla, Jacxsens, Kirezieva, & Rovira,
2013). ISO 22000 standard provides an international solution respon­
sible for improving FS and avoiding foodborne outbreaks (Luning,
Marcelis, et al., 2011). The establishment of a measurable FS objective is
needed to evaluate the performance of the FSMS in an organization
(Standards Malaysia. 2007, 2012). Luning et al. (2009) developed a
Microbiological Assessment Scheme (MAS), which is used to assess the
performance of the FSMS, in which microbiological parameters and
criteria selected are the organization’s FS objectives. FS level is attrib­
uted to each type of microbiological parameter at different critical
sampling locations (CSLs) and consequently measured the FS output to
evaluate the performance of FSMS (Oses et al., 2012). CSLs are identified
within the production process (e.g., raw materials, food contact surfaces,
finished products) and defined as locations where microbial sampling
provides information about the microbiological control (Jacxsens et al.,
2009). The goal of a MAS sampling plan is to obtain insights into the
maximum microbiological counts, the distribution of microbial
contamination, such as where to find contamination in the production
process, and into the dynamics of microbial contamination occurring as
a result of the design and application of the control strategies in a FSMS
(De Loy-Hendrickx et al., 2018).
Puah, Chua, and Tan (2017) reported the prevalence of Staphylo­
coccus aureus of ready-to-eat sushi in Kuala Lumpur, Malaysia, and found
16% (32/200) of the samples were contaminated with that bacterium.
Liang et al. (2016), in their study, had collected 120 samples of
take-away raw salmon finger sushi in Hong Kong and found 1.7%
(2/120) of the samples were contaminated with Escherichia coli (>1.3
log CFU/g) and considered as unacceptable. Meanwhile, Hoel, Mehli,
Bruheim, Vadstein, and Jakobsen (2015) collected 58 samples of raw
fish fillet that normally used for salmon sushi and found 48% (28/58) of
the samples were rated as unacceptable based on the aerobic plate count
(>6 log CFU/g). Studies on the performance of FSMS in relation to the
microbiological FS output of Salmon Nigiri Sushi at CSLs, particularly in
the Japanese chain restaurants, are scarce as the majority of the current
literature predominantly reported studies on the off-the-shelf sushi.
Therefore, this study’s objective was to evaluate the performance of
FSMS in relation to the microbiological FS output of Salmon Nigiri Sushi
at CSLs in the selected outlets of a Japanese chain restaurant. Subse­
quently, the present study’s research question was developed as follows;
what is the performance FSMS in relation to the microbiological FS
output of Salmon Nigiri Sushi at various CSLs in the selected outlets of a
Japanese chain restaurant. Such study will enable the organization to
obtain insight into the distribution of microbial contamination within
the production process, thus helping determine which contamination of
CSLs is out of control to facilitate intervention strategies that reduce the
risk of food poisoning outbreaks upon consumption of Salmon Nigiri
Sushi.
2. Materials and methods
2.1. Characteristic of outlets
A multiple case study was conducted in the kitchens of four outlets of
a Japanese chain restaurant located in Klang Valley, Malaysia, from
23rd April until 7th June 2018. Outlets 1 and 2 are ISO 22000-certified
FSMS, whereas outlets 3 and 4 are non-ISO 22000-certified FSMS. The
Characteristics of the four outlets of a Japanese chain restaurant.
Restaurant Parameters ISO 22000-certi­ Non-ISO 22000-
fied FSMS certified FSMS
Outlet Outlet Outlet Outlet
1 2 3 4
Outlet sizea 120 m2 200 m2 150m2 210 m2
Average number of customers visited 350 300 180 290
the outlet per dayb
Total of employeec 11 18 11 18
Total of new employeed 2 15 1 12
Total of experienced employeee 9 3 10 6
a
The size of the outlet. Using one shop lot categorised as small, using two shop
lots categorised as medium and using three shop lots categorised as large.
b
Average order per day.
c
Total of staff working in a day.
d
Total of new staff in a day (less than one-month employment).
e
Total of experienced staff in a day (more than one-month employment).
outlets’ characteristics in terms of the size of premises, the total number
of food handlers, and the average number of customers who visited the
outlet per day were recorded in Table 1. The ethical approval was ob­
tained from the Universiti Putra Malaysia (JKEUPM-2018-024), while
informed consent was obtained from the participants.
2.2. Microbial assessment scheme (MAS)
As described by Jacxsens et al. (2009), the MAS was employed in the
present work to obtain insights into the performance of FSMS activities
with microbiological results as the output. The MAS was included in the
following sub-sections: Selected CSLs and Sampling Frequencies, Se­
lection of Microbiological Parameters and Analytical Methods, Sample
Preparation for Microbiological Analysis of Ingredients and Final
Products, Sampling of Air Quality, Personal Hygiene using Swab Test,
Sampling of Food Contact Surfaces using Swab Test, and Sampling of
Tap Water.
2.2.1. Selected critical sampling locations and Sampling Frequencies
CSLs were selected according to Jacxsens et al. (2009). A total of 29
CSLs were selected, which include the ingredients for making the
Salmon Nigiri Sushi (salmon slice after thawing and after cutting,
salmon slice after five and 10 h of storage, uncooked and cooked rice
before and after mixed with vinegar, rice mix after five and 10 h of
storage, final food products (Salmon Nigiri Sushi), cleanliness of pro­
duction equipment and utensils (cutting boards, knives, gloves, and
aprons), personal hygiene of food handlers (before and after washing
hand), environment exposed to the processing and serving areas, and tap
water. The critical steps in making Salmon Nigiri Sushi were followed
through, and samples were collected at these identified critical steps.
The locations of ingredients and the final product in which they were
sampled are illustrated in Fig. 1. Researchers visited each outlet, and
samples were collected throughout all the selected CSLs. Two samples
were taken for every CSL in every outlet. A total of 232 samples (29 CSLs
× 4 outlets × 2 replicates) were collected. Samples were aseptically
stored in ice and transported in an insulated box to the Microbiology
Laboratory, Faculty of Food Science and Technology, Universiti Putra
Malaysia, Malaysia, for microbiological analyses within 6–24 h of
sampling.
2.2.2. Selection of microbiological parameters and Analytical Method
The selection of microbiological parameters was made according to
the Microbiological Examination guidelines of Ready-to-Eat Foods
(FSANZ, 2016). Staphylococcus aureus, Escherichia coli, and Coliform
were selected as the hygiene indicators. Vibrio parahaemolyticus, Bacillus
cereus, and Listeria monocytogenes were selected as the FS indicators.
Total Plate Count (TPC) was selected as the total microbiological quality

2
R.N. Fathurrahman et al.
Fig. 1. Process flow diagram of salmon nigiri sushi from CSL 1 up to CSL 10.
indicator. Yeast and Mould Count (YMC) was selected as the environ­
mental quality indicator. Baird Parker Agar (BPA), MacConkey Agar
(MA), Eosin Methylene Blue Agar (EMB), Bacillus Cereus Agar (BCA),
Vibrio Selective Agar (VSA), Plate Count Agar (PCA), Potato Dextrose
Agar (PDA), PALCAM agar, and buffered peptone water were purchased
from Oxoid, UK. They were prepared according to the instructions given
by the manufacturer.
3
Food Control 127 (2021) 108111
2.2.3. Sample Preparation for Microbiological Analysis of Ingredients and
Final Products
The sample preparation for TPC, Coliform, B. cereus, V. para­
haemolyticus, Listeria monocytogenes, E. coli, and S. aureus count was
performed according to ISO 11333: 2004. Twenty-five of the 300 g of
food sample was homogenized with 225 mL of buffered peptone water
for 2 min in a sterile stomacher bag by using a stomacher. Homogenized
samples were then serially diluted with 1% sterile peptone water up to
10− 6 dilutions. 0.1 mL of the samples at each dilution factor were
R.N. Fathurrahman et al. Food Control 127 (2021) 108111

Table 2
Microbial assessment scheme of the four outlets of a Japanese chain restaurant with indication of critical sampling locations, selected microbiological parameters and
interpretation of the results.
Critical Sampling Location 1–9 10 11–20 21–24 25–27 28–29
(CSL)
Ingredients Product Food Contact Personal Hygiene Air Quality Water Quality
Surfaces

Microbiological Parameters
Interpretation of results
a
M: Maximum microbiological count allowed in 25g.
Staphylococcus aureus Staphylococcus aureus Staphylococcus aureus Staphylococcus Mould and Yeast Coliform
Coliform Coliform Coliform aureus Escherichia coli
Escherichia coli Escherichia coli Escherichia coli Coliform Total Plate Count
Bacillus cereus Bacillus cereus Total Plate Count Escherichia coli
Vibrio Vibrio Total Plate Count
parahaemolitycus parahaemolitycus
Listeria monocytogenes Listeria monocytogenes
Total Plate Count Total Plate Count
Salmon and Rice Staphylococcus aureus Staphylococcus aureus Staphylococcus Mould and Yeast Coliform
Staphylococcus aureus M: 1.99 log CFU/g M: 1.99 log CFU/cm2 aureus M: 1.95 log CFU/ Filtered water
Ma: 1.99 log CFU/g Coliform Coliform M: 1.99 log CFU/ m3 M: Absent in 100
Coliform M: 1.69 log CFU/g M: 1.69 log CFU/cm2 cm2 mL
M: 1.69 log CFU/g Escherichia coli Escherichia coli Coliform Unfiltered water
Escherichia coli M: Absent in 1 g M: Absent in 1 g M: 1.69 log CFU/ M: 1.69 log CFU/
M: Absent in 1 g Bacillus cereus Total Plate Count cm2 mL
Bacillus cereus M: 1.99 log CFU/g M: 5.99 log CFU/cm2 Escherichia coli Escherichia coli
M: 1.99 log CFU/g Vibrio M: Absent in 1 g Filtered water
Vibrio parahaemolitycus Total Plate Count M: Absent in 100
parahaemolitycus M: 0.47 log CFU/g M: 5.99 log CFU/ mL
M: 0.47 log CFU/g Listeria monocytogenes cm2 Unfiltered water
Listeria monocytogenes M: Absent in 25 g M: 1.69 log CFU/
M: Absent in 25 g Total Plate Count mL
Total Plate Count M: 5.99 log CFU/g Total Plate Count
M: 5.99 log CFU/g Filtered water
M: 1.99 log CFU/
mL

transferred and spread evenly onto PCA, MA, BCA, VSA, PALCAM, EMB,
and BPA. Following incubation at 37 ◦ C for 18–24 h, 25 to 250 colonies
on the plates were counted using a colony counter (Today’s Instruments,
Taiwan). Results were then expressed as Colony Forming Units per gram
(CFU/g).
2.2.4. Sampling of Air Quality
The air quality was inspected with a culture settling plating tech­
nique according to ISO 11057. PDA plates were opened and exposed at
the processing and accommodating area for 15 min. Enumeration of
yeast and mould count denotes the air quality in the processing and
service areas. The petri dishes were closed and incubated at 21 ◦ C for
two to three days. Only 25–250 colony forming units (CFU/g) were
counted on plates by utilizing colony count (Today’s Instruments,
Taiwan).
2.2.5. Personnel hygiene with hand swab
Sampling of the food handlers’ hygiene using hand swab tests was
performed before and after they washed their hands according to ISO
18593. A sterile swab was dipped into 1% sterile peptone water and
immediately swabbed in an area covered approximately 25 cm2 (5 cm ×
5 cm). Following swabbing, the swab head was gently re-immersed in
the 1% sterile peptone water, mixed by hand, and kept in an icebox. The
samples were serially diluted up to 10− 5 dilution. Next, 0.1 mL of
peptone water was pipetted and spread on PCA, MA, BCA, VSA, PAL­
CAM, EMB, and BPA. The plastic cover of the plate was closed and
pressed by utilizing a presser. The plates were incubated at 37 ◦ C for
24–48 h. Results were expressed in CFU/g.
2.2.6. Sampling of food contact surface
Sampling of the food contact surfaces after the equipment and
utensils were cleaned was also conducted by using the swab test as
described in Sub-Section 2.2.6 above. The selected food contact surfaces
include a cutting board, knife, apron, and gloves. The swabbed stick was
transferred to the laboratory using an icebox. The culture media was
BPA to detect S. aureus, MA to detect Coliform, EMB to detect E. coli, and
PCA to detect TPC. The resulting counts indicated the performance of
cleaning the equipment and utensils. The isolates obtained were iden­
tified as described by the media supplier (Oxoid, UK).
2.2.7. Sampling of Tap Water
Coliform and E. coli counts for tap water were analysed according to
ISO 9308. A tenfold dilution (10ˉ1 - 10ˉ⁶) was diluted from tap water
samples that were taken at 10ˉ1. Next, 0.5 mL of the samples were
transferred onto the MA (Oxoid, U.K) and EMB (Oxoid, U.K). Diluted
samples were spread evenly on the surface of the medium. The MA and
EMB plates were incubated at 37 ◦ C for 18–24 h, and if there was no
growth of colonies, the plates were incubated for another 24 h. Only
25–250 colony forming units (CFU) were counted on plates with the use
of the colony. Microbial isolates were identified by cultural, morpho­
logical, and physiological characteristics as described in the media
supplier.
2.3. Data processing and interpretation
The obtained microbial counts of ingredients and final product
samples were compared against the relevant guidelines, and they were
considered unsafe for consumption if the count was higher than the
acceptable level. Table 2 shows the maximum permissible level of the
selected microbiological parameters at the corresponding CSLs. Ac­
cording to FSANZ (2016), the acceptable levels are S. aureus < 102
CFU/g, Bacillus cereus < 102 CFU/g, V. parahaemolyticus < 3 CFU/g, and
Listeria monocytogenes were not detected in 25 g sample. According to
Malaysia’s Food Act and Regulations (Laws of Malaysia. 1985), E. coli
must not be detected in 1 g sample, TPC < 106 CFU/g, and Coliform <50
CFU/g. Meanwhile, the microbial counts of hands and food contact
surfaces were considered unacceptable when the microbial contamina­
tion is equal to or higher than that present in the food samples (Oses
et al., 2012). E. coli and Coliform must be absent in 100 mL filtered tap
water and <50 CFU/ml in unfiltered tap water according to Malaysia’s

4
R.N. Fathurrahman et al. Food Control 127 (2021) 108111

Table 3
Microbiological qualities of Salmon Nigiri Sushi at various Critical Sampling Locations in the outlet 1 of ISO 22000-certified FSMS Japanese chain restaurant.
Critical Sampling Location (CSL) Hygiene indicators Food safety indicators Overall Air quality
indicator

Staphylococcus Coliform Escherichia Bacillus Vibrio Listeria Total Plate Mould and
aureus coli cereus parahaemolitycus monocytogenes Count Yeast

CSL1: Salmon slice after thawing 1.61 ± 0.89 1.57 ± 0.61 ± 0.85 -a ND ND 5.35 ± 1.59 –
0.71
CSL2: Salmon slice after cutting 1.57 ± 0.86 1.62 ± 0.62 ± 0.72 – ND ND 5.36 ± 1.84 –
0.89
CSL3: Salmon slice after 5 h of 1.57 ± 0.79 2.61 ± 0.55 ± 0.81 – ND ND 5.35 ± 1.63 –
storage 0.77
CSL4: Salmon slice after 10 h of 1.61 ± 0.82 2.61 ± 0.64 ± 0.89 – ND ND 5.37 ± 1.44 –
storage 1.01
CSL5: Uncooked rice 1.62 ± 0.91 1.57 ± 0.62 ± 0.66 ND – ND 5.36 ± 1.93 –
0.71
CSL6: Cooked rice 1.61 ± 0.82 1.58 ± 0.61 ± 0.85 ND – ND 5.35 ± 1.67 –
0.91
CSL7: Cooked rice after mixed with 1.61 ± 0.85 1.61 ± 0.58 ± 0.91 ND – ND 5.34 ± 1.26 –
vinegar 0.85
CSL8: Rice mix after 5 h of storage 1.55 ± 0.81 1.62 ± 0.58 ± 0.83 ND – ND 5.35 ± 1.59 –
0.89
CSL9: Rice mix after 10 h of storage 1.61 ± 0.85 1.62 ± 0.62 ± 0.91 ND – ND 5.37 ± 1.21 –
0.54
CSL10: Salmon nigari sushi 1.61 ± 0.77 1.61 ± 0.58 ± 0.83 ND – ND 7.62 ± 1.72 –
0.68
CSL11: Cutting board (dedicated to 1.61 ± 0.77 1.59 ± 1.35 ± 1.61 – – – 5.63 ± 1.78 –
cut Salmon only) 0.89
CSL12: Cutting board (dedicated to 1.63 ± 0.93 1.59 ± 1.35 ± 1.67 – – – 5.63 ± 1.82 –
cut seafood beside Salmon) 0.89
CSL13: Cutting board (dedicated to 1.61 ± 0.85 1.6 ± 2.34 ± 1.83 – – – 6.61 ± 1.51 –
cut meat only) 0.82
a
refers to parameter not analysed for this critical sampling location

Critical Sampling Location (CSL) Hygiene indicators Food safety indicators Overall Air quality
indicator

Staphylococcus Coliform Escherichia Bacillus Vibrio Listeria Total Plate Mould and
aureus coli cereus parahaemolitycus monocytogenes Count Yeast

CSL14: Cutting board (dedicated to 1.57 ± 0.86 1.62 ± 0.56 ± 0.81 -a – – 5.35 ± 2.01 –
cut ready-to-eat food only) 0.83
CSL15: Cutting board (dedicated to 1.6 ± 0.85 1.6 ± 0.63 ± 0.77 – – – 7.2 ± 1.63 –
cut vegetable only) 0.57
CSL16: Knife (dedicated to cut 1.64 ± 0.51 1.62 ± 1.35 ± 1.63 – – – 6.63 ± 1.75 –
Salmon only) 0.89
CSL17: Knife (dedicated to cut 1.57 ± 0.79 1.61 ± 2.36 ± 1.58 – – – 6.62 ± 1.58 –
seafood beside Salmon) 0.77
CSL18: Knife (dedicated to cut 1.6 ± 0.97 1.57 ± 2.35 ± 1.78 – – – 5.63 ± 1.82 –
meat only 0.77
CSL19: Knife (dedicated to cut 1.59 ± 0.81 1.59 ± 2.35 ± 1.65 – – – 5.63 ± 1.92 –
ready-to-eat food only) 0.89
CSL20: Knife (dedicated to cut 1.57 ± 0.87 3.57 ± 2.35 ± 1.95 – – – 5.63 ± 1.59 –
vegetable only) 0.79
CSL21: Personal hygiene before 1.59 ± 0.89 1.63 ± 2.33 ± 1.15 – – ND 5.44 ± 1.79 –
handwash 0.77
CSL22: Personal hygiene after 1.6 ± 0.82 1.6 ± 2.34 ± 1.65 – – ND 5.45 ± 1.67 –
handwash 0.77
CSL23: Apron 1.62 ± 0.81 1.6 ± 1.35 ± 1.79 – – ND 5.43 ± 1.76 –
0.82
CSL24: Gloves 1.6 ± 0.97 1.6 ± 1.36 ± 1.54 – – ND 5.44 ± 1.86 –
0.93
CSL25: Air quality in wet kitchen – – – – – – 1.45 ± 1.01
a
refers to parameter not analysed for this critical sampling location

Critical Sampling Location Hygiene indicators Food safety indicators Overall Air quality
(CSL) indicator

Staphylococcus Coliform Escherichia Bacillus Vibrio Listeria Total Plate Mould and
aureus coli cereus parahaemolitycus monocytogenes Count Yeast

CSL26: Air quality in sushi -a – – – – – 1.46 ± 1.73

preparation table
CSL27: Air quality in service – – – – – – – 1.75 ± 1.88
area
CSL28: Water quality – 3.65 ± 3.66 ± 2.11 – – – 5.67 ± 1.63 –
(filtered) 0.81
CSL29: Water quality – 3.62 ± 4.67 ± 2.23 – – – 6.67 ± 1.35 –
(unfiltered) 0.75
FS Levelb 3 1 1 3 3 3 1 3
(continued on next page)

5
R.N. Fathurrahman et al.
Table 3 (continued )
Critical Sampling Location Hygiene indicators
(CSL)
Staphylococcus Coliform Escherichia
aureus coli
FS Total 18/24
FS Outputc (2–3)
a
Refers to parameter not analysed for this critical sampling location.
b
Level 3 – Good result (legal criteria or guidelines are respected, no improvement are needed – current level of FSMS is high enough to cover this hazard. Level 2 –
Medium result (legal criteria or guidelines are exceeded, improvements need to be made on a single control activity of FSMS). Level 1 – Low result (legal criteria or
guidelines are exceeded, improvements need to be made on multiple control activities of the FSMS).
c
An overall score of 1 (poor risk) was assigned when the sum of the levels was 8–10, a sum of 11–14 resulted in an overall scores of 1–2 (poor to moderate level), a
sum of 15–17 resulted in an overall score of 2 (moderate-risk), as sum of 18–21 resulted in an overall scores of 2–3 (moderate to good level), and a sum of 22 or 24
resulted in an overall score of 3 (good level).
Drinking Water Quality Standard (Ministry of Health, 2000). TPC < 102
CFU/ml in filtered tap water according to European Drinking Water
Standard (European Commission, 1998). Yeast and Mould Count’s
maximum value recommended by the American Public Health Associ­
ation (Sveum, Moberg, Rude, & Frank, 1992) must not exceed 90
CFU/m3.
The microbiological results from all the CSLs could be classified as
low, medium, and high risk in microbiological FS levels. For each
microbiological parameter at different CSLs, a FS level ranging from 1 to
3 was used (Jacxsens et al., 2009). Levels 1, 2, and 3 of FS level indicate
as “poor”, “moderate”, and “good” respectively. An overall score of 1
(“poor”) was assigned when (i) the sum of the levels was 8–10, (ii) a sum
of 11–14 resulted in an overall score of 1–2 (“poor to moderate”), (iii) a
sum of 15–17 resulted in an overall score of 2 (“moderate”), (iv) a sum of
18–21 resulted in an overall score of 2–3 (“moderate to good”), and (v) a
sum of 22–24 resulted in an overall score of 3 (“good”).
3. Results
The FS output for outlets 1, 2, 3, and 4 was 2–3 (Table 3), 1 to 2
(Table 4), 2 to 3 (Table 5), and 2 (Table 6), respectively. Table 3 shows
that all FS indicators, one hygiene indicator, and air quality received a
good FS level of 3, as legal criteria or guidelines were respected at all
corresponding CSLs. On the other hand, two hygiene indicators and
overall indicator received a poor FS level of 1, which is due to the legal
criteria or guidelines that were exceeded at multiple CSLs. The Coliform
counts for the following CSLs have exceeded the limits: salmon slice
after 5 h of storage (CSL 3), salmon slice after 10 h of storage (CSL 4),
knife dedicated to cut vegetable only (CSL 20), filtered (CSL 28), and
unfiltered tap water (CSL 29). E. coli counts exceeded the limits at all
CSLs. The TPC for the following CSLs have exceeded the limits: Salmon
Nigiri Sushi (CSL 10), cutting board dedicated to cut meat only (CSL 13),
cutting board dedicated to cut vegetable only (CSL 15), knife dedicated
to cut Salmon only (CSL 17), knife dedicated to cut seafood other than
Salmon (CSL 17), and unfiltered tap water (CSL 29). The total FS level
for outlet 1 was 18 over 24, which resulted in an overall score of 2–3,
which is a moderate to a good level of FS output.
Table 4 shows that all FS indicators received a good FS level of 3, as
legal criteria or guidelines were respected at all corresponding CSLs. On
the other hand, all hygiene indicators, overall indicator, and air quality
received a poor FS level of 1, as the legal criteria or guidelines exceeded
multiple CSLs. The Staphylococcus aureus counts for personal hygiene
before (CSL 21) and after (CSL 22) handwashing exceeded the limits.
The Coliform counts for the following CSLs have exceeded the limits:
salmon slice after 5 h of storage (CSL 3), salmon slice after 10 h of
storage (CSL 4), knife dedicated to cut vegetable only (CSL 20), and
filtered (CSL 28) and unfiltered tap water (CSL 29). E. coli counts
exceeded the limits at all CSLs. The TPC for the following CSLs have
exceeded the limits: Salmon Nigiri Sushi (CSL 10), cutting board dedi­
cated to cut meat only (CSL 13), cutting board dedicated to cut vegetable
Food Control 127 (2021) 108111
Food safety indicators Overall Air quality
indicator
Bacillus Vibrio Listeria Total Plate Mould and
cereus parahaemolitycus monocytogenes Count Yeast
only (CSL 15), knife dedicated to cut Salmon only (CSL 17), knife
dedicated to cut seafood other than Salmon (CSL 17), and unfiltered tap
water (CSL 29). The MYC for the following CSLs has exceeded the limits:
air quality in the wet kitchen (CSL 25) and air quality in the service area
(CSL 27). The total FS level for outlet 2 was 14 over 24, which resulted in
an overall score of 1–2, which signifies the poor to moderate level of FS
output.
Table 5 shows that all FS indicators, one hygiene indicator, and air
quality received a good FS level of 3, as legal criteria or guidelines were
respected at all corresponding CSLs. On the other hand, one hygiene
indicator and overall indicator received a poor FS level of 1 as legal
criteria or guidelines exceeded multiple CSLs. One hygiene indicator
received a moderate FS level of 2, and this is factorized by the legal
criteria or guidelines that were exceeded at one CSL. The Coliform
counts for the unfiltered tap water (CSL 29) were exceeded the limit.
E. coli counts exceeded the limits at all CSLs. The TPC for the cutting
board dedicated to cut vegetables (CSL 15) and unfiltered tap water (CSL
29) exceeded the limits. The total FS level for outlet 3 was 18 over 24,
which resulted in an overall score of 2–3, or a moderate to a good FS
output level.
Table 6 shows that all FS indicators and one hygiene indicator
received a good FS level of 3 as legal criteria or guidelines were
respected at all corresponding CSLs. On the other hand, two hygiene
indicators, overall indicator, and air quality, received a poor FS level of 1
as legal criteria or guidelines exceeded multiple CSLs. The Coliform
counts for the following CSLs were exceeded the limits: salmon slice
after thawing (CSL 1), salmon slice after 5 h of storage (CSL 3), salmon
slice after 10 h of storage (CSL 4), cutting board dedicated to cut seafood
other than Salmon (CSL 12), knife dedicated to cut Salmon only (CSL16),
knife dedicated to cut seafood besides Salmon (CSL 17), personal hy­
giene after hand washing (CSL 22), and filtered (CSL 28) and unfiltered
tap water (CSL 29). E. coli counts exceeded the limits at all CSLs. The TPC
for the following CSLs have exceeded the limits: salmon slice after 10 h
of storage (CSL 4), cutting board dedicated to cut vegetable only (CSL
15), knife dedicated to cut vegetable only (CSL 20), and unfiltered tap
water (CSL 29). MYC exceeded the limits at all CSLs. The total FS level
for outlet 4 was 16 over 24, which resulted in an overall score of 2,
signifying a moderate FS output level.
4. Discussion
The present study evaluated the performance of FSMS in relation to
the microbiological FS output of Salmon Nigiri Sushi at various CSLs in
the selected outlets of a Japanese chain restaurant. It was found that the
overall FS outputs of the outlet 1 and 2, which are ISO 22000-certified
FSMS were 2–3 (moderate to a good level) and 1 to 2 (poor to a mod­
erate level), respectively. However, outlets 3 and 4, non-ISO 22000-
certified FSMS scored a moderate to a good level (overall score of
2–3) and a moderate level (overall score of 2). It appeared the FS outputs
of outlets that are non-ISO 22000-certified FSMS were better than
6
R.N. Fathurrahman et al. Food Control 127 (2021) 108111

Table 4
Microbiological qualities of Salmon Nigiri Sushi at various Critical Sampling Locations in the outlet 2 of ISO 22000-certified FSMS Japanese chain restaurant.
Critical Sampling Location (CSL) Hygiene indicators Food safety indicators Overall Air quality
indicator

Staphylococcus Coliform Escherichia Bacillus Vibrio Listeria Total Plate Mould and
aureus coli cereus parahaemolitycus monocytogenes Count Yeast

CSL1: Salmon slice after thawing 1.55 ± 1.21 1.47 ± 0.61 ± 0.82 -a ND ND 5.24 ± 4.87 –
1.44
CSL2: Salmon slice after cutting 1.49 ± 1.36 1.13 ± 0.61 ± 0.68 – ND ND 5.24 ± 5.39 –
1.49
CSL3: Salmon slice after 5 h of 1.42 ± 1.21 2.49 ± 0.63 ± 0.86 – ND ND 5.26 ± 3.57 –
storage 1.65
CSL4: Salmon slice after 10 h of 1.49 ± 1.21 2.49 ± 0.59 ± 0.81 – ND ND 5.24 ± 5.23 –
storage 1.36
CSL5: Uncooked rice 1.49 ± 1.41 1.54 ± 0.65 ± 0.81 ND – ND 5.29 ± 4.44 –
1.51
CSL6: Cooked rice 1.52 ± 1.54 1.54 ± 0.63 ± 0.79 ND – ND 5.21 ± 3.42 –
1.55
CSL7: Cooked rice after mixed with 1.49 ± 1.51 1.45 ± 0.54 ± 0.73 ND – ND 5.26 ± 5.56 –
vinegar 1.05
CSL8: Rice mix after 5 h of storage 1.46 ± 1.45 1.45 ± 0.61 ± 0.89 ND – ND 5.22 ± 3.72 –
1.17
CSL9: Rice mix after 10 h of storage 1.5 ± 1.47 1.51 ± 0.58 ± 0.83 ND – ND 5.23 ± 4.86 –
1.47
CSL10: Salmon nigari sushi 1.54 ± 1.41 1.52 ± 0.59 ± 0.89 ND – ND 7.57 ± 5.07 –
1.58
CSL11: Cutting board (dedicated to 1.49 ± 1.29 1.49 ± 1.29 ± 2.82 – – – 5.57 ± 5.08 –
cut Salmon only) 1.77
CSL12: Cutting board (dedicated to 1.41 ± 1.46 1.51 ± 1.29 ± 3.26 – – – 5.57 ± 3.12 –
cut seafood beside Salmon) 1.48
CSL13: Cutting board (dedicated to 1.48 ± 1.59 1.48 ± 2.31 ± 3.19 – – – 6.55 ± 5.03 –
cut meat only) 1.51
a
refers to parameter not analysed for this critical sampling location

Critical Sampling Location (CSL) Hygiene indicators Food safety indicators Overall Air quality
indicator

Staphylococcus Coliform Escherichia Bacillus Vibrio Listeria Total Plate Mould and
aureus coli cereus parahaemolitycus monocytogenes Count Yeast

CSL14: Cutting board (dedicated to 1.47 ± 1.24 1.49 ± 0.57 ± 0.86 -a – – 5.21 ± 5.08 –
cut ready-to-eat food only) 1.06
CSL15: Cutting board (dedicated to 1.53 ± 1.59 1.57 ± 0.59 ± 0.89 – – – 7.14 ± 3.97 –
cut vegetable only) 1.53
CSL16: Knife (dedicated to cut 1.51 ± 1.81 1.48 ± 1.31 ± 2.81 – – – 6.57 ± 4.56 –
Salmon only) 1.37
CSL17: Knife (dedicated to cut 1.49 ± 1.45 1.45 ± 2.29 ± 3.18 – – – 6.58 ± 4.81 –
seafood beside Salmon) 1.68
CSL18: Knife (dedicated to cut 1.46 ± 1.45 1.55 ± 2.31 ± 3.19 – – – 5.54 ± 3.99 –
meat only 1.41
CSL19: Knife (dedicated to cut 1.47 ± 1.53 1.44 ± 2.31 ± 3.31 – – – 5.59 ± 5.02 –
ready-to-eat food only) 1.44
CSL20: Knife (dedicated to cut 1.54 ± 1.32 3.49 ± 2.31 ± 2.54 – – – 5.56 ± 4.38 –
vegetable only) 1.41
CSL21: Personal hygiene before 2.55 ± 1.39 1.43 ± 2.31 ± 3.29 – – ND 5.56 ± 4.51 –
handwash 1.58
CSL22: Personal hygiene after 2.31 ± 1.44 1.46 ± 2.31 ± 3.04 – – ND 5.58 ± 5.55 –
handwash 1.63
CSL23: Apron 1.52 ± 1.31 1.53 ± 1.31 ± 3.11 – – ND 5.56 ± 4.94 –
1.63
CSL24: Gloves 1.54 ± 1.31 1.52 ± 1.33 ± 2.83 – – ND 5.56 ± 4.75 –
1.49
CSL25: Air quality in wet kitchen – – – – – – – 2.23 ± 0.89
a
refers to parameter not analysed for this critical sampling location

Critical Sampling Location Hygiene indicators Food safety indicators Overall Air quality
(CSL) indicator

Staphylococcus Coliform Escherichia Bacillus Vibrio Listeria Total Plate Mould and
aureus coli cereus parahaemolitycus monocytogenes Count Yeast

CSL26: Air quality in sushi -a – – – – – – 1.88 ± 1.45

preparation table
CSL27: Air quality in service – – – – – – – 2.19 ± 0.77
area
CSL28: Water quality – 3.53 ± 3.62 ± 5.12 – – – – 5.73 ± 4.81 –
(filtered) 1.36
CSL29: Water quality – 3.41 ± 4.63 ± 5.01 – – – – 6.71 ± 4.67 –
(unfiltered) 1.51
FS Levelb 1 1 1 3 3 3 1 1
(continued on next page)

7
R.N. Fathurrahman et al.
Table 4 (continued )
Critical Sampling Location Hygiene indicators
(CSL)
Staphylococcus Coliform Escherichia
aureus coli
FS Total 14/24
FS Outputc 1–2
a
Refers to parameter not analysed for this critical sampling location.
b
Level 3 – Good result (legal criteria or guidelines are respected, no improvement are needed – current level of FSMS is high enough to cover this hazard. Level 2 –
Medium result (legal criteria or guidelines are exceeded, improvements need to be made on a single control activity of FSMS). Level 1 – Low result (legal criteria or
guidelines are exceeded, improvements need to be made on multiple control activities of the FSMS).
c
An overall score of 1 (poor risk) was assigned when the sum of the levels was 8–10, a sum of 11–14 resulted in an overall scores of 1–2 (poor to moderate level), a
sum of 15–17 resulted in an overall score of 2 (moderate-risk), as sum of 18–21 resulted in an overall scores of 2–3 (moderate to good level), and a sum of 22 or 24
resulted in an overall score of 3 (good level).
outlets that are ISO 22000-certified FSMS. Our findings contrast with the
results of Nyarugwe, Linnemann, Nyanga, Fogliano, and Luning (2018)
and Kokkinakis, Fragkiadakis, Loakeimidi, Giankoulof, and Kokkinaki
(2008) who reported that FSMS certified companies had a better
microbiological safety performance as compared with the ones who
were not FSMS certified. Nevertheless, other researchers reported that
the quality assurance standards and guidelines implemented did not
necessarily result in the required FS output (Ngoc, Arturu, Ha, &
Miyamoto, 2020; Njage, Opiyo, Wangoh, & Wambui, 2018). Each
company has its unique FSMS because it depends on which quality
assurance (QA) standards and guidelines they are using and how they
translate and adapt the guiding principle to the company-specific cir­
cumstances. The output of a system is not only dependent on the system
performance itself, but it also depends on the characteristics of the
context wherein it operates. Thus, FSMS should be adapted to its context
of characteristics to achieve a good FS output (Luning, Marcelis, et al.,
2011).
It appears that none of the outlets of Japanese chain restaurants was
able to achieve their FS objectives. This is due to the microbiological
results obtained at the selected CSLs in the outlets exceeding acceptable
levels. For example, E. coli and the counts of TPC were above the
acceptable limits at multiple CSLs in all outlets, which contributed to the
low FS levels obtained. The results are consistent with Luning, Jacxsens,
et al. (2011), where they evaluated the microbiological FS output of
meat processing industries and reported various cross-contamination
problems in which E coli and Enterobacteriaceae, as well as TPC, were
detected above the limits in more than one CSLs. TPC can provide a
general indication of the microbiological quality of food; a high TPC
may indicate that the products may have been prepared unhygienically
or stored inappropriately (NSW Food Authority, 2013). The TPC that
exceeded 106 CFU/g indicates that such foods contain food poisoning
pathogens such as salmonella, staphylococci, E. coli, et cetera. (Iacumin
& Comi, 2019; Muirhead, 2019; Rodrigues et al., 2018). Moreover, food
contact surfaces are an additional crucial potential source of
cross-contamination, while sanitation (cleaning and disinfection) is the
significant day-to-day control. The detection of E. coli is widely used as a
tool for measuring the effectiveness of sanitation programs (Buchanan &
Oni, 2012). Furthermore, the present study found TPC of Salmon Nigiri
Sushi prepared in outlets 1 and 2 that are ISO 22000-certified FSMS
has exceeded the limits. High TPC in the final product of outlets 1
and 2 is most likely due to the use of a contaminated cutting board and
knife dedicated to handling Salmon. In outlets 1 and 2, E. coli counts for
both CSL 11 (i.e., cutting boards dedicated to cut Salmon only) and CSL
16 (i.e., knife dedicated to cut Salmon only) were exceeded the limit.
The results are consistent with Nahar and Mahyudin (2018), who
established a correlation between high TPC and E. coli on the swab
samples of food contact surfaces (spoons) in the selected Klang Valley
area restaurants. Further, this is similar to Nik Rosmawati, Wan Manan,
Noor Izani, and Nik Nurain (2014) ‘s work in which microbiological
analysis of food contact surfaces such as chopping board, apron, and
Food Control 127 (2021) 108111
Food safety indicators Overall Air quality
indicator
Bacillus Vibrio Listeria Total Plate Mould and
cereus parahaemolitycus monocytogenes Count Yeast
kitchen utensils (knife and spoons inclusive) was conducted. Different
researchers showed that E. coli commonly present on the cutting board
(Abdul-Mutalib, Syafinaz, Sakai, & Shirai, 2015; Isa, Nur Syifa’,
Fathurrahman, & Nor-Khaizura, 2018). Isa et al. (2018) isolated E.coli
from 24 cutting board samples collected around Seri Kembangan,
Selangor, Malaysia. In another study, Abdul-Mutalib et al. (2015)
detected E.coli that exceeded the limit (6 log CFU/g) in eight out of 12
cutting boards that were sampled in Seri Kembangan, Selangor,
Malaysia. Cunningham, Rajagopal, Lauer, and Allwood (2011) cited
improper sanitation for the presence of E.coli on the food contact sur­
faces. In addition, Kirezieva, Jacxsens, Uyttendaele, Van Boekel, and
Luning (2013) identified administrative conditions that revolve around
people through the variability of workforce composition and sufficiency
of operators’ competencies as factors that affect the output of a FSMS.
For example, outlet 2 is considered a large size premise and patronized
by many customers with an estimated total of 300 per day; however, it is
managed by mostly inexperienced employees (Table 1). Foodservice is a
less structured work environment serving food to order and typically
suffered high employee turnover rates (Moona, Ramendran, & Yacob,
2012). Different authors identified various factors, in addition to
knowledge, that affect employees’ FS practices, including time con­
straints, turnover, and training, and regarded them as the common
barriers for the effective implementation of FSMS (Galstyan & Har­
utyunyan, 2016; Strohbehn et al., 2014). This is similar to Nieto-­
Montenegro, Brown, and LaBorde (2008) ‘s work, in which FS practices
of workers in fruit and vegetable production were evaluated, and their
study has found the insufficiencies in operators’ knowledge and
involvement besides technological expertise and formalization lead to
lower FS levels of implemented FSMS.
In contrast, the TPC of Salmon Nigiri Sushi in outlets 3 and 4 that are
non-ISO 22000-certified FSMS were lower than the established limit. It
appeared that non-ISO 22000-certified FSMS outlets are better in per­
forming cleaning and sanitation of food contact surfaces than ISO
22000-certified FSMS outlets. Especially outlet 3 that was able to serve
Salmon Nigiri Sushi with TPC lower than the limit at 5.77 log10 CFU/g,
possibly due to effective cleaning and sanitation practices in outlet 3 as
evidence by low E. coli counts for all food contact surfaces (from CSL 11
through CSL 20) tested (Table 5). In contrast to outlet 2, outlet 3 is a
smaller premise that is patronized by a smaller number of customers and
managed by the experienced employee (Table 1). Due to the smaller
crowd, experienced employees can better implement FS practices in the
much smaller premises. Lee and Seo (2020) also indicated that variables,
including the characteristics of food premises, such as the size of the
operation and number of customers served, are among the motivator
factors influencing FS practices. In addition, the Japanese chain
restaurant that participated in the present study has more than 100
outlets throughout Malaysia. Although few of the outlets are ISO
22000-certified FSMS, the remaining others are not; a team of quality
assurance officers manages all outlets, and they are based in a head­
quarter office in Kuala Lumpur, Malaysia. To promote better
8
R.N. Fathurrahman et al. Food Control 127 (2021) 108111

Table 5
Microbiological qualities of Salmon Nigiri Sushi at various Critical Sampling Locations in the outlet 3 of non-ISO 22000-certified FSMS Japanese chain restaurant.
Critical Sampling Location (CSL) Hygiene indicators Food safety indicators Overall Air quality
indicator (log10 CFU/m)

Staphylococcus Coliform Escherichia Bacillus Vibrio Listeria Total Plate Mould and
aureus coli cereus parahaemolitycus monocytogenes Count Yeast

CSL1: Salmon slice after thawing 1.33 ± 0.81 1.29 ± 0.29 ± 0.85 -a ND ND 4.09 ± 1.12 –
0.77
CSL2: Salmon slice after cutting 1.39 ± 0.81 1.29 ± 0.26 ± 0.75 – ND ND 5.50 ± 1.48 –
0.93
CSL3: Salmon slice after 5 h of 1.36 ± 0.87 1.33 ± 0.35 ± 0.77 – ND ND 5.54 ± 2.03 –
storage 0.81
CSL4: Salmon slice after 10 h of 1.36 ± 0.79 1.33 ± 0.31 ± 0.82 – ND ND 5.64 ± 0.88 –
storage 0.89
CSL5: Uncooked rice 1.27 ± 0.89 1.34 ± 0.29 ± 0.85 ND – ND 1.81 ± 1.35 –
0.91
CSL6: Cooked rice 1.24 ± 0.93 1.29 ± 0.34 ± 0.91 ND – ND <1.00 –
0.93
CSL7: Cooked rice after mixed 1.31 ± 0.82 1.33 ± 0.26 ± 0.83 ND – ND <1.00 –
with vinegar 0.81
CSL8: Rice mix after 5 h of 1.31 ± 0.89 1.41 ± 0.31 ± 0.77 ND – ND <1.00 –
storage 0.63
CSL9: Rice mix after 10 h of 1.31 ± 0.89 1.31 ± 0.31 ± 0.97 ND – ND <1.00 –
storage 0.85
CSL10: Salmon nigari sushi 1.29 ± 0.85 1.36 ± 0.33 ± 0.62 ND – ND 5.77 ± 1.21 –
0.79
CSL11: Cutting board (dedicated 1.27 ± 0.89 1.27 ± 0.38 ± 0.81 – – – 5.20 ± 1.03 –
to cut Salmon only) 0.96
CSL12: Cutting board (dedicated 1.33 ± 0.96 1.29 ± 0.34 ± 0.83 – – – 4.78 ± 1.21 –
to cut seafood beside Salmon) 0.77
CSL13: Cutting board (dedicated 1.35 ± 0.77 1.35 ± 0.34 ± 0.83 – – – 3.50 ± 1.45 –
to cut meat only) 0.77
a
refers to parameter not analysed for this critical sampling location

Critical Sampling Location (CSL) Hygiene indicators Food safety indicators Overall Air quality
indicator

Staphylococcus Coliform Escherichia Bacillus Vibrio Listeria Total Plate Mould and
aureus coli cereus parahaemolitycus monocytogenes Count Yeast

CSL14: Cutting board (dedicated to 1.31 ± 0.93 1.31 ± 0.29 ± 0.85 -a – – 4.36 ± 1.98 –
cut ready-to-eat food only) 0.85
CSL15: Cutting board (dedicated to 1.24 ± 0.77 1.38 ± 0.34 ± 0.83 – – – 7.20 ± 1.67 –
cut vegetable only) 0.72
CSL16: Knife (dedicated to cut 1.34 ± 0.83 1.3 ± 0.33 ± 0.89 – – – 5.50 ± 1.77 –
Salmon only) 0.73
CSL17: Knife (dedicated to cut 1.30 ± 0.82 1.34 ± 0.36 ± 0.79 – – – 4.52 ± 2.05 –
seafood beside Salmon) 0.83
CSL18: Knife (dedicated to cut 1.29 ± 0.85 1.24 ± 0.31 ± 0.93 – – – 4.96 ± 1.54 –
meat only 0.77
CSL19: Knife dedicated to cut 1.36 ± 0.79 1.23 ± 0.24 ± 0.86 – – – 5.77 ± 1.61 –
ready-to-eat food only) 0.71
CSL20: Knife (dedicated to cut 1.31 ± 0.89 1.23 ± 0.24 ± 0.77 – – – 5.64 ± 1.61 –
vegetable only) 0.87
CSL21: Personal hygiene before 1.31 ± 0.77 1.27 ± 0.36 ± 0.87 – – ND 2.25 ± 1.74 –
handwash 0.81
CSL22: Personal hygiene after 1.29 ± 0.85 1.27 ± 1.29 ± 0.85 – – ND 2.13 ± 1.48 –
handwash 0.62
CSL23: Apron 1.23 ± 0.87 1.24 ± 0.34 ± 0.75 – – ND 2.10 ± 1.48 –
0.93
CSL24: Gloves 1.24 ± 0.86 1.35 ± 0.24 ± 0.77 – – ND <1.00 –
0.93
CSL25: Air quality in wet kitchen – – – – – – – 1.44 ± 0.48
a
refers to parameter not analysed for this critical sampling location

Critical Sampling Location Hygiene indicators Food safety indicators Overall Air quality
(CSL) indicator

Staphylococcus Coliform Escherichia Bacillus Vibrio Listeria Total Plate Mould and
aureus coli cereus parahaemolitycus monocytogenes Count Yeast

CSL26: Air quality in sushi -a – – – – – – 1.38 ± 0.61

preparation table
CSL27: Air quality in service – – – – – – – 1.51 ± 0.44
area
CSL28: Water quality – 0.29 ± 0.35 ± 0.77 – – – – 2.25 ± 1.65 –
(filtered) 0.85
CSL29: Water quality – 3.33 ± 3.57 ± 0.81 – – – – 6.52 ± 1.48 –
(unfiltered) 0.72
FS Levelb 3 1 1 3 3 3 1 3
(continued on next page)

9
R.N. Fathurrahman et al.
Table 5 (continued )
Critical Sampling Location Hygiene indicators
(CSL)
Staphylococcus Coliform Escherichia
aureus coli
FS Total 18/24
FS Outputc (2–3)
a
Refers to parameter not analysed for this critical sampling location.
b
Level 3 – Good result (legal criteria or guidelines are respected, no improvement are needed – current level of FSMS is high enough to cover this hazard. Level 2 –
Medium result (legal criteria or guidelines are exceeded, improvements need to be made on a single control activity of FSMS). Level 1 – Low result (legal criteria or
guidelines are exceeded, improvements need to be made on multiple control activities of the FSMS).
c
An overall score of 1 (poor risk) was assigned when the sum of the levels was 8–10, a sum of 11–14 resulted in an overall scores of 1–2 (poor to moderate level), a
sum of 15–17 resulted in an overall score of 2 (moderate-risk), as sum of 18–21 resulted in an overall scores of 2–3 (moderate to good level), and a sum of 22 or 24
resulted in an overall score of 3 (good level).
implementation of FSMS in the Japanese chain restaurants, the suc­
cessful implementation of FS practices in outlet 3 should be made visible
to the team of quality assurance officers that manage all other outlets to
ease their decision-making.
In addition, hand washing is a fundamental precautionary measure
to protect against the spread of disease, and this is among the primary
practices that help to reduce the transfer of bacteria, whether from
person to person or from person to food contact surfaces (Chinakwe
et al., 2012). In outlet 2, Staphylococcus aureus was detected on the food
handlers’ hands (before and after handwashing), and the counts were
above the acceptable level of 102 CFU/g; however, Staphylococcus aureus
was detected below the limit in other outlets. The results obtained from
this study could not be compared with the ones from the literature
because of the unavailability of studies that compare the counts of
Staphylococcus aureus before and after hand washing during Salmon’s
preparation Nigiri Sushi. Most studies reported in the literature pre­
dominantly reported the Staphylococcus aureus counts of the
off-the-shelf sushi (Abdel-Hakeem, Mahmoud, & Abdel-Hafeez, 2019;
Li, Stegger, Dalsgaard, & Leisner, 2019; Yap et al., 2019). Nevertheless,
Abdul-Rashid (2017) compared the counts of Staphylococcus aureus
before and after hand washing during the chicken dish preparation and
reported a mixed result, in which Staphylococcus aureus in one hospital
kitchen was detected below the limit, whereas three other kitchens re­
ported the counts were above the limit. Furthermore, food handlers with
poor personal hygiene and improper food handling practices in the retail
industry have been the reasons for most Staphylococcal food poisoning
outbreaks (Dablool, 2014). E coli counts were also determined on the
swab samples of food handlers’ hands and found that E. coli in all outlets
exceeded the acceptable level. The use of sanitizer, especially during
hand washing, can reduce microbial contamination from food handlers
(Zulfakar, Sahani, & Hamid, 2018). The researchers of this current study
had observed that food handlers did not incorporate hand sanitizer in
handwashing and therefore explains the results of high Staphylococcus
aureus and E coli counts on the food handlers’ hands after hand washing,
especially in outlets 1, 2 and 4. Clayton and Griffith (2008) suggested
that the type of FS culture existing within a business can explain why
food handlers choose not to implement known FS practices. Nyarugwe
et al. (2018) assessed the FS culture in dairy processing organizations
using a comprehensive mixed-methods approach and reported that a
poor microbial safety performance likely related to noncompliance with
sanitation requirements, negative attitudes towards personal hygiene
and an ambivalent attitude towards sanitation. In line with the data
reported by Nyarugwe et al. (2018) and Ungku Fatimah, Strohbehn, and
Arendt (2014), our findings suggest that there is a need for continued
efforts to ensure that effective procedures, training, and monitoring to
be implemented, especially in a Japanese restaurant that serves raw
fresh food such as sushi, to protect public health.
Although coliforms are used as the universal food hygiene indicator,
they are unable to indicate the presence of specific pathogenic micro­
organisms (Nkere, Ibe, & Iroegbu, 2011). According to Chye, Abdullah,
Food Control 127 (2021) 108111
Food safety indicators Overall Air quality
indicator
Bacillus Vibrio Listeria Total Plate Mould and
cereus parahaemolitycus monocytogenes Count Yeast
and Ayob (2004), there was a significant correlation between Coliform
and E. coli. Their studies showed that tested food samples with higher
numbers of Coliform detected would also have higher E. coli counts. The
present study found the exceeded limits of Coliform, E. coli, and TPC in
unfiltered and filtered tap water in all outlets. This is similar to the work
of Anita, Saharuddin, Tan, Linn, and Bokhari (2016), who evaluated the
drinking water quality collected from various households and restau­
rants in Selangor, Malaysia, and reported that 38% of the tested samples
had coliform counts that exceeded the limit. Similarly, Chan, Zalifah,
and Norrakiah (2007) evaluated water samples collected before and
after filtration treatment on samples collected randomly from houses in
Klang Valley and reported that TPC exceeded the limit for all samples
and E. coli were detected exceeded the limit in 9 out of 10 samples
collected. Coliforms in treated water that is claimed as usually
coliform-free may indicate treatment ineffectiveness (Rompre, Servais,
Baudart, de-Roubin, & Laurent, 2002). It is possible that the filtering
system of water from the tap source is not effectively maintained, in
which the water filters are not changed according to the schedule that in
turn might explain the exceeded limits of Coliform, E. coli, and TPC in
unfiltered and filtered tap water samples. In addition, as E. coli is found
in the intestinal tract of both humans and animals, finding this organism
in ready-to-eat foods is generally viewed as an indication of fecal
contamination (Jay, Loessner, & Golden, 2008). It seems that fecal
contamination has happened in the majority of CSLs in all outlets. This
situation is possible since E. coli counts in filtered tap water in the
aforementioned outlets have already exceeded the limit, and they were
used in the cleaning and sanitation of food contact surfaces, including
hand washing. Hsin-I Feng (2012) stated that proper hygiene, including
hot wash using filtered hot water and sanitizer at the end of each wash, is
paramount in Japanese restaurants that served raw fresh food such as
sushi. Besides the absence of hand sanitizer in hand washing, re­
searchers observed the absence of hot wash and the use of sanitizer
during cleaning and sanitation in Japanese chain restaurants. The pre­
sent study utilizes MAS, a well-established assessment tool, to evaluate
and therefore differentiate the performance of the FSMS of outlets that
are FSMS certified or not certified with ISO 22000. However, other
research methods such as face-to-face in-depth interviews, participant
observations, and organizational document analysis were not utilized.
Therefore, FSMS activities and records, especially on the frequency of
changing water filters, compliance to the handwashing procedures, and
compliance to cleaning and sanitation procedures, could not be verified.
Future studies could utilize a mix-methods approach to obtain insight
into the barriers and motivators for implementing FSMS in a Japanese
chain restaurant, using quantitative methodology.
Bacillus cereus, Vibrio parahaemolyticus, and Listeria monocytogenes
were not detected at all CSLs, and therefore the FS level was determined
at level 3 (good result) for all outlets. The results are consistent with
Lahou, Jacxsens, Daelman, Van Landeghem, and Uyttendaele (2012),
who evaluated the performance of FSMS in a food service operation and
reported an absence of FS indicators such as Bacillus cereus, Listeria
10
R.N. Fathurrahman et al. Food Control 127 (2021) 108111

Table 6
Microbiological qualities of Salmon Nigiri Sushi at various Critical Sampling Locations in the outlet 4 of non-ISO 22000-certified FSMS Japanese chain restaurant.
Critical Sampling Location (CSL) Hygiene indicators Food safety indicators Overall Air quality
indicator

Staphylococcus Coliform Escherichia Bacillus Vibrio Listeria Total Plate Mould and
aureus coli cereus parahaemolitycus monocytogenes Count Yeast

CSL1: Salmon slice after thawing 1.29 ± 0.85 2.28 ± 2.22 ± 0.73 -a ND ND 4.58 ± 1.48 –
0.83
CSL2: Salmon slice after cutting 1.27 ± 0.72 1.38 ± 0.27 ± 0.72 – ND ND 4.67 ± 1.71 –
0.72
CSL3: Salmon slice after 5 h of 1.33 ± 0.81 2.29 ± 0.35 ± 0.86 – ND ND 5.67 ± 1.57 –
storage 0.85
CSL4: Salmon slice after 10 h of 1.3 ± 0.73 2.33 ± 0.23 ± 0.79 – ND ND 6.64 ± 1.32 –
storage 0.81
CSL5: Uncooked rice 1.23 ± 0.79 1.31 ± 0.33 ± 0.72 ND – ND 2.87 ± 1.91 –
0.82
CSL6: Cooked rice 1.27 ± 0.81 1.31 ± 0.36 ± 0.87 ND – ND 4.01 ± 1.71 –
0.93
CSL7: Cooked rice after mixed with 1.26 ± 0.83 1.33 ± 0.3 ± 0.82 ND – ND 5.35 ± 1.63 –
vinegar 0.81
CSL8: Rice mix after 5 h of storage 1.33 ± 0.81 1.31 ± 0.27 ± 0.81 ND – ND 5.37 ± 1.53 –
0.85
CSL9: Rice mix after 10 h of storage 1.31 ± 0.82 1.23 ± 0.23 ± 0.6 ND – ND 5.36 ± 1.84 –
0.61
CSL10: Salmon nigari sushi 1.38 ± 0.72 1.31 ± 0.18 ± 0.63 ND – ND 5.21 ± 1.69 –
0.89
CSL11: Cutting board (dedicated to 1.31 ± 0.85 1.31 ± 0.26 ± 0.83 – – – 4.67 ± 1.96
cut Salmon only) 0.89
CSL12: Cutting board (dedicated to 1.26 ± 0.83 2.35 ± 1.90 ± 0.82 – – – 4.44 ± 2.16
cut seafood beside Salmon) 0.82
CSL13: Cutting board (dedicated to 1.31 ± 0.93 1.31 ± 1.29 ± 0.77 – – – 4.55 ± 1.71
cut meat only) 0.77
a
refers to parameter not analysed for this critical sampling location

Critical Sampling Location (CSL) Hygiene indicators Food safety indicators Overall Air quality
indicator

Staphylococcus Coliform Escherichia Bacillus Vibrio Listeria Total Plate Mould and
aureus coli cereus parahaemolitycus monocytogenes Count Yeast

CSL14: Cutting board (dedicated to 1.38 ± 0.81 1.27 ± 1.00 ± 0.93 -a – – 4.64 ± 1.75 –
cut ready-to-eat food only) 0.72
CSL15: Cutting board (dedicated to 1.26 ± 0.91 1.31 ± 2.02 ± 0.83 – – – 6.59 ± 1.68 –
cut vegetable only) 0.89
CSL16: Knife (dedicated to cut 1.31 ± 0.93 2.30 ± 0.27 ± 0.89 – – – 4.01 ± 1.95 –
Salmon only) 0.93
CSL17: Knife (dedicated to cut 1.31 ± 0.89 2.42 ± 0.34 ± 0.91 – – – 5.95 ± 1.57 –
seafood beside Salmon) 0.72
CSL18: Knife (dedicated to cut 1.26 ± 0.91 1.31 ± 2.33 ± 0.91 – – – 4.67 ± 1.57 –
meat only 0.93
CSL19: Knife (dedicated to cut 1.31 ± 0.82 1.38 ± 0.31 ± 0.89 – – – 4.56 ± 1.59 –
ready-to-eat food only) 0.72
CSL20: Knife (dedicated to cut 1.31 ± 0.89 1.31 ± 0.29 ± 0.85 – – – 6.51 ± 1.86 –
vegetable only) 0.85
CSL21: Personal hygiene before 1.23 ± 0.61 1.38 ± 2.31 ± 0.83 – – ND 2.35 ± 1.67 –
handwash 0.81
CSL22: Personal hygiene after 1.19 ± 0.73 3.29 ± 1.82 ± 0.89 – – ND 2.21 ± 2.01 –
handwash 0.93
CSL23: Apron 1.29 ± 0.85 1.33 ± 2.42 ± 0.70 – – ND 2.08 ± 2.06 –
0.81
CSL24: Gloves 1.29 ± 0.93 1.27 ± 0.31 ± 0.85 – – ND 2.02 ± 1.53 –
0.89
CSL25: Air quality in wet kitchen – – – – – – – 2.93 ± 1.01
a
refers to parameter not analysed for this critical sampling location

Critical Sampling Location Hygiene indicators Food safety indicators Overall Air quality
(CSL) indicator

Staphylococcus Coliform Escherichia Bacillus Vibrio Listeria Total Plate Mould and
aureus coli cereus parahaemolitycus monocytogenes Count Yeast

CSL26: Air quality in sushi -a – – – – – – 2.54 ± 1.09

preparation table
CSL27: Air quality in service – – – – – – – 3.01 ± 1.22
area
CSL28: Water quality – 2.19 ± 1.33 ± 0.81 – – – – 4.67 ± 1.59 –
(filtered) 0.73
CSL29: Water quality – 4.39 ± 4.23 ± 0.79 – – – – 6.51 ± 1.51 –
(unfiltered) 0.73
FS Levelb 3 1 1 3 3 3 1 1
(continued on next page)

11
R.N. Fathurrahman et al.
Table 6 (continued )
Critical Sampling Location Hygiene indicators
(CSL)
Staphylococcus Coliform Escherichia
aureus coli
FS Total 16/24
FS Outputc 2
a
Refers to parameter not analysed for this critical sampling location.
b
Level 3 – Good result (legal criteria or guidelines are respected, no improvement are needed – current level of FSMS is high enough to cover this hazard. Level 2 –
Medium result (legal criteria or guidelines are exceeded, improvements need to be made on a single control activity of FSMS). Level 1 – Low result (legal criteria or
guidelines are exceeded, improvements need to be made on multiple control activities of the FSMS).
c
An overall score of 1 (poor risk) was assigned when the sum of the levels was 8–10, a sum of 11–14 resulted in an overall scores of 1–2 (poor to moderate level), a
sum of 15–17 resulted in an overall score of 2 (moderate-risk), as sum of 18–21 resulted in an overall scores of 2–3 (moderate to good level), and a sum of 22 or 24
resulted in an overall score of 3 (good level).
monocytogenes, and Salmonella at all 10 CSLs, covering both product and
environmental samples. Similarly, Osés et al. (2012) reported the
absence of FS indicators such as Listeria monocytogenes at all 10 CSLs
along the lamb production chain. Although the consumption of raw fish
such as sashimi has been increasing Vibrio outbreaks, Vibrio para­
haemolyticus was not detected in any samples collected. Different au­
thors reported that spoilage bacteria normally outgrow pathogenic
bacteria during storage (Iacumin & Comi, 2019; Nkere et al., 2011; NSW
Food Authority, 2008), and the present study supported the findings of
these cited studies. Salmon Nigiri Sushi is an example of perishable foods
that have a short life span. Therefore, the production of Salmon Nigiri
Sushi of good quality depends on the choice of raw materials, good rice
acidification (pH of the rice must be less than 4.6), and the maintaining
of cold chain during preparation and storage as those are vital in a way
to obtain products of good microbiological status as reported by Mus­
colino et al. (2014).
5. Conclusions
This study showed the performance of FSMS in relation to the
microbiological FS outputs of Salmon Nigiri Sushi of outlets that are
non-ISO 22000-certified FSMS were better than outlets that are ISO
22000-certified FSMS. However, none of the outlets achieved their FS
objectives, a good level with an overall 3 of FS performance score.
Although Bacillus cereus, Vibrio parahaemolyticus, and Listeria mono­
cytogenes were not detected, E. coli counts have exceeded the limit (even
in filtered tap water). Low results (level 1) of FS levels for TPC besides
E. coli in all outlets indicated a broader cross-contamination problem,
particularly the practice of using a contaminated cutting board and knife
that are dedicated to handling Salmon. Therefore, potential measures
are discussed to improve, especially in cleaning and sanitation of food
contact surfaces, handwashing, and compliance to procedures. Future
intervention strategies can be taken to these identified areas as an
improvement to eliminate cross-contamination problems and assure the
safety of Salmon Nigiri Sushi that served to consumers.
CRediT authorship contribution statement
R.N. Fathurrahman: Investigation, Project administration, Meth­
odology, Formal analysis, Validation, Visualization, Writing – original
draft, Writing – review & editing. Y. Rukayadi: Resources, Conceptu­
alization, Methodology, Formal analysis, Validation, Supervision,
Writing – review & editing. U.Z.A. Ungku Fatimah: Resources,
Conceptualization, Methodology, Formal analysis, Supervision, Writing
– review & editing. S. Jinap: Supervision, Validation, Writing – review
& editing. N.A. Abdul-Mutalib: Supervision, Validation, Writing – re­
view & editing. M. Sanny: Funding acquisition, Resources, Conceptu­
alization, Methodology, Formal analysis, Validation, Supervision,
Writing – review & editing, Project administration.
Food Control 127 (2021) 108111
Food safety indicators Overall Air quality
indicator
Bacillus Vibrio Listeria Total Plate Mould and
cereus parahaemolitycus monocytogenes Count Yeast
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