Food Control 37 (2014) 51e55
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Food Control
journal homepage: www.elsevier.com/locate/foodcont
Transmission of Listeria monocytogenes from raw chicken meat to
cooked chicken meat through cutting boards
Sur Guat Goh a, *, Afsah-Hejri Leili a, Chee Hao Kuan a, Yuet Ying Loo a, Ying Ling Lye a,
Wei San Chang a, Puspanadan Soopna a, Mohd. Shahril Najwa a, John Yew Huat Tang b,
Rukayadi Yaya a, Mitsuaki Nishibuchi c, Yoshitsugu Nakaguchi c, Radu Son a
a
Food Safety Research Center (FOSREC), Faculty of Food Science and Technology, Universiti Putra Malaysia, 43400 UPM Serdang, Selangor Darul Ehsan,
Malaysia
Faculty of Food Technology, Universiti Sultan Zainal Abidin, 21300 Kuala Terengganu, Terengganu Darul Iman, Malaysia
c
Center for Southeast Asian Studies, Kyoto University, Kyoto 606-8501, Japan
b
a r t i c l e i n f o
a b s t r a c t
Article history:
Received 5 May 2013
Received in revised form
29 July 2013
Accepted 20 August 2013
Listeria monocytogenes (L. monocytogenes) is a food-borne pathogen contaminating poultry products.
Ready-to-eat (RTE) cooked chicken meat can easily be contaminated with L. monocytogenes in postprocessing activities. This study aimed to determine transmission of L. monocytogenes from raw
chicken meat to hot and cooled chicken meat through polyethylene and wooden cutting boards. Raw
chicken breast samples were purchased from retail markets and were artificially contaminated with
L. monocytogenes at concentration of 7.35 0.22 log CFU/ml. Contaminated raw samples were placed on
polyethylene and wooden cutting boards to simulate bacterial transfer to cutting boards. Cooked chicken
samples (hot and cooled) were then placed on the same cutting boards to simulate transfer of bacteria
from cutting boards to cooked meat. L. monocytogenes successfully attached to polyethylene and wooden
cutting boards and recovered after holding time up to 1 h. Transmissions of L. monocytogenes to cooled
cooked samples from both types of cutting boards were relatively higher than hot cooked samples.
Moreover, transfer rates of L. monocytogenes from wooden cutting boards at holding time of 1 h to both
cooled and hot cooked samples were lower than those from polyethylene cutting board. It is recommended to use different cutting boards for raw and cooked materials and apply detergents and hot water
for cleaning procedure to eliminate L. monocytogenes attached to the cutting boards and prevent crosscontamination of final products.
Ó 2013 Elsevier Ltd. All rights reserved.
Keywords:
Cutting boards
Cooked chicken meat
Listeria monocytogenes
Transmission
1. Introduction
Listeria monocytogenes (L. monocytogenes) is a food pathogen
contaminating variety of food products such as vegetables, milk,
dairy products, poultry and meat products (Ryser & Marth, 2000).
Ready-to-eat (RTE) cooked chicken meat can easily be contaminated with L. monocytogenes in post-processing activities
(Beresford, Andrew, & Shama, 2001). Consumption of contaminated
RTE cooked chicken meat results in severe health problems,
including listeriosis with high mortality rate (Low & Donachie,
1997; Siegman-Igra et al., 2002). Listeriosis is a rare food-borne
disease comparing to salmonellosis and campylobacteriosis. However, like any other zoonotic disease, its significance is not fully
* Corresponding author. Tel.: þ60 389471961; fax: þ60 389423552.
E-mail address: [email protected] (S.G. Goh).
0956-7135/$ e see front matter Ó 2013 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.foodcont.2013.08.030
dependent on its occurrence (EFSA, 2010). The fatality rate and
severity of the disease depends on other factors. USDA set a zero
tolerance policy for L. monocytogenes in RTE foods (USDA-FSIS,
2004).
L. monocytogenes can be easily inactivated by heat treatments,
such as cooking (Cygnarowicz-Provost, Whiting, & Craig, 1994).
Muriana, Quimby, Davidson, and Grooms (2002) showed that postpackage pasteurization by submersion heating can reduce
L. monocytogenes in RTE deli meats. Liquid smoke, potassium/sodium lactate, quaternary ammonium compounds and bacteriocins
are used to reduce L. monocytogenes in RTE poultry and meat
products (Mereghetti, Quentin, Marquet-Van Der Mee, & Audurier,
2000; Ryser & Marth, 2000). Fabrizio and Cutter (2005) showed
that application of electrolyzed oxidizing water on RTE meat can
reduce number of L. monocytogenes.
Presence of L. monocytogenes in cooked meat is due to crosscontamination. Cross-contamination is referred to transmission of
52
S.G. Goh et al. / Food Control 37 (2014) 51e55
bacteria (direct or indirect) from contaminated source to a noncontaminated source. Food-related infections are attributed to
cross-contamination of food products after processing or during
storage and handling. Moreover, pathogens can be spread from one
contaminated location to a clean location (Mylius, Nauta, &
Havelaar, 2007). Cross contamination is well known as a route of
transmission of bacteria from naturally contaminated sources to
finished products (Kusumaningrum, van Asselt, Beumer, &
Zwietering, 2004). Cross-contamination of cooked meat during
food preparation in kitchen, results in an unsafe food (de Boer &
Hahné, 1990).
Cutting and chopping boards are common utensils in kitchens
and food processing units. Different types of cutting boards can be
used such as polyethylene, wood and bamboo boards. Wooden
cutting boards are considered as potential source of food pathogens
as deep cracks on the surface of the board provides a suitable
environment for microorganisms to survive (Carpentier, 1997).
Plastic (or polyethylene) cutting boards were introduced in 1970s
to replace traditional wooden cutting board. Cutting boards used
for food preparation in domestic kitchens, had always been
recognized as possible vehicles for cross-contamination (Cliver,
2006). Different cutting boards must be used for cutting raw materials and cooked food as pathogens on the surface of cutting
boards can easily be transmitted to cooked food. Re-use of the same
cutting board for raw and RTE food without washing is a potential
source of L. monocytogenes transmission (Jevsnik, Hoyer, & Raspor,
2008). It is recommended to wash cutting boards with detergents
and warm water between using the cutting board for raw material
and RTE or cooked food (Anonymous, 2008). Several researches
were conducted to find a material that can reduce the risk of crosscontamination while using cutting boards. Triclosan is a compound
with antimicrobial properties which is allowed to be used in plastic
food-contact materials in European countries (European
Commission, 2010). Triclosan showed antibacterial activity over a
wide range of food pathogens (Møretrø, Høiby-Pettersen,
Habimana, Heir, & Langsrud, 2011). In another research, Møretrø,
Høiby-Pettersen, Halvorsen, and Langsrud (2012) showed that
cutting boards containing silver have antibacterial activity against
some important food pathogens.
L. monocytogenes is able to grow at ambient temperature or
below. Remnant of raw meat left on cutting board is considered a
potential transmission vehicle for bacterial transfer to RTE food (Ak,
Cliver, & Kaspar, 1994a). There is limited research on transmission
of L. monocytogenes through cutting boards. Thus, this study was
conducted to determine transmission of L. monocytogenes from raw
chicken meat to cooked meat via cutting boards.
single cutting board was sterilized under UV light for 1 h in laminar
flow hood before experiment.
2.3. Chicken samples
Sample preparation was carried out according to Tang et al.
(2011). Chicken breasts were purchased from wet markets located
at Serdang, Selangor, Malaysia. Chicken breasts were cut into
approximately 10 0.5 g pieces. Cooked chicken samples were
prepared by boiling the samples in sterile distilled water for 30 min.
Cooled chicken samples were prepared by storing the cooked
chicken meat in sterile beaker at room temperature (28 0.5 C)
for 1 h. Hot chicken samples were used immediately after boiling
(100 0.5 C).
2.4. Cross-contamination experiment
All utensils were autoclaved before use. Four groups of raw
chicken meat and 2 groups of cooked (cooled and hot) chicken
meat were used in this experiment. All chicken samples were
inoculated with 0.2 ml microbial load of 7.35 0.22 log10 CFU/ml of
L. monocytogenes. First group of the samples were used as control
samples to determine the number of L. monocytogenes attached to
chicken meat. The mean value was determined as mean concentration of L. monocytogenes attached to chicken meat. The second
group samples were spread over the surface of cutting boards for
5 s. The surface of cutting board was enumerated for
L. monocytogenes immediately. The mean value was determined as
the mean number of bacteria transferred from chicken samples to
cutting boards. The third group samples were also spread over the
cutting boards for 5 s, and then cooled cooked chicken meats were
put on the same area immediately. Cooled cooked chicken meat
was then enumerated for L. monocytogenes. The mean value was
determined as the mean number of bacteria transferred from cutting boards to cooled cooked meat samples. The fourth group’s
samples were treated as the third group, but hot cooked chicken
meat was used instead of cooled cooked meat. The mean value was
determined as the mean number of bacteria transferred from cutting board to hot cooked meat. All experiments were done in
triplicate.
The whole experiment was repeated twice for two holding time,
which were 30 min and 1 h after attachment of contaminated
chicken on cutting board. Inoculated chicken samples were spread
over the cutting board’s surface for 5 s, and then the cutting boards
were left at ambient temperature for either 30 min or 1 h holding
time. Cooked chicken samples (cooled and hot) were put on the
same area after the holding time.
2. Materials and methods
2.5. Enumeration of L. monocytogenes
2.1. Preparation of L. monocytogenes inoculum
Pure culture of L. monocytogenes ATCC 19112 was inoculated on
PALCAM agar (Merck), and incubated for 48 h at 30 C. To prepare
the reference suspension, single colony of L. monocytogenes was
inoculated into 10 ml of Tryptic Soy Broth (TSB) (Merck) and
incubated for 1 day at 37 C (Wong et al., 2011). The harvested broth
culture was serially diluted (101e108) in normal saline (0.85%
sodium chloride) to determine the density of the bacterium by
spread plate method using PALCAM agar. The mean concentration
of the inoculums was approximately 7.35 0.22 log CFU/ml.
2.2. Cutting boards
Polyethylene and rubber wood cutting boards were purchased
from supermarkets and cut into approximately 3.5 3.5 cm. Every
Control samples, hot and cooled cooked chicken meat samples
were mixed with 90 ml of normal saline. Serial dilutions were
prepared in same diluents and plated in PALCAM agar using spread
plate technique. Plates were incubated for 48 h at 30 C and the
typical Listeria spp. colonies grown on PALCAM agar were considered as L. monocytogenes. The experiment was conducted twice
using triplicate samples each time.
2.6. Recovery method
According to our knowledge, there is no standard method for
recovery of bacteria from cutting boards’ surfaces. The method used
in this study was rinsing method proposed by Tang et al. (2011). The
surface of cutting board was rinsed using 100 ml of normal saline.
Successive dilutions were prepared in same diluents and plated in
S.G. Goh et al. / Food Control 37 (2014) 51e55
PALCAM agar using spread plate technique and plates were incubated at 30 C for 48 h.
2.7. Data analysis
Quantitative data were expressed as mean standard deviation
log10 CFU/g for chicken meat sample and log10 CFU/ml for
contaminated cutting board. Percentage of L. monocytogenes
(LMPs), (%) were reported as percentage of L. monocytogenes on the
recipient in comparison with the number of L. monocytogenes found
in the donor calculating as follows:
LMP ð%Þ ¼ ðCFUrecipient =CFUdonorÞ 100%
For statistical analysis, Minitab (v. 14) statistical package (Minitab Inc., PA, USA) (ManneWhitney Test) was used to determine
the significant (P 0.05) difference between transfer rates from
different type of cutting board to chicken samples.
3. Results
Results of transmission of L. monocytogenes from artificially
contaminated raw chicken samples to both polyethylene and
wooden cutting boards are presented in Table 1. Number of bacteria
transmitted to cooked chicken samples (cooled and hot) were
expressed as log10 CFU/g chicken.
Both types of cutting board were free of L. monocytogenes at the
beginning of the experiment. Inoculated samples were donor in
transmission of bacterium from raw sample to cutting boards
(polyethylene and wooden). The initial concentration of 7.35 0.22
log10 CFU/ml was used for all inoculated samples.
No significant difference (P > 0.05) was observed for bacterial
attachment to polyethylene cutting boards for time intervals of 0 s
(immediately), 30 min and 1 h. About 1 h after removal of
contaminated chicken sample from wooden cutting boards, transmission of bacteria was significantly (P 0.05) lower than 0 s
(immediately), 30 min and those on polyethylene cutting boards
(Table 1).
The LMP of bacteria to cooled samples from wooden cutting
board (1 h after contamination of cutting board) was significantly
(P 0.05) lower than all other bacterial transmission to cooled
samples. Transmission of bacteria from polyethylene cutting board
after 1 h to hot sample was lower (P 0.05) than polyethylene
53
cutting board [0 s (immediately)] and wooden cutting board [0 s
(immediately)]. Besides, L. monocytogenes could not be detected
from hot samples attached to wooden cutting boards at 1 h after
contamination of cutting boards.
At 0 s (immediately), there were no statistical significant
(P > 0.05) differences between the rates of L. monocytogenes
transmission from both polyethylene and wooden cutting boards to
cooled and hot samples. However, at 30 min, transmission of bacteria from both polyethylene and wooden cutting boards to cooled
samples were higher (P 0.05) than transmission of bacteria to hot
samples on wooden cutting boards. Furthermore, at 1 h, the
transfer rate of bacteria to cooled samples from wooden cutting
board were lower (P 0.05) than polyethylene cutting boards.
L. monocytogenes was undetectable after 1 h of inoculation on
wooden cutting board.
4. Discussion
There are several ways of exposure to disease including consumption of contaminated food or cooked food that has been crosscontaminated during preparation. Cross-contamination is a well
known route for transmission of bacteria from naturally contaminated sources to the finished products (Kusumaningrum et al.,
2004). Presence of bacteria on surfaces of cutting boards can lead
to transmission of bacterium to food and cause food-borne diseases. L. monocytogenes, is recognized as cross-contaminant on
kitchen cutting boards as it is able to be transmitted via food. As
mentioned before, remnant of raw meat left on cutting board is a
risk for transmission of bacteria to RTE food (such as raw vegetable
or cooked meat) (Ak et al., 1994a). This study simulated the condition of using un-washed cutting boards for cooked meat, after
removal of raw meat from the cutting boards. In this study, both
polyethylene and wooden cutting boards were initially free of
L. monocytogenes. Cooked meat was chosen to be used in this
experiment as a vehicle for transmission of bacteria to consumers
as it is assumed that all Listeria spp. were inactivated during heat
treatment. The study aimed to simulate cross-contamination on
cooked meat when using the cutting boards after 0 s (immediately),
30 min and 1 h of exposure to raw chicken meat. Generally, crosscontamination occurs if the food processing surfaces (such as cutting boards) are not cleaned properly. According to Ak et al. (1994a)
recovery of bacteria from cutting board within 3 min after inoculation, does not influenced by the age of the cutting boards
(whether it was new or used cutting board).
Table 1
Transmission of L. monocytogenes from artificially contaminated raw chicken samples to different types of cutting board and cross contamination of cooled and hot chicken
through plastic and wooden cutting boards.
0 s (immediately)
Transfer to cutting board
Plastic cutting board
Wooden cutting board
Transfer to cooled chicken meat
From plastic cutting board
From wooden cutting board
Transfer to hot chicken meat
From plastic cutting board
From wooden cutting board
30 min
1h
Log10 CFU/ml
LMP (%)
Log10 CFU/ml
LMP (%)
Log10 CFU/ml
LMP (%)
5.2 0.5
5.5 0.6
71.2 8.3ac
74.1 7.8a
5.4 0.2
4.6 1.4
72.6 3.4a
62.1 20.6a
5.1 0.3
0.4 1.3
71.0 4.0a
6.1 18.3b
4.7 0.6
4.8 0.3
88.5 6.4Aab
87.9 6.9Aa
4.9 0.3
3.2 1.2
90.2 4.8Aa
73.5 33.8ABa
4.5 0.3
0.4 1.2
87.2 6.9Aa
11.0 33.0Bb
3.9 1.6
3.8 2.2
73.2 28.5Aa
65.6 37.9Aa
2.8 2.2
0.8 1.6
51.1 39.0BCab
21.5 42.6Cab
1.3 1.9
0.0 0.0
25.0 37.6Bb
0.0 0.0a
The results were expressed as mean SD log10 CFU/ml. Each value in the table represents mean SD of three measurements from triplicate experiments (Log10 CFU/g for
chicken samples and log10 CFU/ml for washes from cutting boards).
LMP (%) were percentage of L. monocytogenes on the recipient in comparison with the number of L. monocytogenes found in the donor. LMP (%) ¼ (CFUrecipient/CFUdonor) 100%.
a
Undetectable counts.
b
Within columns, means SD followed by same capital letter are not significant (P 0.05) different.
c
Within rows, means SD followed by same small letter are not significant (P 0.05) different.
54
S.G. Goh et al. / Food Control 37 (2014) 51e55
It was found that L. monocytogenes can be transferred from raw
chicken samples to polyethylene cutting boards and was recovered
after 1 h of holding time and subsequently contaminate cooked
meat samples. Wooden cutting boards showed lower (P 0.05)
bacteria count after 1 h of using raw meat. This might be due to the
topography of different kind of cutting board. Inoculated bacteria
were readily recovered from polyethylene surfaces. Conversely,
inoculums were readily absorbed into wooden cutting board. This
finding was in agreement with previous findings by Ak, Cliver, and
Kaspar (1994b).
However, the temperature at which the samples were held had
an influence on transmission of L. monocytogenes from cutting
boards to cooked samples. Transfer rate of L. monocytogenes to hot
cooked samples at 30 min and 1 h was lower (P 0.05) comparing
to cooled samples. The finding is in agreement with the finding of
Tang et al. (2011), who reported that transfer rate of Campylobacter
jejuni from breast fillet to cooked sample maintained at room
temperature and boiling temperature (100 C) were 57.6% and
25.3% respectively.
Wooden cutting boards showed lower transmission of bacteria
to cooked samples (hot and cooled) at 1 h holding time compared
to polyethylene cutting boards. This might be due to the nature and
topography of wooden cutting boards which allowed absorption of
bacteria into the holes and cracks on the cutting board.
Washing of cutting boards with hot water and detergents after
use is an efficient method to eliminate the bacteria attached to the
surface of cutting boards. Unfortunately, some food-processing
equipment cleaners are not aware of the health risks associated
with L. monocytogenes. Improper cleaning procedures might
concomitantly displace bacteria from contaminated equipments to
other area within the processing environment. Moreover, some
bacterial cells can be transmitted to sterile surface and subsequently contaminate final food product (Taormina & Beuchat,
2002).
According to Wong et al. (2011), L. monocytogenes was able to be
transfered to food through direct contact with contaminated area
or during food handling. In their study, samples were cooked before
the experiment to destroy vegetative pathogens. As confirmed by
other researchers, cross-contamination of cooked samples can be
occurred during handling and distribution (Walls, 2006). Several
factors (such as density of the bacteria) affect cross contamination
process. In this study, samples were inoculated with high level of
L. monocytogenes to demonstrate the worst case at which raw
chicken samples were highly contaminated with L. monocytogenes
before being brought into kitchen. The inoculum used in this
experiment was approximately 109 CFU/ml of L. monocytogenes.
Transfer rate in reality might even be higher than the transfer rates
determined in this study.
As mentioned before, re-use of the same cutting board for raw
and RTE cooked food without washing is a critical factor in bacterial
transmission. In study of Worsfold and Griffith (1997), 60% of the
respondents used a single cutting board to perform all cuttings in
kitchen. While Altekruse, Street, Fein, and Levy (1996) stated that
only 67% of the respondents cleaned the cutting boards after being
used directly for raw meat. For safety purposes, different cutting
boards must be used to cut raw material and cooked food as
pathogens on the surface of cutting boards can easily be transmitted to cooked food. It is also recommended to conduct proper
washing process and minimize the contact time of food and cutting
board.
5. Conclusions
As shown in this study, cutting boards are potential vehicles for
cross contamination of L. monocytogenes from raw meat to RTE
meat, irrespective of material of the cutting boards. Generally,
L. monocytogenes can be transferred from naturally contaminated
raw chicken meat to cooked chicken meat and can even be spread
to other utensils and surfaces around kitchen. So, hands and
utensils involved in the preparation of cooked meat must be
cleaned and properly washed. Different utensils such as cutting
boards must be used for raw and cooked meat. Transfer rates of
L. monocytogenes from raw meat to cooked meat were influenced
by the material of the cutting boards. In order to study the survival
of L. monocytogenes on different materials, further study on the
cleaning and drying methods for the cutting boards is
recommended.
Acknowledgements
This research was supported by Grant-ineAid of Ministry of
Health, Labour and Welfare from Japan.
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