Assessment of Food Safety Knowledge, Attitude, Self-Reported Practices, and Microbiological Hand Hygiene of Food Handlers
Assessment of Food Safety Knowledge, Attitude, Self-Reported Practices, and Microbiological Hand Hygiene of Food Handlers
Assessment of Food Safety Knowledge, Attitude, Self-Reported Practices, and Microbiological Hand Hygiene of Food Handlers
Environmental Research
and Public Health
Short Communication
Assessment of Food Safety Knowledge, Attitude,
Self-Reported Practices, and Microbiological Hand
Hygiene of Food Handlers
Hui Key Lee 1 , Hishamuddin Abdul Halim 2 , Kwai Lin Thong 1 and Lay Ching Chai 1, *
1 Institute of Biological Sciences, Faculty of Science, University of Malaya, Kuala Lumpur 50603, Malaysia;
[email protected] (H.K.L); [email protected] (K.L.T)
2 Occupational Safety & Health Unit, Registrar’s Department, University of Malaya, Kuala Lumpur 50603,
Malaysia; [email protected]
* Correspondence: [email protected]; Tel.: +603-7967-5832
Abstract: Institutional foodborne illness outbreaks continue to hit the headlines in the country,
indicating the failure of food handlers to adhere to safe practices during food preparation. Thus,
this study aimed to compare the knowledge, attitude, and self-reported practices (KAP) of food
safety assessment and microbiological assessment of food handlers’ hands as an indicator of hygiene
practices in food premises. This study involved 85 food handlers working in a university located in
Kuala Lumpur, Malaysia. The food safety KAP among food handlers (n = 67) was assessed using a
questionnaire; while the hand swabs (n = 85) were tested for the total aerobic count, coliforms,
and Escherichia coli, Staphylococcus aureus, Salmonella, Vibrio cholerae and Vibrio parahaemolyticus.
The food handlers had moderate levels of food safety knowledge (61.7%) with good attitude (51.9/60)
and self-reported practices (53.2/60). It is noteworthy that the good self-reported practices were
not reflected in the microbiological assessment of food handlers’ hands, in which 65% of the food
handlers examined had a total aerobic count ≥20 CFU/cm2 and Salmonella was detected on 48% of
the food handlers’ hands. In conclusion, the suggestion of this study was that the food handlers
had adequate food safety knowledge, but perceived knowledge failed to be translated into practices
at work.
Keywords: food safety; food handler; KAP; microbiological assessment; hand hygiene
1. Introduction
The World Health Organization (WHO) reports that there approximately 2 million fatal cases of
food poisoning occur every year globally [1], especially in developing countries. This scenario could be
due to the poor state of food safety and general hygiene in those countries. In 2014, Malaysia recorded
49.79 cases of food poisoning per 100,000 population [2]. More than 50% of the total food poisoning cases
were attributed to improper food handling by food handlers [3]. The outbreaks in academic institutions
contributed 43% of the total foodborne poisoning incidents in Malaysia [4]. The Ministry of Health
Malaysia [5] has identified ineffective food handling training, the use of untreated water for non-drinking
purposes, and poor sanitation and hygiene as the primary risk factors of food poisoning in the country.
Food handlers play a paramount role in ensuring food safety and prevention of food poisoning.
Michaels and co-workers [6] reported that infected food handlers were able to transmit agents of
gastrointestinal infectious diseases via poor personal hygiene practices. A previous study successfully
isolated Salmonella from seafood [7] but Salmonella is not a common carrier. This was thought to be a
result of cross-contamination by infected food handlers [7]. Moreover, many reports have demonstrated
Int. J. Environ. Res. Public Health 2017, 14, 55; doi:10.3390/ijerph14010055 www.mdpi.com/journal/ijerph
Int. J. Environ. Res. Public Health 2017, 14, 55 2 of 14
similarities between the pathogens isolated from patients and food handlers, clearly indicating that
food handlers were the vehicles of transmission for the foodborne pathogens [8,9]. Angelillo et al. [10]
suggested that food handlers who had good knowledge of proper food handling practices could help
to control food poisoning cases as they were in direct contact with food, particularly ready-to-eat foods.
Poor personal hygiene, primarily ineffective hand washing, has been recognised as a significant
risk factor of food contamination that leads to food poisoning [11,12]. Hand hygiene is the most basic
yet critical criterion for ensuring safe food handling by food handlers. In fact, hand washing has long
been known to be a fundamental precautionary measures in health care settings [13], as well as in the
kitchen, for preventing the spread of infectious disease through human to human or human to food
contact [14–17]. Therefore, it is thought that hand hygiene could serve as an indicator of food handlers
adherence to safe food practices during food preparation.
In Malaysia, it is mandatory under the Food Act 1983 for all food handlers to attend and complete
the safe food handling course established by the Malaysian government, and they need to be vaccinated
against typhoid since this disease is endemic in Malaysia. Many local studies have reported that the
food handlers are mostly foreign contract workers who have adequate knowledge, positive attitudes,
and good self-reported practices [18–20]. Nevertheless, the food poisoning rates in this country have
still been increasing since 2000 [21]. The discrepancy observed between the previous research findings
and epidemiological statistics have motivated us to compare the real practice of hygiene to the knowledge,
attitude, and self-reported practices related to food hygiene and safety among food handlers.
Information on the food safety and hygiene practices of food handlers is scant. Thus, this study
focused on assessing the food safety knowledge, attitude, and self-reported practices among food
handlers via a questionnaire, in addition to hand hygiene assessment via microbiological assays.
By combining both approaches, the findings provided us with a better understanding of the extent
of translation of knowledge into real hygiene and safety practices as reflected in the hand hygiene of
food handlers. The data generated provides an important basis for planning and determination of
further approaches to be taken to improve food safety in the country.
Malaysia. The respondents were required to choose either “true” or “false” for each item on food safety
knowledge and the score was given for each correct answer. The overall performance on food safety
knowledge was converted to a percentage by dividing the total score over the total number of items of food
safety knowledge. While the food safety attitude and self-reported practices were assessed by four-level
and five-level Likert scale questions, respectively. For items under the attitude section, the lowest point
(1 point) was given to “disagree” to the highest (4 points) for “agree”; while the self-reported practices
were scored from the lowest (1 point) for “never” to the highest (5 points) for “always”.
We collected questionnaires from 67 food handlers of contract and/or permanent status from
twelve food premises within the campus from December 2013 to August 2014. The participation of
food handlers in this study was conducted on a voluntary basis. A self-administered questionnaire
adapted from previous studies [22,23] was given to the literate food handlers; whereas the illiterate
food handlers were assisted by a trained moderator in answering the questionnaire.
2.3.3. Detection and Enumeration of Salmonella spp., V. cholerae and V. parahaemolyticus Enumeration by
Polymerase Chain Reaction (PCR)
The Most Probable Number (MPN) three-tube method was applied to quantify Salmonella spp.,
V. cholerae and V. parahaemolyticus of the hands of food handlers. Buffered peptone water (Merck) was
used as the pre-enrichment broth Salmonella spp. whereas the alkaline peptone water (Merck) was
used as an enrichment medium for V. cholerae and parahaemolyticus. The MRD containing bacteria
from the hands of food handlers was diluted with enrichment medium and incubated overnight at
35 ± 2 ◦ C in 1.5 mL microcentrifuge tubes. The enriched samples were subjected to DNA extraction
and then Polymerase Chain Reaction (PCR) assay was used for Salmonella spp., Vibrio cholerae and
V. parahaemolyticus detection.
DNA templates were prepared using the boiling method. A pair of primers namely
OMPCF/OMPCR designed by Alvarez et al. [27], were used for Salmonella spp. detection while
Int. J. Environ. Res. Public Health 2017, 14, 55 4 of 14
primers named pntA 1C/2C and pntA 1P/2P were used [28] for V. cholerae and V. parahaemolyticus
detection. PCR products were analysed by using 1.5% of LE agarose (Promega, Madison, WI, USA) at
100 V for 30 min. All the oligonucleotides used were commercially synthesised (IDT, Coralville, IA,
USA). The laboratory culture collections in this study, Salmonella enterica subsp. serovar Enteritidis
(SE H16), Vibrio cholerae 86020, and Vibrio parahaemolyticus J 42 were used as the positive controls.
3. Results
Approximately 64.2% (n = 43) of the food handlers who undertook the questionnaire were aged
from 21 to 41 years old; while 61.2% (n = 41) were of foreign nationality. More than half of the
participants (n = 36, 53.7%) had ≥2 years’ experience in the food service industry (Table 1). Out of
67 food handlers involved in this study, a quarter (n = 17, 25.4%) of the food handlers had not attended
the safe food handling course, which is compulsory under the Malaysian Food Act 1983; and therefore,
most of these untrained food handlers were not vaccinated for typhoid fever either (Table 1).
The food handlers demonstrated moderate overall knowledge of food safety (mean score =
61.7 ± 8.1%). Of the six constructs on food safety knowledge tested, the respondents scored highest in
the construct of personal hygiene (mean score = 97.7 ± 11.4%) but performed poorly in the construct of
cross-contamination prevention and sanitation (mean score = 51.1 ± 15.0%) and foodborne pathogens
(mean score = 19.6 ± 25.1%; Figure 1). Based on the questionnaires, the participants showed an overall
good attitude, scoring an average of 51.9 ± 4.2 out of the total score of 57 (Table 2). Also, the participants
had reported that they frequently practised safe food handling during food preparation, scoring an
average of 53.2 ± 5.5 of the total score of 60 (Table 3).
Percentageofofthe
Figure1.1.Percentage
Figure thecorrect
correctanswers
answerson
onfood
foodsafety
safetyknowledge
knowledgescored
scoredby
by67
67food
foodhandlers.
handlers.
Int. J. Environ. Res. Public Health 2017, 14, 55 7 of 14
This study showed that the education level, working experience, and safe food handling course
had different degrees of impact on food safety knowledge and attitudes of food handlers (Table 4).
It is interesting to note that those who had not received any formal education performed better than
those who had received primary education. Nonetheless, it was found that those who had secondary
education and above scored significantly higher on food safety items related to food handling (p < 0.05;
Table 4); and only food handlers with tertiary education knew more about foodborne pathogens than
the rest (p < 0.05; Table 4). On the other hand, food handlers who had more working experience in
the food service industry had a better overall food safety knowledge (more than 6 years > 5–6 years
> 2–4 years ≥ 2 years, p < 0.05) than food handlers with lesser experience. From the questionnaire,
even though the safe food handling course did not significantly improve the food safety knowledge,
those who had attended the course performed slightly better than those who had not attended the
course (Table 4). Most importantly, the safe food handling course had a significant positive impact on
the attitudes toward food safety.
Ironically, the food handlers who had a non-compliant coliform count (≥20 CFU/cm2 ) claimed to
use gloves more frequently when touching or distributing unwrapped foods than those who had a
compliance count of coliform (Table 6). On the contrary, the food handlers who were detected with
the presence of Salmonella attested that they were less frequent in using caps while handling food
(4.2 ± 1.6, n = 24, p < 0.05) than those who had negative detection for in the presence of Salmonella.
Furthermore, the respondents who had of an exceeded limit of total aerobic bacteria (≥20 CFU/cm2 )
on their hands declared that they wash their hands before touching the unwrapped foods (4.7 ± 0.5,
n = 27, p < 0.05) more frequently. The food handlers who has coliform count exceeded the threshold
reported that they sanitise their working cloths more frequently (5.0 ± 0.0, n = 15, p < 0.05).
Int. J. Environ. Res. Public Health 2017, 14, 55 8 of 14
Table 4. Attribution of food safety knowledge, attitude, and self-reported scores to educational level, work experience, and safe food handling course of participants
(n = 67).
Did You Attend the Safe When Did You Attend the
Education Level Work Experience
Food Handling Course? Safe Food Handling Course?
Construct No Formal Primary Secondary Never ≤3 Years >3 Years
College/University ≤2 Years 2–4 Years 5–6 Years >6 Years No Yes
Education School School Attended Ago Ago
(n = 11) (n = 7) (n = 37) (n = 12) (n = 31) (n = 16) (n = 9) (n = 11) (n = 17) (n = 50) (n = 17) (n = 29) (n = 21)
Knowledge (%)
Personal hygiene 95.5 a 87.1 a 94.3 a 88.3 a 92.3 a 91.3 a 94.4 a 94.6 a 90.0 a 93.6 a 90.0 a 94.8 a 91.9 a
Cross contamination
49.2 a 60.7 a 49.8 a 53.5 a 50.5 a 53.1 a 50.9 a 52.3 a 48.0 a 52.7 a 48.0 a 53.5 a 51.6 a
prevention and sanitation
Food handling a,b 52.9 a b b,c a,b 61.3 a a,b b 73.5 a 70.4 a 73.5 a 68.3 a 73.3 a
66.4 75.1 74.2 73.2 66.7 83.6
Health problems that a a a a a a a a a a a a
62.7 54.3 69.2 68.3 61.9 63.1 73.3 78.2 72.9 64.2 72.9 60.0 70.0 a
would affect food safety
Symptoms of
78.8 a 66.7 a 66.1 a 75.9 a 66.7 a 72.2 a 70.4 a 75.8 a 66.0 a 71.3 a 66.0 a 68.6 a 75.1 a
foodborne diseases
a a,b a b a a a a a b a b
Foodborne pathogens 6.1 25.4 16.2 38.9 14.7 19.4 19.8 33.3 4.6 24.7 4.6 23.8 25.9 b
Overall knowledge score 60.0 a 58.3 a 62.1 a 66.4 a 60.2 a 60.3 a 62.8 a,b 69.5 b 59.6 a 63.0 a 59.6 a 61.7 a 64.7 a
Food safety attitude
Self-improvement 3.5 a,b 3.5 a,b 3.7 a 3.3 b 3.6 a 3.5 a 3.5 a 3.9 a 3.6 a 3.6 a 3.6 a 3.6 a 3.5 a
Food safety concern 3.5 a 3.6 a 3.4 a 3.5 a 3.4 a 3.5 a 3.5 a 3.4 a 3.1 a 3.5 b 3.1 a 3.5 b 3.5 b
Overall attitude score 3.5 a 3.6 a 3.5 a 3.4 a 3.4 a 3.5 a 3.5 a 3.6 a 3.3 a 3.5 b 3.3 a 3.6 b 3.5 a,b
Self-reported practices
Overall practices score 4.3 a 4.2 a 4.2 a 4.0 a 4.3 a 4.2 a 4.0 a 4.3 a 4.3 a 4.2 a 4.3 a 4.2 a 4.1 a
The values expressed in the column for the knowledge section are the mean percentage of each category in respect to each construct of KAP while the values expressed in the food
safety attitudes and self-reported practices are the mean score obtained from the questionnaire analysis. Values in the same row and subtable not sharing the same superscript (a , b , c )
are significantly different at p < 0.05 in the two-sided test of equality for column means. Cells with no superscript are not included in the test. Tests assume equal variances and are
adjusted for all pairwise comparisons within a row of each innermost subtable using the Bonferroni correction.
Int. J. Environ. Res. Public Health 2017, 14, 55 9 of 14
Hand hygiene assessment of the food handlers participating in this study revealed that 65%
(n = 55) of them had an aerobic bacterial count exceeding the threshold of ≥20 CFU/cm2 based on
Sneed et al. [26] and Tan et al. [24]. Approximately 35% (n = 30) had exceeded the standard coliform
count (≥10 CFU/cm2 ; Table 5). Moreover, Salmonella, V. cholerae and V. parahaemolyticus were detected
in 41 (48%), 2 (2%), and 1 (1%) of the 85 food handlers examined (Table 5). The number of Salmonella
present on the contaminated hands ranged from 3 to 150 MPN/hand (Table 5).
Table 5. Performance of participants’ hand hygiene based on aerobic bacteria, coliforms and E. coli,
S. aureus count and the detection of Salmonella, V. cholerae and V. parahaemolyticus.
Microbial Indicator Status Number Percentage (%) Min a (CFU/cm2 ) Max a (CFU/cm2 )
Aerobic count b
>Threshold 55 65 23 >29
<Threshold 30 35 <1 19
Coliform c
>Threshold 30 35 20 >29
<Threshold 55 65 <1 17
E. coli d
>Threshold 2 2 12 13
<Threshold 83 98 n.d. 8
S. aureus e
>Threshold 3 4 11 >29
<Threshold 82 96 n.d. 5
Foodborne Pathogens Presence Number Percentage (%) MPNmin per Person f MPNmax per Person f
Salmonella
Detected 41 48 3 150
Not detected 44 52 <3 n.a.
V. cholerae
Detected 2 2 3 n.a.
Not detected 83 98 <3 n.a.
V. parahaemolyticus
Detected 1 1 23 n.a.
Not detected 84 99 <3 n.a.
n.d.: Not detected or below detection limit; n.a.: Not applicable; MPN: Most probable number; a The minimum
(Min) and maximum (Max) CFU/ cm2 ; b Aerobic count threshold based on Tan et al. [25] and Sneed et al. [26],
which is ≥20 CFU/cm2 ; c Coliform count threshold based on Tan et al. [25] and Sneed et al. [26], which is
≥20 CFU/cm2 ; d E. coli count threshold based on Tan et al. [25] and Sneed et al. [26], which is ≥10 CFU/cm2 ;
e S. aureus count threshold based on Tan et al. [25] and Sneed et al. [26], which is ≥10 CFU/cm2 ; f The minimum
4. Discussion
In Malaysia, the food service industry has shown an increasing trend of hiring foreign labourers
to work as servants, stewards, and cooks to prepare foods. The actual number of foreign food workers
working in Malaysia is not known because most of them are working on a contract basis. The use
of contract workers in food premises has raised the public concern about food operations’ ability to
ensure food safety [29]. Our study reflected the scenario where there are more foreign food handlers
(61.2%) working in the food premises than the locals (Table 1). Other similar studies conducted in
another part of Malaysia have also reported the same scenario [19,20,29]. One of the main concerns of
having more foreign food handlers in Malaysia is the effectiveness of the safe food handling course
which is conducted in either Malay or English languages. The majority of the foreign food handlers
are from India, Pakistan, Nepal, and Cambodia and their command of English is low and therefore it
is presumed that the safe food handling course will be of little impact in instilling proper food safety
practices among the food handlers. However, our findings did not reflect such a scenario. Although
the improvement of knowledge performance was not significant between those who had attended the
course and those who had not, the safe food handling course showed a significant impact on instilling
positive food safety attitudes, particularly regarding food safety concerns among the respondents
who were predominantly foreigners (Table 4). Nonetheless, more detailed work is required to review
the effectiveness of the national safe food handling course, particularly regarding the foreign food
workers. An easy-to-understand module such as those based on illustrations could be more efficient in
delivering the knowledge to food handlers of different backgrounds and education levels.
Of the six constructs assessed on food safety knowledge, the food handlers who participated in
this study demonstrated good knowledge of personal hygiene (mean score: 97.7 ± 11.4%) but not on
cross-contamination (mean score: 51.1 ± 15.0%). Our finding was in agreement with other studies in
Malaysia [19]. We believe that this scenario is a reflection of the current safe food handling course
in Malaysia which focuses on the personal hygiene of food handlers while less emphasis is given to
prevention of cross-contamination. The food handlers demonstrated poor knowledge of foodborne
pathogens (19.6 ± 25.1%). This finding is supported by Liu et al. [30] Based on the study conducted
by Saad and co-workers [29] on hygiene practices among food handlers in governmental institutions
in Malaysia, about 30% of the food handlers commented that the safe food handling course failed to
improve their knowledge at work. However, our study suggested that the food safety handling course
could have significantly improved the awareness of food handlers, particularly regarding foodborne
pathogens (Table 4). Nevertheless, the findings indicated that the contents of the safe food handling
course need to be reviewed and improved.
The education level of food handlers is generally perceived as one of the factors that compromised
the food safety and hygiene. Although we have observed an improvement in the food safety knowledge
among those with tertiary education, food handlers with lower education levels, particularly those
who had no formal education outperformed those with higher education (Table 4). For instance, the
food handlers without formal education outperformed others on personal hygiene knowledge (Table 4).
These findings are further supported by the Pichler et al. [23], McIntyre et al. [31], Lynch et al. [32] and
Toh and Birchenough [33]. Working experience, on the other hand, was found to have a significant
impact on the overall food safety knowledge among the respondents in this study (Table 4). Saad and
co-workers [29] also reported a similar observation.
In this study, a microbial assessment to examine the hand hygiene of the participating food
handlers was conducted to obtain a better insight into the current food safety practices in food
premises. The microbiological hygiene assessment reflects the real practices of proper safe food
handling and at the same time could be used to validate the self-reported practices. The findings
from our study were not encouraging as many food handlers were found to have microbial counts
exceeding the standards (Table 5). More alarmingly, Salmonella was detected on the hands of about
half of the participated food handlers. These food handlers could be the asymptomatic carriers for
Salmonella transmission as Salmonella can remain in a carrier state up to 300 days after infection [34].
Int. J. Environ. Res. Public Health 2017, 14, 55 12 of 14
This raises many public health concerns, as most of the food handlers were not wearing gloves during
food handling, as we observed during the study. This situation could eventually increase the risk of
food poisoning.
Other studies have reported that provision of food safety and hygiene knowledge is not necessarily
translated into safe food behaviour or practice [10,35–37]. Similarly, our results indicated that the
generally moderate performance on food safety knowledge was not reflected in the microbial hand
hygiene assessment. For instance, the respondents who claimed that they often wore gloves had
coliform counts exceeding the threshold (Table 6). Our observation did not suggest that the food
handlers often wore gloves. This scenario could eventually increase the risk of coliform contamination
in foods. Overall, the findings suggested that the safe food handling course did, in fact, impart some
knowledge and awareness of food safety, but failed to change the safe food behaviour among the
food handlers. According to Worsfold et al. [38], behaviour change in safe food handling can be
attained when the knowledge and skills learned are being rehearsed and used. Continual training and
management support are important elements in the transfer of knowledge into behaviour [39]. In this
case, further studies are required to understand the factors that have limited the transfer of knowledge
into safe food practice among food handlers.
5. Conclusions
Although the food handlers had a moderate level of food safety knowledge with a good attitude,
and self-reported practices, the poor performance in the hand hygiene assessment indicated a failure
in actually practising safe food handling in their job. The contaminated hands of food handlers could
easily transmit foodborne diseases through cross-contamination of food products. The current findings
indicated a need to review the effectiveness of the current national safe food handling course, not just
to improve the effectiveness to disseminate food safety knowledge and attitudes, but also to induce
a real change in safe food handling behavior among food handlers by taking into consideration the
multi-cultural and education level of food handlers in Malaysia. It is apparent from this study that a
good knowledge in food safety is not indicative of food safety practice in the real world. Studies are
required to look into the factors that inhibit the transfer of knowledge into food safety behaviour in
Malaysia so that an effective food safety policy can be put in place.
There are several limitations in this research. These results only relied on the very limited number
of food handlers who took part in this study and therefore the observation or findings in the study
should not be extrapolated to represent the scenario in Malaysia. However, this study is exploratory in
nature and serves as a pilot study for a nationwide study of the relationship between hand sanitation
and the KAP of food handlers. Future studies should involve a collaboration with the government
and a larger population of food handlers so that the authority can establish a more comprehensive
approach to ensure food safety.
Acknowledgments: This study was fully funded by University Malaya Research Grant (RP003C-13BIO and
RP003A-13BIO). Hui Key Lee was supported by MOHE MyBrain scholarship. We thank Siti Sofea and Siti Azwani
for the assistance in collecting samples and questionnaires.
Author Contributions: Hui Key Lee performed the experiments, analysed data and drafted the manuscript.
Hishamuddin Abdul Halim involved in experimental design. Kwai Lin Thong provided the research instruments
and edited the manuscript. Lay Ching Chai designed the experiments, contributed the research materials,
cross checked the analysed data and edited manuscript.
Conflicts of Interest: The authors declare no conflict of interest.
References
1. World Health Organization (WHO). Food Safety; WHO: Geneva, Switzerland, 2015. Available online:
http://www.who.int/mediacentre/factsheets/fs399/en/ (accessed on 19 October 2016).
2. Ministry of Health (MOH). Health Facts 2014; MOH: Putrajaya, Malaysia, 2014.
3. Ministry of Health (MOH). Annual Report 2007; MOH: Putrajaya, Malaysia, 2007.
Int. J. Environ. Res. Public Health 2017, 14, 55 13 of 14
4. Ministry of Health (MOH). The National Level 2014 Clean, Safe and Healthy Canteen Award; Department of
Food Safety and Food Quality, Ed.; MOH: Putrajaya, Malaysia, 2014.
5. Ministry of Health (MOH). Annual Report 2010; MOH: Putrajaya, Malaysia, 2012.
6. Michaels, B.; Keller, C.; Belvins, M.; Paoli, G.; Ruthman, T.; Todd, E.; Griffith, C.J. Prevention of food worker
transmission of foodborne pathogens: Risk assessment and evaluation of effective hygiene intervention
strategies. Food Serv. Technol. 2004, 4, 31–49. [CrossRef]
7. Lunestad, B.T.; Borlaug, K. Persistence of Salmonella enterica serovar agona in oil or fish feed production.
J. Aquacult. Feed Sci. Nutr. 2009, 1, 73–77.
8. Olsen, S.J.; Hansen, G.R.; Bartlett, L.; Fitzgerald, L.; Sonder, A.; Manjrekar, R.; Riggs, T.; Kim, J.; Flahart, R.;
Pezzin, G.; et al. An outbreak of Campylobacter jejuni infection associated with food handler contamination;
the use of pulsed-field gel electrophoresis. J. Infect. Dis. 2001, 183, 164–167. [CrossRef] [PubMed]
9. Quiroz, E.S.; Bern, C.; MacArthur, J.R.; Xiao, L.; Fletcher, M.; Arrowood, M.J.; Shay, D.K.; Levy, M.E.;
Glass, R.I.; Lal, A. An outbreak of cryptosporidiosis linked to a food handler. J. Infect. Dis. 2000, 181, 695–700.
[CrossRef] [PubMed]
10. Angelillo, I.F.; Viggiani, N.M.; Rizzo, L.; Bianco, A. Food handlers and foodborne diseases: Knowledge,
attitudes, and reported behavior in Italy. J. Food Prot. 2000, 63, 381–385. [CrossRef] [PubMed]
11. Scarborough, M.F. Hand Washing in Georgia’s Public Schools—A Community Needs Assessment and
Intervention Study. Master’s Thesis, Emory University, Atlanta, GA, USA, May 2002.
12. Curtis, V.; Cairncross, S. Effect of washing hands with soap on diarrhea risk in the community: A systemic
review. Lancet Infect. Dis. 2003, 3, 275–281. [CrossRef]
13. World Health Organization. World Health Organization. Evidence of hand hygiene to reduce transmission
and infections by multidrug resistant organisms in health-care settings. In WHO Guidelines on Hand Hygiene
in Health Care; Clean Care is Safer Care Team, Ed.; WHO: Geneva, Switzerland, 2009.
14. Gibson, L.L.; Rose, J.B.; Haas, C.N.; Gerba, C.P.; Rusin, P.A. Quantitative assessment of risk reduction from
hand washing with antibacterial soaps. J. Appl. Microbiol. 2002, 92 (Suppl. S1), 136S–143S. [CrossRef]
[PubMed]
15. Chinakwe, E.C.; Nwogwugwu, N.U.; Nwachukwu, I.N.; Okorondu, S.I.; Onyemekara, N.N.;
Ndubuisi-Nnaji, U.U. Microbial quality and public health implications of hand-wash water samples of
public adults in Owerri, South-east Nigeria. Int. Res. J. Microbiol. 2013, 3, 144–146.
16. Soares, L.S.; Almeida, R.C.C.; Cerqueira, E.S.; Carvalho, J.S.; Nunes, I.L. Knowledge, attitudes and practices
in food safety and the presence of coagulase-positive staphylococci on hands of food handlers in the schools
of Camaçari, Brazil. Food Control 2012, 27, 206–213. [CrossRef]
17. Perez-Rodriguez, F.; Valero, A.; Carrasco, E.; Garcia, R.M.; Zurera, G. Understanding and modelling bacterial
transfer to foods: A review. Trends Food Sci. Technol. 2008, 19, 131–144. [CrossRef]
18. Noor-Azira, A.-M.; Mohammad-Faid, A.-R.; Shuhaimi, M.; Syafinaz, A.-N.; Hamat, A.H.R.A.; Malina, O.
Knowledge, attitude and practices regarding food hygiene and sanitation of food handlers in Kuala Pilah,
Malaysia. Food Control 2012, 27, 289–293.
19. Norrakiah, A.S.; Siow, O.N. Knowledge, attitudes and practices of food handlers on food safety in food
service operations at the Universiti Kebangsaan Malaysia. Food Control 2014, 37, 210–217.
20. Rosnani, A.H.; Son, R.; Mohhidin, O.; Toh, P.S.; Chai, L.C. Assessment of knowledge, attitude and practices
concerning food safety among restaurant workers in Putrajaya, Malaysia. Food Sci. Qual. Manag. 2014, 32,
20–27.
21. Ministry of Health (MOH). Health Facts 2013; MOH: Putrajaya, Malaysia, 2013. Available online: http://vlib.moh.
gov.my/cms/content.jsp?id=com.tms.cms.section.Section_3549ea8f-c0a81049-874bd300-302e756b (accessed on
3 May 2015).
22. Osaili, T.M.; Jamous, D.O.A.; Obeidat, B.A.; Bawadi, H.A.; Tayyem, R.F. Food safety knowledge among food
workers in restaurants in Jordan. Food Control 2013, 31, 145–150. [CrossRef]
23. Pichler, J.; Ziegler, J.; Aldrian, U.; Allerberger, F. Evaluating levels of knowledge on food safety among food
handlers from restaurants and various catering businesses in Vienna, Austria 2011/2012. Food Control 2014,
35, 33–40. [CrossRef]
24. Lee, J.Y.; Choi, J.W.; Kim, H. Determination of hand surface area by sex and body shape using alginate.
J. Physiol. Anthropol. 2007, 26, 475–483. [CrossRef] [PubMed]
Int. J. Environ. Res. Public Health 2017, 14, 55 14 of 14
25. Tan, S.L.; Lee, H.Y.; Abu Bakar, F.; Abdul Karim, M.S.; Rukayadi, Y.; Mahyudin, N.A. Microbiological quality
on food handlers’ hands at primary schools in Hulu Langat district, Malaysia. Int. Food Res. J. 2013, 20,
2973–2977.
26. Sneed, J.; Strohbehn, C.; Gilmore, S.A.; Mendonca, A. Microbiological evaluation of foodservice contact
surfaces in Iowa assisted-living facilities. J. Am. Diet. Assoc. 2004, 104, 1722–1724. [CrossRef] [PubMed]
27. Alvarez, J.; Sota, M.; Vivanco, A.; Perales, I.; Cisterna, R.; Rementeria, A.; Garaizar, J. Development of a
multiplex PCR technique for detection and epidemiological typing of Salmonella in human clinical samples.
J. Clin. Microbiol. 2004, 42, 1734–1738. [CrossRef]
28. Teh, C.S.J.; Chua, K.H.; Thong, K.L. Simultaneous differential detection of human pathogenic and
non-pathogenic Vibrio species using a multiplex PCR based on gyrB and pntA genes. J. Appl. Microbiol. 2010,
108, 1940–1945. [PubMed]
29. Saad, M.; Toh, P.S.; Adil, M.A.M. Hygiene practices of food handlers at Malaysian government institutions
training centers. Procedia Soc. Behav. Sci. 2013, 85, 118–127. [CrossRef]
30. Liu, S.; Liu, Z.; Zhang, H.; Lu, L.; Liang, J.; Huang, Q. Knowledge, attitude and practices of food safety
amongst food handlers in the coastal resort of Guangdong, China. Food Control 2015, 47, 457–461. [CrossRef]
31. McIntyre, L.; Vallaster, L.; Wilcott, L.; Henderson, S.; Kosatsky, T. Evaluation of food safety knowledge,
attitudes and self-reported hand washing practices in foodsafe trained and untrained food handlers in
British Columbia, Canada. Food Control 2013, 30, 150–156. [CrossRef]
32. Lynch, R.A.; Elledge, B.L.; Griffith, C.C.; Boatright, D.T. A comparison of food safety knowledge
among restaurant managers, by source of training and experience, in Oklahoma County, Oklahoma.
J. Environ. Health 2003, 66, 9–14. [PubMed]
33. Toh, P.S.; Birchenough, A. Food safety knowledge and attitudes: Culture and environment impact on
hawkers in Malaysia. Knowledge and attitudes are key attributes of concern in hawker food handling
practices and outbreaks of food poisoning and their prevention. Food Control 2000, 11, 447–452. [CrossRef]
34. Todd, E.C.; Greig, J.D.; Batleson, C.A.; Michaels, B.S. Outbreaks where food workers have been implicated
in the spread of foodborne disease. Part 3. Factors contributing to outbreaks and description of outbreak
categories. J. Food Prot. 2007, 70, 2199–2217. [CrossRef] [PubMed]
35. Ackerley, L. Consumer awareness of food hygiene and food poisoning. Environ. Health 1994, 102, 69–74.
36. Curtis, V.; Cousens, S.; Mentens, T.; Kenki, B.; Diallo, I. Structured observations of hygiene behaviours in
Burkira Faso: Validity, variability and utility. Bull. World Health Organ. 1993, 71, 23–32. [PubMed]
37. Pinfold, J.V. Analysis of different communication channels for promoting hygiene behavior. Health Educ. Res.
1999, 14, 629–639. [CrossRef] [PubMed]
38. Worsfold, D.; Griffth, C.; Worsfold, P. A survey of environmental health officers’ views of food hygiene
training. Br. Food J. 2004, 106, 51–64. [CrossRef]
39. Seaman, P.; Eves, A. Perceptions of hygiene training amongst food handlers, managers and training
providers—A qualitative study. Food Control 2010, 21, 1037–1041. [CrossRef]
© 2017 by the authors; licensee MDPI, Basel, Switzerland. This article is an open access
article distributed under the terms and conditions of the Creative Commons Attribution
(CC-BY) license (http://creativecommons.org/licenses/by/4.0/).