Outbreak Investigation Report

Outbreak of foodborne disease in a

boarding school, Negeri Sembilan state,
Malaysia, 2021
Nur Nadiatul Asyikin Bujang,a,b Mohd Shahrol Abd Wahil,c Siti Aishah Abas,a,d Khairul Hafidz Alkhair Khairul Amin,a,e
Nadiatul Ima Zulkifli,a Sharina Mohd Shah,a Nurul Fazilah Aziz,a Syuaib Aiman Amir Kamarudin,a Veshny Ganesan,a
Nur Azieanie Zainuddin,a Muhamad Hazizi Muhamad Hasani,a Noor Khalili Mohd Alia and Mohamad Paid Yusofa
Correspondence to Nur Nadiatul Asyikin Bujang (email: nadiatulasyikin@gmail.com)

Objective: Foodborne disease is a significant global public health concern, with Bacillus cereus being a frequent cause of
outbreaks. However, due to the relatively mild symptoms caused by infection with B. cereus, the shorter duration of illness
and the challenges of testing for it in both stool and food samples, outbreaks are often underreported. This report describes
the epidemiology of cases of foodborne illness, the causative agent and risk factors associated with an outbreak in a boarding
school in Seremban district, Negeri Sembilan state, Malaysia, that occurred in November 2021.
Methods: Epidemiological, environmental and laboratory investigations were performed. A case was defined as any person
with abdominal pain, vomiting or diarrhoea that occurred after consuming food served by the canteen at the school. The data
were analysed using Microsoft Excel and the Statistical Package for the Social Sciences (SPSS).
Results: A total of 152 cases were identified among the 597 students, giving an attack rate of 25.5%. All cases were
females aged 13–17 years. They presented with abdominal pain (100%), nausea (97.4%, 148), vomiting (78.3%, 119)
or diarrhoea (61.8%, 94), or a combination of these. The mode of transmission of the outbreak was a continual common
source. The foods associated with becoming a case were beef rendang (a dry curry) (odds ratio [OR]: 20.54, 95% CI: 4.89–
86.30), rice (OR: 19.62, 95% CI: 2.62–147.01), rice cubes (OR: 18.17, 95% CI: 4.31–76.55) and vermicelli (OR: 17.02,
95% CI: 4.03–71.86). Cross-contamination and inadequate thawing and storage temperatures contributed to the outbreak.
Discussion: This outbreak of foodborne illness at a boarding school was likely caused by B. cereus. The findings highlight
the importance of proper food preparation, temperature monitoring, hygiene practices among food handlers and compliance
with food safety guidelines.

F
oodborne diseases continue to be a public health by 4 (22.2%) at primary schools and 3 (16.7%) at
concern globally, contributing to morbidity and colleges.3
mortality, and associated with substantial economic
costs.1 During the past decade, the national annual Food poisoning associated with Bacillus cereus
incidence of foodborne diseases in Malaysia has been causes diarrhoea or vomiting,4 which is generally mild
decreasing, with the incidence reported as 50.1/100 000 and self-limiting. Emetic syndrome develops upon in-
population in 2019.2 Data from e-Wabak, the gesting the preformed toxin in contaminated foods such
communicable disease monitoring system run by the as rice or rice products.4,5 Diarrhoeal syndrome, com-
Ministry of Health in Malaysia, reported 46 outbreaks of monly associated with contaminated fish, vegetables
foodborne disease in Seremban district, Negeri Sembilan or meat, is caused by heat-labile toxins, which have a
state, between 2017 and 2021, with 18 (39.1%) longer incubation period.5,6 The incubation period for the
involving educational institutions. Eleven (61.1%) of emetic syndrome is 0.5 to 6 hours, and for diarrhoeal
these outbreaks occurred at secondary schools, followed syndrome it ranges from 8 to 16 hours.7 B. cereus can

a
Seremban District Health Office, Ministry of Health, Seremban, Negeri Sembilan, Malaysia.
b
Department of Social and Preventive Medicine, Faculty of Medicine, Universiti Malaya, Kuala Lumpur, Malaysia.
c
Disease Control Division, Ministry of Health, Putrajaya, Malaysia.
d
Department of Public Health and Population Medicine, Faculty of Medicine, Universiti Teknologi MARA, Shah Alam, Selangor, Malaysia.
e
Department of Community Health, Faculty of Medicine and Health Sciences, Universiti Putra Malaysia, Serdang, Selangor, Malaysia.
Published: 30 September 2023
doi: 10.5365/wpsar.2023.14.3.1043

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Bacillus cereus outbreak in Seremban, Malaysia Bujang et al

withstand unfavourable conditions8 and survives cook- using convenience sampling. The control group was
ing processes, forming spores that can multiply and defined as those who consumed the same food but did
produce toxins in cooked rice.9 not experience any symptoms.

On 22 November 2021, the Seremban District The attack rate of all students was determined,
Health Office was notified by a local hospital about and the odds ratio (OR) was calculated for all reported
cases of food poisoning occurring among boarding food exposures. P values were calculated using Fisher’s
school students. The outbreak was confirmed by the exact test, with statistical significance defined as
rapid assessment team, consisting of doctors and P<0.05. The data were verified by cross-checking with
environmental health assistant officers. The aim of health-care facility and school records. Then the data
this report is to describe the epidemiology of the were transformed into a line list using Microsoft Excel
outbreak, the steps taken to determine the causative (2021). All data were collected in hardcopy form and
pathogen and the contaminated foods and risk fac- kept confidential in locked storage by the Seremban
tors, and highlight recommendations to prevent future District Health Office. Data were analysed using the
outbreaks. IBM Statistical Package for the Social Sciences (SPSS)
version 26 (Chicago, IL, USA).
METHODS
Laboratory investigation
Outbreak location
Samples were collected for testing on 22 November 2021.
The outbreak occurred in a secondary-level boarding Proxy food samples, hand swabs from food handlers
school attended by 597 female students in Seremban and swabs from kitchen utensils were tested by culture
district, Negeri Sembilan state, an urban area in and sensitivity for B. cereus, Escherichia coli, coliform
Malaysia. bacteria, Salmonella species and Staphylococcus aureus.
Rectal swabs from patients and food handlers were tested
Epidemiological investigation for enteric pathogens by culture and for sensitivity. Test
results were obtained from the Public Health Laboratory
A case was defined as any person who developed Information System.
abdominal pain, vomiting or diarrhoea after consuming
any food or drinks at the boarding school canteen from Environmental investigation
19 November 2021 at 06:30 to 21 November 2021
at 22:00. Active case-finding was conducted through An environmental investigation was conducted to assess
face-to-face interviews, guided by a standardized Min- the physical environment by examining factors such as
istry of Health food poisoning questionnaire. Data were the water source, food storage areas, sanitation practices,
gathered about the sociodemographic characteristics of ventilation systems and other possible sources of con-
the cases, their symptoms, time of symptom onset and tamination. The food preparation process was assessed
food consumption history. Records from government and using Hazard Analysis Critical Control Point standards.
private health-care facilities were reviewed to identify Food handlers were questioned about their typhoid vac-
similar cases that may have been linked to the outbreak cination status and their attendance at food handling
of foodborne illness through formal requests made to the courses, as guided by the Ministry of Health’s risk-based
relevant authorities. food premises inspection form, amendment 2018.

An unmatched case–control study was conducted RESULTS

due to the challenges of recruiting participants during
the coronavirus disease (COVID-19) pandemic and of Epidemiological investigation
conducting a field study. Individuals were eligible for
inclusion if they had been exposed to the food prepared A total of 152 cases were identified among the 597 stu-
and served by the boarding school canteen during dents who lived at the boarding school, giving an attack
19 to 21 November 2021. Participants were recruited rate of 25.5%. For the case–control study, there were

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Bujang et al Bacillus cereus outbreak in Seremban, Malaysia

152 cases and 200 controls, for a ratio of 1:1.3. All cases and had received typhoid vaccinations and attended
were female and aged 13–17 years. They presented with food safety training.
abdominal pain (100%), nausea (97.4%, 148), vomiting
(78.3%, 119) or diarrhoea (61.8%, 94), or a combination Laboratory investigation
of these. All cases were treated as outpatients and none
died. The samples collected included five proxy foods (stir fry
macaroni, white bread, fried chicken, soto vermicelli and
The epidemic curve suggests an outbreak with chocolate cake), one sample of boiled water, 24 rectal
a continual source, as indicated by the multiple peaks swabs from 17 cases and seven food handlers, seven
(Fig. 1), with a suggested first exposure at breakfast on swabs from food preparers’ hands, seven environmental
20 November 2021. The epidemic curve also suggests samples and 15 water samples from drinking-water
that there was ongoing exposure because the onset dispensers at the school. The laboratory investigation
of symptoms for the first case was on 20 November yielded B. cereus (<4000 colony forming units [CFU]/g)
2021 at 16:00, and the onset for the last case was on from the hand swab of one food preparer (staff member A)
22 November 2021 at 07:30. who worked the morning shifts on 20 and 21 November.
Samples from two chopping boards also yielded
The food served by the canteen operator during B. cereus and E. coli (Table 2). The proxy food samples
20 and 21 November 2021 with the highest ORs included and the rice-scooping spoon yielded coliforms (Table 2).
beef rendang and rice cubes, served during breakfast on
20 November (OR: 20.54, 95% CI: 4.89–86.30 for the Outbreak control measures
beef rendang; OR: 19.62, 95% CI: 2.62–147.01 for the
rice cubes); white rice served during lunch (OR: 9.64, Following the outbreak, all activities at the canteen were
95% CI: 4.32–76.55); white rice and chicken curry temporarily suspended in accordance with Malaysia’s
served during dinner on the same day (OR: 19.62, 95% Infectious Disease Control Act 1988. This allowed the
CI: 2.62–147.01); and vermicelli and spicy soy sauce kitchen operator to take necessary measures to ensure
served during breakfast on 21 November (OR: 17.02, compliance with food and hygiene regulations before
95% CI: 4.03–71.86) (Table 1). Leftover food was not resuming operations. Food handlers were reminded to
consumed by students or staff. monitor temperatures closely, while the district health
educator delivered talks to the food handlers and stu-
Environmental investigation dents as well as distributed informational pamphlets to
students and teachers. To prevent future outbreaks, it is
The assessment of food processing showed a important to emphasize how to handle food safely and
temperature monitoring violation, as there was no to educate food handlers, school administrators and stu-
temperature monitoring when raw food was received or dents about food safety as well. A subsequent inspection
during its storage in the chiller and freezer. The beef was done to ensure that all necessary actions had been
was defrosted for less than 1 hour. The beef was boiled taken promptly.
in 40-kg quantities in a cauldron without temperature
monitoring for 20 minutes, which may have contributed DISCUSSION
to uneven and insufficient heating. The rice was washed
before cooking and was cooked in a large pot, with Investigating outbreaks of foodborne illnesses enables
approximately 5 kg rice per pot. It was cooked fresh for possible sources of infection to be identified. This
each meal and was not served again. outbreak was most likely caused by B. cereus cross-
contamination and poor temperature monitoring. In this
During inspection of the premises, flies were outbreak, there were cases with emetic and diarrhoeal
noted in the kitchen due to non-functioning fly traps. symptoms, suggesting a mixed source of B. cereus.5
Hand-washing stations were not equipped with soap.
Otherwise, the overall cleanliness of the premises was The longer incubation periods observed and the
rated at 96.6%. All 14 food handlers were asymptomatic continual common source pattern evidenced by the

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Bacillus cereus outbreak in Seremban, Malaysia Bujang et al

Fig. 1. Epidemic curve of an outbreak of foodborne illness in a boarding school canteen, by date and time of
symptom onset, Seremban district, Negeri Sembilan state, Malaysia, 20–22 November 2021

Table 1. Case–control analysis of an outbreak of foodborne illness in a boarding school canteen, Seremban district,
Negeri Sembilan state, Malaysia, 20–22 November 2021a
Cases (n = 152) Controls (n = 200)
Type of food Odds ratio (95% CI) P
Exposed Not exposed Total Exposed Not exposed Total
20 November 2021 – Breakfast, 06:30 to 07:30
Rice cubesb 150 2 152 161 39 200 18.17 (4.31–76.55) < 0.001
Beef rendang c
150 2 152 157 43 200 20.54 (4.89–86.30) < 0.001
Peanut gravy 148 4 152 140 60 200 15.86 (5.61–44.78) < 0.05
Malted chocolate drink 147 5 152 129 71 200 16.18 (6.34–41.31) < 0.05
20 November 2021 – Lunch, 12:30 to 13:30
White rice 151 1 152 188 12 200 9.64 (1.24–74.96) < 0.05
Fried spicy stuffed
151 1 152 187 13 200 10.50 (1.36–81.16) < 0.05
torpedo scad
Turmeric fried prawns 150 2 152 181 19 200 7.87 (1.80–34.35) < 0.05
Cabbage cooked in coconut
150 2 152 179 21 200 8.80 (2.03–38.14) < 0.05
broth
20 November 2021 – Dinner, 18:00 to 19:00
White rice 151 1 152 177 23 200 19.62 (2.62–147.01) < 0.05
Chicken curry 151 1 152 177 23 200 19.62 (2.62–147.01) < 0.05
Stir fry vegetables 149 2 152 170 30 200 13.15 (3.09–55.95) < 0.05
Red apple 146 6 152 170 30 200 4.29 (1.74–10.60) < 0.05
Plain water 150 2 152 170 30 200 13.24 (3.11–56.32) < 0.05
21 November 2021 – Breakfast, 06:30 to 07:30
Vermicelli 150 2 152 163 37 200 17.02 (4.03–71.86) < 0.05
Spicy soy sauce 150 2 152 163 37 200 17.02 (4.03–71.86) < 0.05
Malted drinks 147 5 152 150 50 200 9.8 (3.80–25.27) < 0.05

CI: confidence interval.

a
Foods in bold are suspected to have been associated with the outbreak.
b
Rice cubes are compacted rice that is boiled and subsequently cut into small cubes.
c
Beef rendang is a dry curry that is prepared using coconut milk and spices.

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Bujang et al Bacillus cereus outbreak in Seremban, Malaysia

Table 2. Laboratory results from an outbreak of foodborne illness in a boarding school canteen, Seremban
district, Negeri Sembilan state, Malaysia, from samples collected on 22 November 2021
No. of Test result
Type of specimen Test and method Organism identified
samples Positive Negative
Samples from cases and food handlers
Hand swabs Bacillus cereus (<4000
7 1 6
(food handler) CFU/g) from staff member A
Culture and sensitivity for enteric pathogens
Rectal swabs (food
24 0 24 –
handlers and cases)
Samples from food and water
Stir fry macaroni 1 1 0 Coliform (1300 CFU/g)
B. cereus (ISO 7932:2004 [E])a
White bread 1 1 0 Coliform (30 000 CFU/g)
Escherichia coli (AOAC 991.14)
Fried chicken Coliform (AOAC 991.14) 1 0 1 –
Salmonella species (ISO 6579-1:2017 [E])
Soto vermicelli b
1 0 1 –
Staphylococcus aureus (AOAC 2003.07-2006)
Chocolate cake 1 0 1 –
Water (from drinking-water
1 0 1 –
dispenser)
Coagulase-positive Staphylococci
Drinking-water dispenser (ISO 6888-1:1999/ Amd.1.2003 [E]) 1 0 1 –
Filtered water dispenser 1 0 1 –
Samples from kitchen utensils
B. cereus (<4000 CFU/g)
Cutting board (sample 1) E. coli (700 CFU/g)
Coliform (350 000 CFU/g)
B. cereus (<4000 CFU/g)
Cutting board (sample 2) B. cereus (ISO 7932:2004 [E]) 1 1 0 E. coli (100 CFU/g)
E. coli (AOAC 991.14) Coliform (34 000 CFU/g)
Coliform (AOAC 991.14)
Rice spoon S. aureus (AOAC 2003.07-2006) 1 1 0 Coliform (6500 CFU/g)
Ladle 1 0 1 –
Tip of water bottle 1 0 1 –
Pan surface 1 0 1 –

AOAC: Association of Official Analytical Collaboration International; CFU: colony forming units; ISO: International Organization for Standardization; –: indicates no findings.
a
The letter E after an ISO standard indicates that it was published in English.
b
Soto vermicelli is a plain soup eaten with vermicelli noodles.

epidemiological curve, characterized by a gradual rise in allow B. cereus to survive the cooking process and con-
the number of cases and numerous peaks over time, can tinue multiplying,10 which could explain the high OR for
be explained by multiple contamination incidents occur- beef rendang. Multiple factors commonly contribute to
ring over 2 days. The food could have been continually outbreaks of foodborne illness, especially those related to
contaminated by staff member A, kitchen equipment or improper storage (i.e. refrigeration) and failure to maintain
contaminated food. The self-service buffet style of food proper temperatures.11 Other sauce-based dishes, such
service during which students have their meals in groups as chicken curry and spicy soy sauce, also had a high OR
in the dining hall may also have contributed to this type of since they were served with rice. Rice was often served
epidemiological curve and could have facilitated possible for breakfast, lunch and dinner on the dates around the
contamination by students. outbreak occurrence, so it is possible that rice was also
responsible for this outbreak.
The ORs associated with the food should be inter-
preted with caution due to the wide confidence intervals, Despite swabbing workers’ hands and kitchen equip-
which make it difficult to determine which foods were ment, only low numbers of CFUs were found; however,
most strongly associated with illness. However, not the positivity still indicates contamination since low num-
monitoring the temperature of the raw meat could also bers of B. cereus have caused outbreaks.12 To improve

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Bacillus cereus outbreak in Seremban, Malaysia Bujang et al

the efficacy of hand-washing and reduce the number of Conflicts of interest

B. cereus spores, soap should be used and hands should
be washed for at least 20 seconds.13,14 Drying hands The authors have no conflicts of interest to declare.
with disposable towels instead of cloth towels can also
reduce the risk of cross-contamination.15 The presence Ethics statement
of E. coli and coliforms suggests poor hygiene practices.
Ethical approval was obtained from the Medical Research
The study has limitations that make it difficult to and Ethics Committee, Ministry of Health, Malaysia (no.
definitively confirm that B. cereus caused the outbreak. NMRR-22-00798-WMX).
None of the food items from the days on which con-
tamination likely occurred were available for testing; Funding
instead, proxy food samples were used. When tested,
these proxy samples were negative for B. cereus toxins. None.
In terms of the statistical analyses, multivariable analysis
was not performed, and the assessment of potentially References
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