E. Coli-caused Foodborne Outbreak in Bantul Regency, Indonesia, 2023: A Retrospective Cohort Study

1. INTRODUCTION

Foodborne diseases remain a major public health concern worldwide [1]. In both developed and developing nations, foodborne diseases contribute to the primary cause of morbidity and mortality [2]. The two contributing factors include the general population's greater susceptibility [e.g., the elderly or the immunocompromised], which leads to more serious illness outcomes, and the spread of antibiotic resistance [3]. Another essential aspect is the globalization of food supply chains, which results in large-scale food distribution and the potential for disease transmission. Foodborne infections are also significantly impacted by changes in the virulence of recognized pathogens, new consumption habits, and population movements [4]. Foodborne pathogenic bacteria contamination in food systems is a severe concern that can result in the development of various diseases and even mortality. The World Health Organization estimates that the consumption of unsafe food globally results in the loss of at least 33 million years of healthy life each year [5].

A foodborne disease outbreak happens when two or more people become sick after consuming food that has been epidemiologically confirmed as a source of infection [6]. Food toxicity is caused by the presence of bacterial toxins, which are produced when bacteria proliferate in food. In contrast, food infection occurs when bacteria enter the body via contaminated food, triggering the body's immune response. Both factors can lead to gastrointestinal disease. E. coliand Salmonellaare among the most common bacteria responsible for foodborne illnesses [7].

Escherichia coli [E. coli] is a common bacterium found in the human intestines that does not typically cause harm to health [8]. Few strains of E. coli acquire virulence genes through horizontal transfer and cause gastroenteritis. Diarrheagenic Escherichia coli [DEC] is the primary cause of acute gastroenteritis in children. However, until now, DEC-related epidemiology information islimited [9].

In Indonesia, according to the SPIMKER [Sistem Pelaporan Informasi Masyarakat Keracunan] application, the Indonesian Food and Drug Authority [BPOM] reported 122 foodborne outbreaks in 2023. Of the 8,937 individuals who were reported, 4,729 experienced illness, resulting in an attack rate of 52.91%. The case fatality rate was 0.38%, with 18 deaths. From 2019 to 2021, the attack rate increased and then declined in 2022 [45.29% in 2019, 46.62% in 2020, 69.40% in 2021, and 50.64% in 2022]. However, the attack rate increased in 2023 compared to 2022 [10].

Based on the fooddistribution, foodborne outbreaks in 2023 occurred in 29 provinces, with West Java reporting the highest [16.11%], followed by Central Java with 14 cases [11.48%]. Microbiological contamination wasthe most frequent cause of 68 cases, of which 42 [34.43%] were suspected and 26 [21.31%] were confirmed. The outbreaks were caused by pathogens, such asSalmonella, Escherichia coli, Clostridium perfringens, Bacillus cereus, Staphylococcus aureus, and Bacillus cereus. In addition, there were 19 food poisoning outbreaks caused by chemicals, with 13 [10.66%] suspected and 6 [4.92%] confirmed, involvinghistamine, cyanide, arsenic, and lead [Pb]. The remaining 35 cases [28.69%] had unknown causes. Foodborne outbreaks were linked to food produced by households, catering services, snacks, MD food, ML food, and Home Industry Food (PIRT). Over the past five years, home-cooked food has been the leading source of foodborne outbreaks, accounting for 53.28% in 2023, 34.72% in 2022, 52% in 2021, 49% in 2020, and 40.30% in 2019 [10].

On October 18, 2023, the Pleret Public Health Center (PHC) notified the Bantul District Health Office about several employees experiencing diarrhea and stomach aches. The initial assumption was that this incident occurred after they consumed fried chicken served by one of the workers on October 16, 2023.Based on this information, the investigative team conducted an epidemiological investigation and collected food samples, specifically fried chicken, which was suspected to be the source of the foodpoisoning. An e-questionnaire was distributed to all PHC employees to continue tracking disease cases.

In this view, this investigation aims to establish a working case definitionand verify the existence of an outbreak. This assessment must be initiated and completed immediately to avoid further illness. The process should include verifying the validity of the information, collecting data from relevant laboratory examinations conducted, identifying cases and collectingdetails about them, and ensuring the collection of proper clinical specimens and food samples [6].

2. METHODOLOGY

3. RESULTS

3.2. Incubation Period

Based on the epidemic curve [Fig. 2], this outbreak followed a common source transmission pattern, with cases increasing rapidly. The first case occurred on October 16, 2023, at 7 p.m., peaking at 3 a.m. on October 17, 2023, before gradually decreasing. The incubation period ranged from 1 to 20 hours, with an average of 5 hours and 6 minutes.

The food menu for this outbreak included fried chicken, chili sauce, and a side salad, all stored in a lunch box lined with banana leaves. A bivariate analysis showed that both fried chicken and chili sauce werestatistically significant foods. Fried chicken had the highest and most significant relative risk [RR], with an RR of 5.82 and a 95% CI of 1.54 to 21.97 [Table 2].

Multivariable analysis using multiple binomial regression is shown in Table 3. Only fried chicken was found to be statistically significant in this study. According to multivariable analysis, friedchicken hadthe largest and most significant relative risk, with an RR of 5.09 and a 95% confidence interval of 1.33-19.47. This means that after controlling for other variables, people who ate fried chicken had a five-fold higher risk of sickness than people who did not eat fried chicken.

Table 1.

Characteristic	Population at Risk	Number of Case	Attack Rate [%]
Sex
Male	59	32	47.1
Female	81	36	52.9
Age [years]
1-10	10	5	7.4
11-20	12	6	8.8
21-30	26	15	22.1
31-40	27	13	19.1
41-50	29	18	26.5
51-60	26	8	11.8
61-70	5	3	4.4
71-80	3	0	-
81-90	1	0	-
91-100	0	0	-
101-110	1	0	-
Occupation
PHC Employees	83	44	35.3
Not PHC Employees	57	24	64.7

Source: Primary data.

Table 2.

Food Items	Ill	Not Ill	RR	95% CI
Fried Chicken
Exposed	66	53	5.82	1.54- 21.97
Unexposed	2	19
Chili Sauce
Exposed	34	19	1.64	1.17-2.28
Unexposed	34	53
Side Salad
Exposed	16	14	1.12	0.76-1.66-
Unexposed	52	58

Table 3.

Food Items	Ill	Not Ill	aRR	95% CI
Fried Chicken
Exposed	66	53	5.09	1.33-19.47
Unexposed	2	19
Chili Sauce
Exposed	34	19	1.32	0.96-1.82
Unexposed	34	53

Table 4.

Characteristic	Bacillus cereus	Staphylococcus aureus	Escherichia coli	Outbreak
Symptoms
Diarrhea	±	±	±	+
Stomache	+	+	+	+
Malaise	-	-	-	+
Nausea	+	+	-	±
Dizziness	-	-	+	±
Fever	-	-	±	±
Vomiting	+	+	-	-
Incubation Period	2-4 hours	30 minutes-8 hours	12-48 hours	1-20 hours
Risk Factors	Storing cooked food at room temperature, storing cooked food in a big container in the refrigerator, and preparing meals several hours before serving	Storing cooked food at room temperature, storing cooked food in a big container in the refrigerator, touching cooked food at room temperature, and preparing meals several hours before serving	Infected people handling food, insufficient cold storage, inadequate cooking, cleaning, and hygiene, ingesting raw or undercooked meat	Fried chicken is cooked repeatedly with insufficient cold storage.
Food Characteristic	Cooked rice	Ham, meat and poultry products, high protein foods	Half-cooked meat, cheese, water	Fried chicken

Table 5.

Type of Sample		Results
Food Samples	Fried Chicken	Mold/yeast, E. coli pathogen, Proteus mirabilis, Escherichia coli non-pathogen

Source: Primary data.

4. DISCUSSION

The epidemiological investigation identified fried chicken as the source of the foodborne illness. Laboratory samples of the fried chicken tested positive for mold/yeast, pathogenic E. coli, Proteus mirabilis, and non-pathogenic E. coli. This supports the differential diagnosis linking the outbreak to E. coli bacteria. The type of food consumed, the symptoms, and the incubation period—ranging up to 20 hours—were key factors in determining the cause of the illness.

Escherichia coli are usually harmless bacteria that live in the intestines of humans and animals and contribute to intestinal health. However, consuming food or water contaminated with specific strains of E. coli can result in gastrointestinal problems ranging from mild to severe. Leafy greens, sprouts, raw milk and cheese, raw beef, and raw poultry have all been linked to previous E. coli outbreaks in the United States [12].

In Indonesia, pathogenic bacteria were shown to be the most common cause of food poisoning, contributing to 74.85% of cases [8,615 cases] and a CFR of 0.1%, with E. coli, Bacillus cereus, and Staphylococcus sp being the most prevalent. The presence of E. coli bacteria indicates poor sanitation and hygiene procedures. Several E. coli strains, particularly enterotoxigenic strains, may cause sickness in humans through various pathways. These bacteria cause toxins to be produced in the gastrointestinal tract [13].

Enterotoxigenic Escherichia coli [ETEC] is the primary intestinal bacteria responsible for tens of millions of cases of gastrointestinal illness annually [14]. ETEC infection is spread by contaminated food and water, particularly in underdeveloped nations with inadequate infrastructure for clean drinking water and waste disposal. Previous studies haveshown that ETEC can remain in excrement for over six months and that they typically appear in water as biofilms, which increases their chance of survival [15].

In this study, the primary symptoms of E. coli infection included abdominal pain, diarrhea, vomiting, and fever [16 ]. These symptoms align with those observed in this outbreak, particularly diarrhea and stomach pain. Anotherstudy noted that E. coli infections typically begin with non-bloody diarrhea, which resolves without complications. Additionally, compared to other types of bacterial gastroenteritis, patients with E. coliinfections often experience more intense abdominal pain. Diarrhea usually developswithin two to twelve daysafter consuming contaminated food [2].

Previous studies have identified E. coli in poultry and duck hatcheries, as well as in environmental samples and from humans in Egypt. In one study, E. coli was detected in 62 of 171 samples, representing 36.3% of the total [17 ]. Additionally, E. coli O157:H7 was isolated from various meat and poultry specimens, including ground beef, pork chop, pork loin, pork hock, ground pork, chicken leg, turkey drumstick, lamb riblet, lamb loin chop, lamb shoulder blade chop, and lamb leg [18 ]. This is consistentwith the findings in this outbreak, where fried chicken was identified as the primary source. It is possible that the infection was present from the outset, even before the food preparation process began.

E.coli bacteria can normally live at temperatures ranging from 8 to 46 degrees Celsius. These bacteriabacteria can be found in the kitchen, where raw materials are produced and processed before entering the cooked meal via hands, tool surfaces, cooking areas, and equipment [19]. According to our study, the chicken wasplaced in a container to allow it to air out after being removed from the pan. The chicken wasthen placed in the cupboards to be fried the following day. Thisindicates that the chicken was placed in an unsealed container. This is consistent with another study, which found that an unsealed food container has twice the risk of E. coli contamination [20].

We also discovered that the chicken was reheated many times, which could result in contamination. In a previous study, the analysis revealed that two re-heated food samples tested positive for E. coli. However, further research revealedno significant changes between re-heating and direct-cooking food [21]. Therefore, all types of foods are equally susceptible to contamination [22].

Thesefindings raiseconcerns regarding food safety. One crucial preventive measure is the promotion of proper personal hygiene practices. Additionally, providing essential facilities, such as access to clean water, handwashing stations with soap, changing rooms, and proper work attire (including uniforms, aprons, head coverings, masks, and gloves), is extremely beneficial [20].

CONCLUSION

There was an outbreak of food poisoning at the Pleret Public Health Center. Those at risk in this food poisoning outbreakincludedwomen between the ages of 41 and 50 and employees of public health centers. The most common symptoms experiencedwere diarrhea, stomach pain, and malaise. The incubation period lastedfrom 1 hour to 20 hours, with an average of 5 hours and 6 minutes. Furthermore, fried chicken wasthe source of food poisoning in this outbreak, with E. coli bacteria serving as the causative agent. Inadequate cooking and inappropriate cold storage wereadditionalrisk factors. Thus, raisingconcerns about food safety with employees and food handlers is essential.

STUDY LIMITATIONS

Our epidemiological investigation has some limitations. The results showed mold/yeast contamination since the samples of fried chicken were collected on October 18, 2023, rather than February 16, 2023, the initial day of the suspected outbreak. Additionally, no biological samples were collected for this study. This study employed total sampling at the health facility, but severelyill people who refused to be interviewed were excluded; thus, they may not be representative of the population.

REFERENCES