Surveillance camera recordings helped identify lapses during food preparation and poor sanitation as part of a Salmonella outbreak in Taiwan in 2018, according to researchers.

In late April 2018, a salmonellosis outbreak among customers of a restaurant was reported to the Taiwan Centers for Disease Control.

Researchers identified 47 patients, including 16 who tested positive for Salmonella, and one who died. Compared with 44 controls, cases were more likely to have had a French toast sandwich.

Camera recordings revealed eggshell contamination, long holding time at room temperature and use of leftovers during implicated food preparation, according to the study published in the journal Epidemiology and Infection.

In Taiwan, Salmonella is the third most common agent, accounting for 97 of 500 bacteria-related foodborne outbreaks from 2013 to 2018.

Patient details
In April 2018, 19 ill people associated with the outbreak in southern Taiwan were reported to the Taiwan CDC. A preliminary investigation by a local health authority found all patients had eaten at a local restaurant.

Onset date for the 47 cases ranged from April 18 to 26 and peaked on April 21. Fourteen of them needed hospital treatment. The median age was 30 years, with a range of 1 to 68 years old, and 32 were men. Median incubation period was 10 and a half hours but ranged from half an hour to 52.5 hours.

The 24-year-old male who died did not have underlying diseases. He ate in the restaurant on April 21. He had abdominal pain and diarrhea the next morning and was found dead two days later. Results of the autopsy and microbiological examination demonstrated Salmonella bacteremia and causes of death were metabolic failure and septic shock.

Of 47 cases, samples from 17 were tested. Salmonella was isolated from 16 patients, of whom 12 ate French toast sandwiches. Among the 16 confirmed infections, one was also positive for norovirus and another for Bacillus cereus. All nine food handlers had no symptoms and specimens were negative for enteric bacteria, norovirus and rotavirus.

Four did not eat a french toast sandwich but researchers said the violations identified via camera recordings strongly suggested cross-contamination occurred in the restaurant. Among 70 items consumed by patients and controls, only the french toast sandwich was significantly associated with illness.

Negative sampling but video records
Restaurant operations were suspended by local health authorities on April 27 and it was cleaned but no historical food safety inspection record was available.

Food items and environmental samples tested negative for Salmonella Enteritidis. The implicated french toast sandwiches and egg mixture were discarded before the investigation and not available for microbiological testing.

Traceback investigation of eggs in early May 2018 found none of the same batches were left and laying hens were all culled. Random sampling of 20 fresh eggs, 20 washed eggs and 20 cloacal swabs of laying hens from other flocks for Salmonella were negative.

According to food handlers, they prepared the egg mixture daily by breaking and mixing eggs in a bowl. They assembled ingredients in the bread, dipped the sandwich into the egg mixture, fried it on a heated griddle and put a pan-fried egg in it. After bread turned golden, a piece of ham was put on the outside of the sandwich. This sandwich could be made-to-order or were ready to serve.

Researchers found lapses in preparation when watching surveillance camera footage such as eggshells being dropped into the mixing bowl and retrieved by food handlers during egg mixture preparation.

“The recordings also showed that the mixing bowl was not washed during operation hours. The egg mixture was stored at room temperature for 18 hours after preparation. Moreover, food handlers reserved the leftover egg mixture and continuously used it for three days. In addition, the recordings also showed that raw eggs, raw ingredients and cooked food items had been placed on the same cooking counter. Food handlers cooked foods right after handling raw ingredients, without washing their hands.”

Prevention steps
Recommendations for restaurants are to use pasteurized egg products, ensure a high enough cooking temperature and long enough cooking time to kill Salmonella.

The outbreak might be attributed to an undercooked egg mixture or contaminated eggs, said researchers.

“. . . restaurants should use a food thermometer to ensure adequate cooking temperature with appropriate time and an internal temperature over 71 degrees C (160 degrees F) for egg dishes, to inactivate Salmonella.”

Scientists also said restaurants should not hold egg mixtures at room temperature for more than two hours before cooking and avoid continuous use of leftover egg mixture.

“Food handlers should be strictly adherent to Good Hygiene Practice guidelines, including separating raw ingredients and cooked foods in different areas, ensuring appropriate storage temperatures according to recommendations for each food and maintaining good personal hygiene during food processing,” according to the report.

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