17-9-12-523 in New South Wales, compared to historical take-away food consumption, April, 2013 Exposure Number of cluster cases that consumed food item (n) Proportion of cluster cases that consumed food item (%) Historical food consumption data* (%) p-value Chicken or produce containing chicken prepared or eaten outside of the home 9 60 44/180 (24) 0.01 Asian cuisine 5 33 10/250 (4) <0.01 Sushi/sashimi 4 26 12/222 (5.4) <0.01
*Proportion of previously notified NSW Salmonella cases that consumed the same food item
Consumption of eggs was higher among cluster cases than historical comparison data (13/15 vs 35/128) (Table 3), however this was not statistically significant (p=0.09). The consumption of Asian cuisine and sushi/sashimi was also higher than expected
compared to historical consumption data and this was significant for both food items (p<0.01) (Table 4).
A separate review of the Asian cuisine meals consumed by the five cluster cases identified five different meals from five different Asian restaurants. Egg was identified as a common high Salmonella risk ingredient in all of the Asian cuisine meals that had been consumed by the separate cluster cases.
After the exclusion of the five cluster cases who had consumed Asian meals, the food consumption information for the remaining ten cluster cases was reviewed. Commonly consumed foods are listed below (Table 5, Table 6). The consumption of a number of food items was higher than expected. The consumption of any eggs was higher among cluster cases when compared to historical data but this was not statistically significant (8/10 vs 101/160, p=0.50). The consumption of free range eggs was also higher than expected among cluster cases compared to historical data and this result was
significant (7/10 vs 35/128, p=0.01).
Eight cases reported eating eggs purchased from the same major supermarket chain. No common brand was identified. A total of four cases reported consuming eggs that were raw or runny or products containing raw or runny egg such as uncooked cake batter. Other food items with higher than expected consumption included sliced deli ham (5/10 vs 49/146, p=0.32), yoghurt (6/10 vs 65/136, p=0.52), milk (8/10 vs 87/136, p=0.50), mushrooms (6/10 vs 82/236, p=0.17), frozen berries (5/10 vs 7/140, p=<0.01) and chocolate (8/10 vs 57/138, p=0.02) (Tables 5 and 6).
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Table 5: Frequency of meat and dairy consumption reported by 10 patients with STm 3- 17-9-12-523 in New South Wales compared to historical meat and dairy food
consumption frequency, April, 2013 Exposure Number of cluster cases that consumed food item (n) Proportion of cluster cases that consumed food item (%) Historical food consumption data* (n/total)(%) p-value Fresh pre-cut chicken 5 50 95/160 (60) 0.74
Sliced deli ham 5 50 49/146 (33) 0.32
Any eggs 8 80 101/160 (63) 0.50
Free range eggs 7 70 35/128 (27) 0.01
Yoghurt 6 60 65/136 (48) 0.52
Pasteurised full cream milk
8 80 87/136 (64) 0.50
Hard cheese 7 70 92/137 (67) 1.00
*Proportion of previously notified NSW Salmonella cases that consumed the same food item
Table 6: Frequency of fruit/vegetable/chocolate consumption reported by 10 patients with STm 3-17-9-12-523 in New South Wales compared to historical fruit/vegetable/chocolate consumption frequency, April, 2013
Exposure Number of cluster cases that consumed food item (n) Proportion of cluster cases that consumed food item (%) Historical food consumption data* (n/total)(%) p-value Carrots 5 50 176/239 (73) 0.14 Red, white or brown onion 6 60 154/239 (64) 0.75 Lettuce 5 50 125/242 (52) 1.00 Mushrooms 6 60 82/236 (34) 0.17 Apples 6 60 155/241 (64) 0.75 Bananas 5 50 179/241 (74) 0.14 Frozen berries 5 50 7/140 (5) <0.01 Chocolate 8 80 57/138 (41) 0.02
*Proportion of previously notified NSW Salmonella cases that consumed the same food item
Environmental Investigation
Details regarding egg brands, size, date of purchase and batch numbers were unable to be provided to the NSWFA for a trace back investigation due to poor case recall and the short shelf life of eggs. The NSWFA reported to HNE OFN that there had not been any detections of STm 3-17-9-12-523 in the chicken meat of the previously implicated poultry processor for six months prior to the cluster.
Discussion
In 2010, 44% of Salmonellosis cases in Australia were attributable to STm.9 Where STm has been identified as the source in an outbreak setting in Australia, raw or undercooked eggs have been the most frequently identified source.9
One of the features of this cluster was the high proportion of cases who had consumed Asian cuisine when compared to historical data (Table 4). Egg was identified as a
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common high risk ingredient for Salmonella in all five Asian cuisine meals which had been consumed by cluster cases. Egg was also identified as a commonly consumed food item among cluster cases who had not consumed this cuisine. Eighty percent of these cases had consumed eggs which is higher than expected when compared to historical egg consumption data (Table 3).
It is biologically plausible that contaminated eggs were the contaminated food responsible for illness in this cluster as the consumption of eggs is a well-known risk factor for Salmonellosis, especially the consumption of raw or undercooked egg.9 In this cluster investigation, 4/10 (40%) of cluster cases who had not eaten Asian cuisine but who had eaten eggs reported consuming eggs that were raw or runny, or had consumed products containing raw egg such as cake batter.
Further, it is possible that the cases who had consumed Asian cuisine had
undercooked egg in their meal, but this couldn’t be verified in this investigation. Asian cuisine however, has previously been implicated in other STm outbreak investigations where raw or undercooked egg has been the suspected source of the outbreak.10,11
Additional evidence implicating egg was the absence of positive STm isolates in the chicken meat sampling program of a previously implicated food processor. The absence of detections in a chicken meat sampling program of a previously implicated processor that did not change over time, in addition to the fact this unique strain of STm has only been previously identified in poultry, added to the evidence that egg was the most likely source of the cluster.
It is also possible that a food item other than eggs may have been the source of this outbreak. STm has been identified in a number of other food items which have caused outbreaks of Salmonellosis in Australia.11,12 Eggs however, remain the predominant cause of STm outbreaks in Australia with approximately 60% of STm outbreaks attributable to eggs.9 In addition to this, the strain of Salmonella detected in this investigation was a novel strain that had previously been found only in poultry so it is unlikely that another food item was the source of this outbreak.
Limitations
There were limitations to this investigation including recall bias due to delays in interviewing cases as a result of the time it takes to receive MLVA data. Salmonella
specimens have to be received and cultured in the local laboratory before being sent to ICPMR for MLVA typing as ICPMR is the Salmonella reference laboratory for NSW.
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This process can take up to a week. Once the specimen has been received by ICPMR, the turnaround time for MLVA is up to two weeks. This means there is up to a three week delay between a person submitting a specimen and the OzFoodNet site receiving the MLVA results. MLVA data, however, remains the timeliest Salmonella surveillance data. Other methods of Salmonella typing such as phage typing can take up to two months.
The time frame from a case consuming contaminated food, becoming symptomatic, submitting a stool sample for analysis and the receipt of MLVA information is approximately 3 weeks. This leads to delays in interviewing which results in cases being unable to recall details about egg consumption, particularly egg brands, size and date of egg purchase. The opportunity to obtain batch numbers for eggs was also lost as eggs have a short shelf life of approximately two weeks. The details of egg
consumption are essential in taking further action such as testing in a cluster investigation where eggs are suspected as the source of infection.
The lack of detail regarding egg consumption in this investigation led to the
investigators being unable to take further public health action. An analytical study may be of limited value in a cluster investigation where egg is suspected as the source of infection, as it can be a common ingredient in a number of foods, hence reducing the possibility of detecting an association between egg and illness.
Another limitation in this investigation is the quality of the historical food consumption comparison data. There is a possibility that historical egg and chicken consumption data may be over-represented in the database as these are common sources of
Salmonella. This could make it difficult to see differences in the consumption of egg and chicken between new Salmonella cases and previous Salmonella cases.
Conclusion
Egg was identified as a possible transmission vehicle in this cluster. A higher than expected proportion of cluster cases had consumed eggs when compared to historical food consumption data. A higher than expected proportion of cluster cases had also consumed Asian cuisine compared to historical food consumption data and a review of the Asian meals identified egg as a common ingredient in these meals. The information obtained in this investigation is consistent with the current understanding of the
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Recommendations
The findings of this investigation should be shared with the OFN network through regular reporting mechanisms. Surveillance of gastroenteritis due to Salmonella
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Salmonella Typhimurium 3-17-9-12-523 outbreak investigation Abstract
Background
Salmonella is a gram negative enteric bacterium which can cause acute gastrointestinal illness or enteric fever in humans. Infection with non-typhoidal
Salmonella serovars causes acute gastrointestinal illness which can result in serious systemic illness and long-term sequelae such as irritable bowel syndrome, reactive arthritis and Guillian Barre syndrome.
Approximately 72% of all Salmonella cases in Australia are transmitted through food and a large proportion (44%) can be attributed to Salmonella Typhimurium (STm). Eggs have been identified as the primary transmission vehicle of this Salmonella type in 60% of foodborne outbreaks where this pathogen is implicated. In May 2013, the HNE OFN team identified nine cases of Salmonella Typhimurium 3-17-9-12-523 who had consumed meals at the same bowling club bistro in the HNE region over a seven day period.
Methods
The outbreak occurred at a bowling club bistro situated within the premises of a licensed club. The HNE OFN team initiated an unmatched case-control study using restaurant booking lists and Salmonella laboratory notifications to recruit cases and controls. Cases were defined as a person who had symptoms of gastroenteritis within seven days of eating at the bowling club bistro and/or had Salmonella Typhimurium with the MLVA profile 3-17-9-12-523 detected in a clinical sample. Controls were defined as a person who ate at the bowling club bistro during the outbreak period and did not have illness within seven days of eating at the bowling club bistro.
Cases and controls were interviewed by telephone using a questionnaire that was a modified version of a case-control questionnaire that had been used in a 2006 national foodborne outbreak investigation. The questionnaire contained questions on
demographic information, details of clinical illness and details of food exposure. The demographic characteristics of cases and controls were described and compared. Univariate analysis was conducted to calculate the attack rate and crude odds ratio for each food item with the 95% confidence intervals and p-values with significance set at 0.05. A multivariable logistic regression model was then constructed using all food items with a p-value<0.25 to calculate the adjusted odds ratio with 95% confidence intervals and p-values with significance set at 0.05.