An Outbreak of Multiple Serotypes of Salmonella in New Zealand Linked to Consumption of Contaminated Tahini Imported from Turkey

Abstract

A widespread salmonellosis outbreak linked to consumption of hummus made from contaminated tahini imported from Turkey occurred in New Zealand in November 2012. This article summarizes the outbreak detection, investigation, and control. The New Zealand Enteric Reference Laboratory alerted public health units regarding a cluster of 11 persons with Salmonella Montevideo infection identified from different regions of the North Island of New Zealand. A multiagency outbreak investigation commenced to determine the source of illness and prevent further transmission. Salmonellosis is a notifiable disease in New Zealand. Outbreak cases were identified through routine salmonellosis notifications, and interviewed using a standardized questionnaire to identify common exposures. Clinical and food isolates were initially characterized by serotyping and then further typed by pulsed-field gel electrophoresis (PFGE). PFGE profiles were sent to PulseNet and international alerts were posted. The scope of the investigation widened to include persons with either Salmonella Maastricht and Salmonella Mbandaka infection following detection of these serotypes in tahini epidemiologically linked to laboratory-confirmed cases. All three of the tahini-associated serotypes were detected in people who had consumed tahini, and these were found to have PFGE profiles indistinguishable from the tahini isolates. Twenty-seven salmonellosis cases infected with at least one of the three tahini-associated Salmonella serotypes were detected between September 1 and December 31, 2012; of these, 16 (59%) cases (12 with Salmonella Montevideo, 3 with Salmonella Mbandaka, and 1 with Salmonella Maastricht infection) had PFGE patterns indistinguishable from the outbreak profile. The investigation led to a trade withdrawal and consumer recall for tahini sesame paste from the consignment and products containing this tahini. The outbreak ceased following the recall. The importer of the implicated tahini was reminded of his duties as a food importer, including ensuring appropriate product testing. Changes to New Zealand legislation strengthened food safety responsibilities of food importers.

Introduction

Outbreaks of salmonellosis have been attributed to consumption of low-moisture foods including spices and raw flour (Vij et al., 2006; Gieraltowski et al., 2013; McCallum et al., 2013), as well as high-fat foods with low water content including chocolate, peanut butter, and tahini (sesame seed paste) (Brockmann et al., 2004; Werber et al., 2005; Vij et al., 2006; CDC, 2007, 2009; Sheth et al., 2011). Outbreaks of Salmonella related to the consumption of contaminated processed sesamum products including tahini and halva have also been documented (Andersson et al., 2001; Unicomb et al., 2005; CDC, 2012, 2013).

On November 21–22, 2012, the Enteric Reference Laboratory (ERL) at the Institute of Environmental Health and Research (ESR) issued alerts to public health units regarding a cluster of 11 isolates of Salmonella enterica subspecies enterica serovar Montevideo (hereafter referred to as Salmonella Montevideo) isolates from cases in the North Island of New Zealand. This was an aberrant event because between 2008 and 2011, Salmonella Montevideo was reported in clinical isolates from only 0–13 patients annually in New Zealand (ESR, 2012). As the alerted cases were geographically dispersed in the North Island, an outbreak investigation was initiated to identify the source and prevent further transmission. The outbreak investigation was widened to include Salmonella Maastricht and Salmonella Mbandaka cases following detection of all three serotypes in food products epidemiologically linked to cases.

Materials and Methods

The outbreak was investigated through the collaboration of public health units, the Ministry for Primary Industries (MPI), the ESR public health laboratory, and ERL. The ESR Health Intelligence Team conducted the epidemiological investigation. Information was shared between agencies via regular teleconferences and electronically distributed situation reports. The New Zealand Ministry of Health participated in teleconferences and assisted throughout the investigation.

Epidemiological investigation

A descriptive epidemiologic study was conducted using routine notification data and data collected from interviews with cases. Salmonellosis is a notifiable disease in New Zealand, and the surveillance process has been described previously (McCallum et al., 2013). The ERL at ESR provides a national Salmonella reference service where presumptive Salmonella species isolated from human, animal, food, and environmental sources are characterized through serotyping and for some serotypes through phage typing. If an outbreak is suspected, molecular characterization of isolates was also performed.

In this investigation, potential cases were retrospectively and prospectively identified from persons notified for salmonellosis and with Salmonella Montevideo, Salmonella Mbandaka, or Salmonella Maastricht isolated from clinical specimens by the ERL. A standardized questionnaire was developed containing questions on demographics, date, and time of symptom onset and duration of illness, in addition to foods consumed and other salmonellosis-associated exposures in the 7 days prior to illness onset. Specific questions were included for foods commonly associated with Salmonella infection. The questionnaire was administered in telephone interviews conducted by public health unit staff.

A case was defined as a person experiencing gastrointestinal illness (diarrhea with abdominal cramps or headache or fever and/or vomiting) with an onset after September 1, 2012, and who were laboratory confirmed by the ERL as being infected with Salmonella Montevideo, Salmonella Mbandaka, or Salmonella Maastricht with a pulsed-field gel electrophoresis (PFGE) profile indistinguishable from the outbreak strain of these organisms.

Data from questionnaires was entered into EpiData (version 3.1 EpiData Association, Odense, Denmark), descriptive analysis was performed using Microsoft Excel (Microsoft Corporation, Redmond, WA).

Microbiological investigation

Presumptive Salmonella isolates were referred by medical laboratories to ERL for confirmation. Routine serotyping using the White-Kauffmann-Le Minor scheme (Grimont and Weill, 2007) was performed by the ERL to identify potential outbreak cases. Single-enzyme PFGE using the standardized laboratory PulseNet protocol (Ribot et al., 2006; CDC, 2011) was then undertaken to further discriminate the Salmonella Montevideo, Salmonella Mbandaka, and Salmonella Maastricht isolates suspected to be part of the outbreak. In addition, a selection of human isolates reported prior to September and nonhuman isolates of the same serotypes originating from meat and bone meal, poultry feed, and bovine sources were also characterized by PFGE for comparison (Swaminathan et al., 2001; Fisher et al., 2005).

Food samples were tested for the presence of Salmonella at ESR using standard culturing methods (APHA, 2001; ISO, 2002). Two of the Salmonella-positive samples were also analyzed quantitatively by the most probable number (MPN) method (APHA, 2001).

Presumptive Salmonella isolates recovered from food samples were serotyped and PFGE typed.

On December 3, 2012, the Salmonella Montevideo PFGE profile was submitted to PulseNet International, the international molecular subtyping network for foodborne disease pathogens, to see if this profile was present in their database.

Environmental investigation

Public health unit and MPI staff carried out environmental investigations of food premises that had manufactured ready-to-eat food consumed by cases. Investigations included review of food preparation systems and processes, inspections for hygiene of premises including hand-washing facilities, review of policies and procedures for managing sick food handlers, and inspection of records for recent illness among food-handlers. Samples of foods that had been consumed by cases were collected for microbial testing. Food handlers and staff at the premises were requested to provide fecal samples for analysis.

Selected food ingredients used by these premises were traced back through the distribution network and to import consignments as appropriate. Samples of these ingredients were collected from distributors.

Results

Epidemiological investigation

Salmonella Montevideo was identified in isolates from 19 persons notified with salmonellosis between September 1 and December 31; of these, 12 (75%) met the case definition. One further patient with Salmonella Montevideo infection had a closely related PFGE pattern and was epidemiologically linked to the investigation; this case was excluded from the descriptive analysis. Four of the remaining six cases with distinguishable PFGE profiles were overseas during the incubation period of the disease.

In the same period, seven people were notified with Salmonella Mbandaka infection, and three of these met the case definition. One person was notified with Salmonella Maastricht infection at the end of November 2012 and was also defined as a case (Fig. 1). This was the first time human infection with this serotype had been identified in New Zealand.

FIG. 1.

Epidemic curve of outbreak-associated salmonellosis cases notified in New Zealand, September 1 to December 19, 2012, by onset date, showing key events. Figure excludes n=1 case of Salmonella Mbandaka where date of symptom onset was unknown.

The 16 cases were reported from six district health boards in the North Island including the following: Auckland and Bay of Plenty (5 cases each), Waikato (2 cases), Waitemata (2 cases), Northland and Hawke's Bay (1 case each). Cases ranged in age from 23 months to 68 years with a median of 24.5 years; 10 (62.5%) cases were female. The majority of cases were identified as being of European descent (14/16 cases).

For those with available information (15/16 cases), illness onset dates ranged between October 1 and December 14, 2012. Three cases were hospitalized, and no deaths were reported. Case symptoms continued for 2–14 days (median 7 days) and included diarrhea (94%, 15 cases), abdominal pain (81%, 13 cases), fever (75%, 12 cases), nausea and headache (44%, 7 cases each), muscle aches (44%, 7 cases), chills (31%, 5 cases), and vomiting (31%, 5 cases). Dizziness was also reported from two cases and itchy/sore skin in another two cases.

Eleven cases (65%) had eaten at 1 of 7 different Middle Eastern restaurants during the incubation period of the disease. The implicated restaurants were located in Auckland, Bay of Plenty, and Napier in the North Island of New Zealand. Nine cases recalled having consumed hummus as part of their meal, and one further case thought it might have been in their meal but was uncertain. Of the five cases that had not eaten from a Middle Eastern food premises, two had consumed commercially prepared hummus purchased from local supermarkets, with one case also having consumed tahini purchased from a bulk bin store. Samples of the bulk tahini were tested and no Salmonella was isolated. No other food items of interest were identified through case interviews.

Environmental investigation

Initial interviews conducted as part of routine surveillance of salmonellosis cases identified that four cases consumed food from the same Middle Eastern food premises between November 3 and 6; tahini-based hummus was identified as a common ingredient in meals consumed by the cases. Samples of tahini, dried chickpeas, bulgur wheat, white pepper, cumin, mint, chilli, garlic, and tomato paste were collected from this premises and tested for the presence of Salmonella. Salmonella Mbandaka and Salmonella Maastricht were identified from the leftover tahini that had been used to prepare hummus consumed by the four cases; all other tests of food items were negative. All food handlers at the premises were interviewed and none declared symptoms of gastroenteritis in the weeks prior to onset of the cases' illnesses; fecal specimens were collected from each food handler, and Salmonella was not detected. Salmonella was not detected in samples of tahini or tahini-based products collected during investigations of the other cases.

The Salmonella-contaminated tahini was part of a consignment imported directly from Turkey, arriving in New Zealand on September 3, 2012; investigators considered that the product was likely to have been distributed nationally shortly after importation. All batches of tahini in the consignment were labeled with an expiration date of June 2014.

Unopened containers of tahini imported as part of this consignment remained at the warehouse of the New Zealand distributor; seven samples were collected from these containers and were tested for Salmonella. Salmonella was detected in each of the seven samples, and in five of the seven samples multiple serotypes were identified. In total, Salmonella Montevideo was detected in six samples, Salmonella Mbandaka was detected in four samples, and Salmonella Maastricht was detected in three samples.

All three outbreak strains (Salmonella Montevideo, Salmonella Mbandaka, and Salmonella Maastricht) were isolated from unopened tubs of tahini sesame paste sourced from the warehouse of the New Zealand distributor. Estimates of the level of contamination (all serovars) in two of the warehouse samples were 0.24 MPN/g (95% CI: 0.07–0.85) and 0.46 MPN/g (95% CI: 0.1–2.1).

New Zealand operates a risk-based food safety regimen for imported foods. Tahini and other crushed sesame seed products are identified as prescribed foods (MPI, 2013a); this requires sampling and clearance Salmonella testing of import consignments. Test frequency is based on importers' past history of test results (MPI, 2013b). Imported foods subject to clearance testing are identified using a tariff code system: Importers identify the contents of their consignments using tariff codes that are then used by the New Zealand Customs Service to detect prescribed foods.

In this outbreak, investigations determined that the tariff code provided for the consignment by the importer's customs agent did not identify that it contained prescribed foods. The testing and clearance process was therefore not triggered before the product was distributed on the New Zealand market.

Microbiological investigation

The PFGE profiles identified during the investigation had not previously been seen before in New Zealand. The profile for the Salmonella Montevideo isolates was identical to a PulseNet USA pattern JIXX01.1027, which was associated with a previous outbreak involving 17 persons in September 2012 (Gonzalez-Aviles, 2012).

The PFGE profiles of the isolates were identical to the pattern found in cases who had reported eating Middle Eastern food prior to becoming ill (Fig. 2).

FIG. 2.

Pulsed-field gel electrophoresis (PFGE) patterns of XbaI-digested DNA from Salmonella Montevideo, Maastricht, and Mbandaka strains isolated in case patients or tahini identified as the source of the 2012 outbreak, and non-outbreak-associated patient, poultry, or bovine isolates confirmed during 2012. The outbreak profiles are illustrated in lanes 3, 4 (Salmonella Montevideo), lanes 9, 10 (Salmonella Mbandaka), and lanes 14, 15 (Salmonella Maastricht). **MBM, meat and bone meal.

Control measures

The investigation in New Zealand led to a trade withdrawal and a consumer recall for tahini sesame paste from the implicated consignment and for products manufactured using the tahini.

Suspected Salmonella species were isolated on December 9 from tahini samples that had been collected from leftover product consumed by three cases. National recall of the entire product consignment was not indicated at this stage because all these samples had been collected from an opened container obtained from a single food premises. However, the New Zealand distributor voluntarily placed all remaining product on hold and advised customers to hold product until the distribution network was established and laboratory testing was completed. Salmonella species were then isolated on December 16 from samples collected from unopened containers of tahini held at the distributor's warehouse, and a national consumer-level recall of the entire consignment was announced the following day. No further cases were identified after this date.

The tahini importer and customs broker were formally advised of appropriate tariff codes to be applied for future shipments of sesame-based products, and subsequent sesame-based product importations by this importer were subjected to mandatory sampling and testing. Information on the outbreak and links to contaminated product were conveyed to the appropriate authorities in Turkey.

Salmonella Montevideo PFGE results were loaded up to PulseNet on December 3, 2012, and as a result of these updates to PulseNet a connection between New Zealand cases and cases reported in the United States between March and May 2013 was established. A subsequent alert was circulated to the International Food Safety Authorities Network (INFOSAN) on June 12, 2013.

Discussion

This multiagency investigation was successful because the contaminated food source was identified early. Findings from case histories, environmental, and microbiological investigation suggested that this outbreak was due to contaminated tahini imported from Turkey. The common link between cases was detected early, and the infecting agents were identified in unopened tubs of tahini.

This is not the first time multiple serotypes of Salmonella have been identified in tahini. The likely reason for this is that sesame seeds can become contaminated with Salmonella during the growth, storage, and processing stages (Podolak et al., 2010). As tahini is usually manufactured without further heat treatment following roasting of the sesame seeds, prevention of cross-contamination after roasting is vital for food safety.

An increase in Salmonella Montevideo cases was observed in 2003 when an outbreak involving 68 cases in New Zealand and Australia was linked to the consumption of tahini imported from Egypt and Lebanon (Unicomb et al., 2005). A separate outbreak occurred in 2007 associated with a kebab takeaway stall in Wellington (Ruscoe, 2008).

Salmonella is unlikely to grow in tahini due to a low-moisture environment, although it is able to survive for long periods of time, representing a risk to the consumer.

A study by Torlak et al. (2013) found that although Salmonella did not grow in tahini, it survived for 4 months at both room and refrigerator temperatures. The study also confirmed that the viability of Salmonella at 4°C was significantly higher compared to at 22°C (Torlak et al., 2013). Foods with a high fat content and low water activity may even protect the Salmonella from inactivation (Podolak et al., 2010). These findings have important implications for tahini, which is widely distributed and has a long shelf-life.

Although the numbers of Salmonella found in the tahini product associated with this outbreak were low, the concentration is consistent with that found in other outbreaks. Quantitative tests on sesame product tested in relation to a 2003 New Zealand outbreak of Salmonella Montevideo also indicated low numbers of the pathogen present in the implicated product. The concentration of the outbreak strain in tahini (eight samples) and other sesame products (halva [one] and hummus [one]) ranged from <0.03 MPN/g to 0.46 MPN/g (Unicomb et al., 2005).

As a result of increasing international trade, food products produced in one country can be widely distributed and consumed in different parts of the world. The New Zealand outbreak concluded with the product recall in December 2012. A few months later, between March and May 2013, 16 persons infected with Salmonella Montevideo and Salmonella Mbandaka were reported from nine states in the United States (CDC, 2013; FDA, 2013). An investigation led to the identification that tahini sesame paste imported from Turkey was the source of the outbreak. A nationwide recall occurred on April 28, 2013 and was later expanded to include further products with different expiration dates. In both the United States and New Zealand, PFGE analysis was conducted on clinical and food samples and shared with PulseNet International. Through PulseNet, it was confirmed that the outbreak strains of Salmonella Montevideo and Salmonella Mbandaka in the United States and New Zealand were indistinguishable. The value of international alerts when food products with a long shelf life are distributed internationally has been demonstrated in these investigations.

It is well documented that reported cases represent a fraction of the total number of people infected, as not all people seek medical attention for enteric illness and provide diagnostic specimens (Lake et al., 2010). In this investigation, early detection and removal of the source minimized the burden on the New Zealand public health system.

Incorrect tariff code reporting during the importation of the product implicated in this outbreak has been addressed by the regulatory agency. Food importers are subject to additional food safety requirements under the recently passed Food Act 2014. This outbreak reinforces the importance of risk-based programs for monitoring the safety of high-risk imported foods.

Conclusions

This outbreak was associated with the consumption of hummus prepared with tahini imported from Turkey and found to be contaminated with multiple serotypes of Salmonella. The investigation led to a trade withdrawal and consumer recall for tahini sesame paste from the consignment and products containing this tahini.

Footnotes

Acknowledgments

The authors would like to thank the staff in the ESR laboratories that conducted the microbiological investigation, the public health unit staff for their case interviews and sample collection, and MPI Food Act Officers for their environmental investigation and sampling, all of whom provided the information crucial to identifying the source of the outbreak. Also acknowledged are the MPI staff for coordinating the food response, managing the product recall and destruction of implicated product, and the Ministry of Health for their involvement and support.

Disclosure Statement

No competing financial interests exist.

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