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Coulombe, G.;  Tamber, S. Salmonella enterica Outbreaks from Tahini and Tahini-Based Products. Encyclopedia. Available online: https://encyclopedia.pub/entry/37882 (accessed on 01 July 2024).
Coulombe G,  Tamber S. Salmonella enterica Outbreaks from Tahini and Tahini-Based Products. Encyclopedia. Available at: https://encyclopedia.pub/entry/37882. Accessed July 01, 2024.
Coulombe, Geneviève, Sandeep Tamber. "Salmonella enterica Outbreaks from Tahini and Tahini-Based Products" Encyclopedia, https://encyclopedia.pub/entry/37882 (accessed July 01, 2024).
Coulombe, G., & Tamber, S. (2022, December 02). Salmonella enterica Outbreaks from Tahini and Tahini-Based Products. In Encyclopedia. https://encyclopedia.pub/entry/37882
Coulombe, Geneviève and Sandeep Tamber. "Salmonella enterica Outbreaks from Tahini and Tahini-Based Products." Encyclopedia. Web. 02 December, 2022.
Salmonella enterica Outbreaks from Tahini and Tahini-Based Products
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This entry is adapted from the peer-reviewed paper 10.3390/microorganisms10112299

Salmonella is a leading cause of bacterial foodborne illness in the world. Although typically associated with foods of animal origin, low-moisture foods, such as tahini, are quickly gaining recognition as an important vehicle of Salmonella exposure.

foodborne illness foodborne outbreak low-moisture foods sesame tahini Salmonella

1. Introduction

Salmonellae are an important cause of human illnesses worldwide. It is estimated that nontyphoidal Salmonella causes 93.8 million illnesses, of which an estimated 80.3 million are foodborne, and 155,000 deaths each year, worldwide [1]. Most salmonellosis cases are sporadic, meaning they are not linked to known outbreaks [2]. Outbreaks linked to Salmonella are often associated with the consumption of foods of animal origin or fresh produce [3]. Multiple outbreaks involving other food commodities have also been reported. Particularly problematic are low-moisture foods, which are defined as foods having a water activity (aw) of 0.85 or below. This category of foods includes chocolate, peanut butter, and tahini, all of which have been linked to multiple large outbreaks of salmonellosis across the globe.
Low-moisture foods are generally regarded as low-risk foods because they cannot support the growth of pathogenic bacteria, including those belonging to the genus Salmonella. Salmonella, however, has the capacity to survive in low-moisture foods for extended periods, up to several years. This prolonged survival increases the risk associated with the consumption of low-moisture foods. As shelf-stable products, a contaminated batch of low-moisture food has the potential to be ingested over time on multiple occasions by multiple people, leading to a wider temporal and geographic distribution of the pathogen than with other food commodities, and a consequent higher number of cases. Three of the largest salmonellosis outbreaks reported in the published literature are linked to low-moisture foods; dried cuttlefish snacks, paprika, and peanut butter with 1505, 1000, and 715 reported cases, respectively [4][5][6].

2. Salmonella

The genus Salmonella consists of two species, S. enterica and S. bongori, that have been subtyped into over 1500 serological variants, or serovars. In terms of human illness, multiple serovars of S. enterica account for over 99% of human salmonellosis cases. Children under 5 years old, the elderly, and people with compromised immunity are most vulnerable to salmonellosis and more likely to develop severe symptoms [7][8].
Estimates of the infectious dose for Salmonella range from 100 to 1011 cells [9][10]. Host-related factors such as age and immune status account for much of this variability. The virulence properties of individual strains and the composition of the food matrix can also influence the number of bacteria required to produce an infection. There is evidence that food matrices with a combination of high fat and low water activity (aw) in a food matrix may protect Salmonella from the acidic conditions of the stomach, thus increasing the likelihood of illness from consuming low numbers of the microorganism [11][12]. Analyses of outbreak-associated, high-fat, low-moisture foods such as chocolate and potato chips indicate that inocula ranging from 1 to 45 cells can lead to symptomatic infections [4][13][14][15].
Concentrations of Salmonella ranging from <0.03 MPN/g to 0.46 MPN/g have been found in tahini and tahini-based products linked to salmonellosis outbreaks [16][17]. Based on these levels and the infectious doses reported above, the consumption of as little as 2 g of contaminated product has the potential to lead to illness.

3. Outbreaks Due to the Presence of Salmonella in Tahini and Tahini-Based Products

The first reported salmonellosis outbreak linked to the consumption of tahini occurred in 1995 in the United States. A total of 137 individuals got sick due to the presence of Salmonella ser. Brandenburg. Following that, in 2001, there was an international outbreak of Salmonella ser. Typhimurium DT104 due to consumption of halva, a ready-to-eat confectionary made with tahini. Cases were reported in Europe as well as Australia and New Zealand. In 2002 and 2003, three outbreaks of Salmonella ser. Montevideo linked to the consumption of tahini occurred in Australia and New Zealand. The implicated tahini products were manufactured in Egypt and Lebanon.
Diverse Salmonella serovars have been isolated during the course of these outbreak investigations, including some reported in multiple outbreaks: Concord (two outbreaks), Heidelberg (two outbreaks), Mbandaka (three outbreaks), Montevideo (five outbreaks), and Typhimurium (three outbreaks). In 2016 and 2017, an outbreak of a previously undescribed Salmonella serovar, Vari, occurred in five European Union countries. The investigation into this outbreak indicated that cross-contamination likely occurred at the Greek manufacturing facility during the production of tahini [18].
Some outbreaks have involved multiple serovars. Six serovars were isolated during the investigation of a multicountry outbreak linked to tahini and halva imported from Syria. In that outbreak, cases were identified intermittently from 2019 to 2022 in five European countries (i.e., Denmark, Germany, the Netherlands, Norway, and Sweden), as well as Canada (eight cases), the United States (six cases), and New Zealand (three cases). This outbreak illustrates the worldwide distribution of tahini and tahini-based products. The investigation into this outbreak was not able to determine the root cause of Salmonella contamination. However, since the implicated products were in sealed packages, it is likely the contamination event occurred prior to packaging and, hence, exportation [19].
In two instances, illnesses linked to tahini and hummus have occurred in Canada. In 2018, Canadian cases were reported, and the source was identified as imported tahini from Israel. This resulted in a recall [20]. In 2020, a localized outbreak linked to hummus involved a restaurant and a food truck from a single region. There were 45 laboratory-confirmed cases, and 185 cases which were symptomatic but were not laboratory confirmed. This outbreak illustrates the risks associated not only with tahini, but also with foods prepared from it, such as hummus.

4. The Ecology of Salmonella in Tahini and Tahini-Based Products

4.1. Salmonella and Sesame Seeds

Sesame seeds are cultivated from the sesame plant (Sesamum indicum). They are used as cooking and baking ingredients. Their high oil content (approximately 50% of the seed’s weight) makes them a valuable source of oil for cooking, cosmetic, and pharmaceutical applications [21]. Over 95% of the world’s sesame seed crop is produced in Africa (43%) and Asia (53%), with worldwide production estimated at seven million metric tonnes. Sudan, Myanmar, the United Republic of Tanzania, and India were the largest producers in 2020 [22]. Many countries, including Canada, do not produce sesame seeds and, therefore, rely on imported sesame seeds to produce tahini and tahini-based products [22]. Approximately 70–75% of the sesame seeds used in the United States are imported, with a few southern states producing seeds domestically [23][24].
S. indicum is a flowering annual that grows in areas with an annual rainfall of 625–1100 mm and temperatures of 27 °C and higher [25]. The sesame plant has an extensive root system and favours well-drained fertile soils with a neutral pH. The fruit of a sesame plant is a capsule that contains multiple seeds. Once the seeds are ripe, the capsule splits open and the seeds are released. These shattering cultivars of sesame seeds are largely harvested by hand. Non-shattering variants have been developed and are more amenable to mechanical harvesting [24]. Excess water, rain, and wind can promote shattering and decrease the yield of the seeds.
Contamination of the sesame seed plant can occur at the preharvest stage. Salmonella may be present in the soil, irrigation water, or in fertilizer. Droppings from wild animals carrying Salmonella are another potential source of the pathogen [26]. After harvest, sesame seeds are dried to an aw of 0.5 [27]. Drying the seeds is a critical step in the production process. It is carried out in open areas that can be exposed to dust and aerosols [28][29]. Wet conditions can complicate the drying process as the size and shape of seed prevents aeration and may prolong the time the seeds are exposed to atmospheric elements.
Many Salmonella serovars have been recovered from sesame seeds and include Typhimurium DT104, Offa, Tennessee, Poona [21], Montevideo, Stanleyville, Tilene [30], Amsterdam, Anatum, Bareilly, Charity, Cubana, Gaminara, Tennessee, Hvittingfoss, Kentucky, S. enterica ssp. diarizonae [31], Weltevreden, Newport, Mbandaka, Anatum, Senftenberg, Give, Tennessee, 3, 10: b:-, Havana, Kentucky, Bonn, Cerro, Glostrup, Idikan, Llandoff, Pottsdam, Westminister, S. enterica ssp. arizonae, and S. bongori 48:z4,z24:- [32]. This diversity suggests multiple sources of contamination. Some of these serovars are known clinically and have been implicated in previous outbreaks linked to low-moisture foods (e.g., Montevideo, Tennessee, Newport, and Poona) [6][33][34][35], whereas others are rarely seen in clinical settings and their virulence properties are unknown (e.g., Tilene, Charity, Idikan, and Amsterdam). It is also not known whether these serovars have geographic significance or unique physiologies that allow them to survive in the sesame seed production environment.
The presence of Salmonella in sesame seeds varies widely. Surveys of sesame seeds from a variety of locations have shown Salmonella prevalence ranging from none detected in 526 samples to 27% out of 359 samples using an analytical unit of 25 g [28]. Studies with enumeration data indicated low levels of contamination with concentrations ranging from 0.06 to 4 MPN/100 g [23] and 360 MPN/100 g [27]. No relationship was observed between Salmonella presence and counts of total aerobic bacteria, coliforms, and/or E. coli [27][31][36][37]. Surveillance studies of sesame seeds for import into the United States over ten years showed a relatively high prevalence in imported seeds (8–11%) compared to seeds that were collected from domestic retail establishments in the USA (no detections). This shows that postprocessing interventions may be able to control the levels of Salmonella on sesame seeds [23][31][32]. These studies also demonstrated a high degree of batch-to-batch variation with respect to Salmonella presence, indicating the pathogen is not distributed homogenously within the product, and may require larger sample sizes for reliable detection.

4.2. Salmonella and Tahini

Tahini is the paste produced from ground sesame seeds, which has a high-fat (57–65%) and low-moisture content (<1%) [38]. On average, tahini has a water activity (aw) of 0.16 and a pH of 5.9 [39][40]. Tahini is considered a ready-to-eat product, which is stored at ambient temperature with a long shelf life (up to two years) [16]. Traditional to Middle Eastern and Mediterranean cuisine, tahini is used as an ingredient in the preparation of many other ready-to-eat products, such as hummus, baba ghanoush, mutabbal, tarator sauce, and various salad dressings, sauces, and dips [29][41]. These foods pose an additional risk for acquiring salmonellosis since their high-moisture content could amplify Salmonella levels should it be present in any of the raw ingredients.
Countries that are key global exporters of tahini include Lebanon, Syria, Egypt, Greece, and Israel [42]. Tahini is gaining popularity in North American and European markets [43]. As an example, 6.8% of the respondents who participated in Foodbook, a Canadian population-based telephone survey, reported the consumption of tahini, halva, and other products made from sesame seeds in the last 7 days [44]. However, this may be an underestimation since multi-ingredient foods, such as sandwiches and salads, may contain tahini as an ingredient that consumers are not aware of [45].
Tahini is typically obtained by milling cleaned, dehulled, and roasted sesame seeds [29][39]. The process includes multiple steps: an initial soak step, a dehulling step, a draining and drying step, a thermal treatment step (roasting), followed by grinding [46]. Some manufacturers might pasteurize the finished product, although it is not known how widespread this practice is and what parameters are being used [47][48]. Other variations in the process have been reported [21][47]. The soaking step is of critical importance for process control. It can be carried out in water or salt water for 12 to 24 h. If Salmonella is present on the initial lot of seeds, this practice can amplify the level of Salmonella by up to 3 logs prior to the roasting and grinding of seeds [46].
The majority of tahini sold for consumption is made from roasted seeds. Raw tahini, made from unroasted or lightly roasted sesame seeds, represents a small percentage of all tahini sold (e.g., 4.1% in Canada) [29][49]. Roasting parameters are variable and expected to differ among producers. Different roasting temperatures and times (110 to 170 °C for 40 to 180 min), as well as heat-treatment processes (steam and dry heat roasting treatments), have been reported [50][51][52].
Studies have demonstrated that the roasting of sesame seeds can reduce Salmonella levels [46][52]. Torlak and colleagues reported that roasting temperatures and times of 100 °C for 60 min, 130 °C for 50 min, and 150 °C for 30 min were sufficient to generate a minimum of a 5-log reduction in the initial levels of Salmonella artificially inoculated onto sesame seeds. The authors noted a period of rapid decline within the first 10 min of roasting, followed by a lower rate of reduction. This first ten minutes of heating corresponded to a reduction in the seeds’ aw, from 0.98 to 0.14. This suggests that during the roasting process, the surviving population of Salmonella cells exhibit an increase in heat resistance as the moisture of the seeds decreases [52].
Similarly, Zhang and colleagues inoculated sesame seeds with 8.5 log CFU/g of Salmonella, then soaked and dried them to an aw of 0.90. When these seeds were roasted at 130 °C using an air-forced oven, Salmonella populations decreased below the detection limit (1.7 log CFU/g) within 10 min. However, when the sesame seeds had an aw of 0.45 before roasting at the same temperature, the decline in cell populations took longer with an approximate 5-log reduction after 60 min, meaning that 3.5 log CFU/g remained on the seeds after this roasting process [46].
If Salmonella survives the roasting process, it is likely to remain viable throughout the shelf life of the product. Therefore, tahini and tahini-based products may become contaminated by Salmonella through insufficient or inadequate roasting of contaminated sesame seeds [46][52]. In addition, it is crucial to avoid cross-contamination after the roasting process. Salmonella cross-contamination in low-moisture foods has been traced to factors such as poor sanitation practices, poor equipment design, improper maintenance, and poor ingredient control [26][53].
Guidance documents for manufacturers of tahini and tahini-based products describing Salmonella control practices are available. These documents include the Code of Hygienic Practice for Low-Moisture Foods, CXC 75-2015 [12]; the Hazard Analysis and Critical Control Point Generic Models for Some Traditional Foods: a Manual for the Eastern Mediterranean Region [39]; and the Control of Salmonella in Low-Moisture Foods [53]. The Grocery Manufacturers Association (GMA) of the United States listed the following seven control elements against Salmonella contamination: prevent ingress or spread of Salmonella in the processing facility, enhance the stringency of hygiene practices and controls in the Primary Salmonella Control Area, apply hygienic design principles to building and equipment design, prevent or minimize growth of Salmonella within the facility, establish a raw materials/ingredients control program, validate control measures to inactivate Salmonella, and establish procedures for verification of Salmonella controls and corrective actions [53].
Published Salmonella prevalence levels in tahini from Canada, Germany, and the Middle East ranged from 0.4% to 20% [21][47][54]. As with sesame seeds, no relationship was observed between Salmonella presence and total aerobic mesophile/coliform/E. coli counts. A targeted survey performed in Canada from 2010 to 2014 found a Salmonella prevalence of 0.4% (out of 2,315 samples) in tahini. All positive samples were from tahini imported from Middle Eastern countries (i.e., Lebanon, Syria, and Israel), even though almost half of the products tested were domestically produced [49][55][56]. It is not clear whether the difference between imported and domestic products was due to the origin of the raw ingredients, or to differences in production practices. A study by Alaouie and colleagues comparing tahini made from traditional or more automated methods did not find a difference in Salmonella prevalence among the sampled products [47]. Serovars found in tahini include Amsterdam, Havana, Montevideo, Senftenberg [49][55][56], Typhimurium DT 104 [21], Hadar, Agona, Einsbuettel, and Ubrecht [54].

4.3. Salmonella and Halva

Halva is a confectionary widely consumed in the Middle East and Mediterranean. It is primarily a mixture of tahini and sugar with the following specifications: ≥24% fat, ≥8.5% protein, ≤55% sucrose, ≤2% fibre, and ≤3% water [57]. An analysis of halva produced in a Greek facility indicated an aw of 0.18 and pH of 6 [57]. Halva is made by mixing tahini with a heated, acidified sugar syrup. The syrup contains a high concentration of glucose, citric or tartaric acid, and soapwort root extract (Saponaria officinalis). The syrup is heated to 120–140 °C prior to mixing with the tahini [21][57]. Nuts, cocoa, and other flavourings can be added before portioning and packaging [58]. These additives, particularly cocoa and pistachio, can act as vehicles for the introduction of Salmonella into the product. As an illustration, halva products containing cocoa and/or pistachio demonstrated increased Enterobacteriaceae/coliform/E. coli counts compared to plain halva [58][59]. There was no relationship between the levels of Enterobacteriaceae/coliform/E. coli and Salmonella presence, suggesting these counts can be used as indicators of overall process hygiene as opposed to indicators of pathogen presence. Reported Salmonella prevalences in halva ranged from no detections to 11.3%, with Typhimurium DT 104, Poona, and a monophasic strain from serogroup B isolated [21].

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Subjects: Microbiology
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Geneviève Coulombe
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Sandeep Tamber
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Entry Collection: Gastrointestinal Disease
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