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Review

Salmonella enterica Outbreaks Linked to the Consumption of Tahini and Tahini-Based Products

by
Geneviève Coulombe
1 and
Sandeep Tamber
2,*
1
Microbiology Evaluation Division, Bureau of Microbial Hazards, Food Directorate, Health Canada, 251 Sir Frederick Banting Driveway, Ottawa, ON K1A 0K9, Canada
2
Microbiology Research Division, Bureau of Microbial Hazards, Food Directorate, Health Canada, 251 Sir Frederick Banting Driveway, Ottawa, ON K1A 0K9, Canada
*
Author to whom correspondence should be addressed.
Microorganisms 2022, 10(11), 2299; https://doi.org/10.3390/microorganisms10112299
Submission received: 14 October 2022 / Revised: 15 November 2022 / Accepted: 17 November 2022 / Published: 19 November 2022
(This article belongs to the Special Issue Foodborne Pathogens: Detection Methods, Food Safety, and Public Health)
Review Reports Versions Notes

Abstract

:
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. This review offers the Canadian perspective on the issue of Salmonella in tahini and tahini-based products. A summary of several recent food product recalls and foodborne outbreaks related to the presence of Salmonella in tahini and tahini-based products such as halva are presented. The properties of the food vehicles, their production practices, and potential routes of contamination are discussed. Particular focus is placed on the ecology of Salmonella in the tahini production continuum, including its survival characteristics and response to intervention technologies.

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].
In 2004, the World Health Organization’s International Food Safety Authorities Network (INFOSAN) identified sesame-based foods (i.e., tahini and halva from the Middle Eastern region) as an unusual food source for Salmonella contamination [7]. To date, twenty salmonellosis outbreaks linked to the consumption of tahini and tahini-based products (e.g., halva and hummus) have been identified worldwide (Table 1) [8]. Overall, these outbreaks resulted in 1662 salmonellosis cases, 88 hospitalisations, and 1 death.
In Canada, from 2011–2021, tahini and tahini-based products (e.g., halva and hummus) have been subject to multiple recalls and updated recalls due to the presence of Salmonella [9]. In Canada, salmonellosis illnesses linked to the consumption of tahini imported from Israel and hummus were identified in 2018 and 2020, respectively (Table 1) [10]. In 2019, eight Canadian cases were identified by whole genome sequencing (WGS) as being part of a multicountry outbreak linked to tahini and halva imported from Syria (Table 1). Indeed, tahini, halva, and other products made from sesame seeds were labelled, by the Public Health Agency of Canada (PHAC), as being in the “high-risk” food category due to their potential of being contaminated by Salmonella [11].
This review offers the Canadian perspective on the issue of Salmonella in tahini and tahini-based products and provides an overview of the available literature concerning the ecology of Salmonella in sesame seeds, tahini, and halva. Intrinsic properties of sesame seeds, tahini, and halva will be summarized, along with extrinsic factors that can lead to contamination along the processing continuum. Features of the pathogen allowing for long-range survival, mitigation strategies, and areas for further research will also be covered.
Table
Table 1. Known salmonellosis outbreaks linked to tahini and tahini-based products, 1995–2022.
Table 1. Known salmonellosis outbreaks linked to tahini and tahini-based products, 1995–2022.
YearProductsSalmonella SerovarCountryCases (Hospital/
Deaths)		Country of OriginReferences
11995TahiniBrandenburgUSA137NA[12]
22001HalvaTyphimurium DT104Australia, New Zealand, Sweden, Norway62Turkey[13,14,15,16,17]
32002TahiniMontevideoAustralia55Egypt[18]
42003TahiniMontevideoNew Zealand10Lebanon[18]
52003TahiniMontevideoAustralia3Lebanon[18,19]
62004Hummus, eggplant dipTyphimurium DT197Australia173 (25)NA[8]
72007HummusHeidelbergUSA802 (29)NA[20]
82007HummusHeidelbergUSA11NA[8]
92007HummusMuenchenUK6NA[21]
102010HummusTyphimuriumAustralia45 (8)NA[22]
112011Tahini, hummusBovismorbificansUSA23Lebanon[23,24]
122012TahiniMontevideo, Mbandaka, MaastichtNew Zealand16 (3)Turkey[25]
132013TahiniMontevideo, MbandakaUSA16 (1/1)Turkey[24,26]
142016–2017Tahini, sesame seedsVari (11:z41:e,n,z15)Germany, Czech Republic, Luxembourg, UK, Greece47 (12)Greece[27]
152017HummusThompsonUSA13NA[24]
162018Tahini, hummusConcordIsrael, USA45Israel[28]
172019TahiniConcordUSA6 (1)Israel[29]
182019HummusSalmonellaUSA9NA[30]
192020HummusSalmonellaCanada45 (9)NA[31]
202019–2022Tahini, halvaMbandaka, Havana, Amsterdam, Orion, Kintambo, SenftenbergGermany, Sweden, Norway, Netherlands, Canada, USA, New Zealand138 (24)Syria[32,33]

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 [34,35].
Estimates of the infectious dose for Salmonella range from 100 to 1011 cells [36,37]. 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 [38,39]. 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 [4,40,41,42].
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 [18,25]. 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 (Outbreak #1, Table 1). 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 (Outbreak #2, Table 1). 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 (Outbreaks #3 to 5, Table 1). Of the twenty outbreaks listed in Table 1, country-of-origin information is available for eleven. These countries include Egypt, Greece, Israel, Lebanon, Syria, and Turkey as the source of the tahini and tahini-based products. The source of the sesame seeds, in most cases, remains unknown.
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 (Outbreak #14, Table 1). The investigation into this outbreak indicated that cross-contamination likely occurred at the Greek manufacturing facility during the production of tahini [27].
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 (Outbreak #20 in Table 1). 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 [32].
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 [10]. In 2020, a localized outbreak linked to hummus involved a restaurant and a food truck from a single region (Outbreak #19, Table 1). 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 [13]. 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 [43]. Many countries, including Canada, do not produce sesame seeds and, therefore, rely on imported sesame seeds to produce tahini and tahini-based products [43]. Approximately 70–75% of the sesame seeds used in the United States are imported, with a few southern states producing seeds domestically [44,45].
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 [46]. 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 [45]. 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 [47]. After harvest, sesame seeds are dried to an aw of 0.5 [48]. 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 [49,50]. 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 [13], Montevideo, Stanleyville, Tilene [51], Amsterdam, Anatum, Bareilly, Charity, Cubana, Gaminara, Tennessee, Hvittingfoss, Kentucky, S. enterica ssp. diarizonae [52], 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:- [53]. 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) [6,54,55,56], 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 (Table 2). 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 [49]. Studies with enumeration data indicated low levels of contamination with concentrations ranging from 0.06 to 4 MPN/100 g [44] and 360 MPN/100 g [48]. No relationship was observed between Salmonella presence and counts of total aerobic bacteria, coliforms, and/or E. coli [48,52,57,58]. 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 [44,52,53]. 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%) [69]. On average, tahini has a water activity (aw) of 0.16 and a pH of 5.9 [70,71]. Tahini is considered a ready-to-eat product, which is stored at ambient temperature with a long shelf life (up to two years) [18]. 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 [50,72]. 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 [73]. Tahini is gaining popularity in North American and European markets [74]. 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 [75]. 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 [11].
Tahini is typically obtained by milling cleaned, dehulled, and roasted sesame seeds [50,70]. 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 [76]. Some manufacturers might pasteurize the finished product, although it is not known how widespread this practice is and what parameters are being used [61,77]. Other variations in the process have been reported [13,61]. 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 [76].
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) [50,62]. 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 [78,79,80].
Studies have demonstrated that the roasting of sesame seeds can reduce Salmonella levels [76,80]. 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 [80].
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 [76]. This article indicates that the lethality of the roasting process to Salmonella present on the sesame seeds depends on the starting aw.
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 [76,80]. 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 [47,81].
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 [39]; the Hazard Analysis and Critical Control Point Generic Models for Some Traditional Foods: a Manual for the Eastern Mediterranean Region [70]; and the Control of Salmonella in Low-Moisture Foods [81]. 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 [81].
Published Salmonella prevalence levels in tahini from Canada, Germany, and the Middle East ranged from 0.4% to 20% (Table 2) [13,60,61]. 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 [62,63,64]. 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 [61]. Serovars found in tahini include Amsterdam, Havana, Montevideo, Senftenberg [62,63,64], Typhimurium DT 104 [13], Hadar, Agona, Einsbuettel, and Ubrecht [60].

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 [68]. An analysis of halva produced in a Greek facility indicated an aw of 0.18 and pH of 6 [68]. 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 [13,68]. Nuts, cocoa, and other flavourings can be added before portioning and packaging [65]. 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 [65,67]. 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 (Table 2) [13].

5. Survival of Salmonella in Sesame Seeds, Tahini, and Halva

5.1. Survival Studies

Water activity (aw) is a key determinant for microbial growth as it is a measure of the amount of water available to carry out essential metabolic functions. Salmonella requires a minimal aw of 0.93 to actively grow and reproduce [36]. Therefore, it cannot grow in sesame seeds, tahini, or halva, but it can survive in these matrices for extended periods [47,82]. Studies on the survival of Salmonella in sesame seeds, tahini, and halva have shown survival periods ranging from at least 4 to 12 months [48,68,76,80,83,84]. These studies highlight the public health risk associated with the presence of Salmonella in these foods. Even after prolonged storage, the pathogen remains viable, and therefore, capable of causing disease.
The manner in which tahini and halva are stored appear to have an effect on Salmonella survival. Increased survival was noted when tahini and halva were stored at refrigeration temperatures as opposed to room temperature [80,84]. It has been proposed that the increased survival at lower temperatures may be linked to changes in the composition of the bacterial membrane that would result in lower rates of permeability [83]. It is also possible that the shift in temperature changes the organization of the lipid–water interface of the tahini/halva in a manner that supports bacterial survival. Work carried out with peanut butter and margarine has shown that the size of the lipid–water droplets can influence microbial survival, with finer droplets presenting more of a hurdle [85,86]. Whether this relationship applies to tahini and halva remains to be investigated.
Other factors that can affect survival include additives such as acids or essential oils derived from spices, both of which led to marginal reductions in Salmonella in tahini stored at 10, 25, or 37 °C for 1 month [72,87]. Product packaging can also affect survival, as higher levels of Salmonella were recovered from vacuum-sealed halva after eight months of storage compared to air-sealed packages [68].

5.2. Survival Strategies

Salmonella employs a number of adaptations to survive in low-moisture environments [47,82]. Upon inoculation in peanut oil, cells enter a partially dormant state where less than 5% of their genome is transcribed (compared to 78% of cellular genomes cultured in Luria broth) [88]. Among the genes that are transcribed in peanut oil are stress response genes as well as the global regulators sigma D and sigma E, suggesting that in this state, persistence and survival take precedence over growth and metabolism. Upon prolonged storage, Salmonella cells can become metabolically dormant where they are viable but not culturable (VBNC) until exposed to favourable growth conditions, at which point they can resuscitate and resume metabolic and other accessory functions such as pathogenesis.
Changes to the cell structure and cell surface have been reported in low-aw conditions. Salmonella cells grown in high NaCl, sucrose, or glycerol form long filaments due to an inhibition of cell septation. Similarly, high osmolarity conditions lead to an alteration of the OmpC/OmpF porin ratios in the outer membrane that lead to altered permeability rates. Permeability can also be affected through increased synthesis of unsaturated fatty acids via FabA [89]. Osmotic pressure is maintained through the upregulation of genes encoding osmoprotectant synthesis and transport proteins (ProP, ProU, and OsmU), as well as increased potassium influx through the Kdp transporter [88]. However, it is not clear if these adaptations extend to sesame seeds, tahini, and halva since the method of desiccation can influence the nature of the bacterial response [82].
Salmonella cells that are tolerant to desiccation undergo a number of physiological changes that may render them less susceptible to other food control measures such as heating, acidification, and/or treatment with biocides [47]. For example, Salmonella cells inoculated onto sesame seeds at a starting aw of 0.45 exhibited a slower rate of decline compared to cells on seeds with an aw ≥ 0.95 when the seeds were roasted at 130 °C [76].
There may be a relationship between biofilm formation and desiccation resistance, since cells that form biofilms have increased resistance to many ecological stresses [90]. Cells that overproduce the biofilm extracellular matrix components curli and cellulose have an increased tolerance to desiccation stress [91]. Similarly, mutants deficient in the production of an extracellular matrix have reduced desiccation tolerance [92]. However, it is not clear if this relationship holds in high-fat, low-aw food systems and is an area that requires further study.
The ability of Salmonella to tolerate desiccation varies from strain to strain. Norberto and colleagues reported in a study of 37 Salmonella strains belonging to 16 serovars log reductions ranging from 0.6 to 2.7 when inoculated in dry soybean meal and stored at 25 °C for 18 h [93]. There were considerable differences within strains of the same serovar; for example, the respective range of log reductions was 0.9, 1.1, and 1.3 for S. enterica serovars Ohio, Montevideo, and Havana, respectively [93]. The nature of these differences is not clear, but may reflect differences in gene presence or gene expression that can impact the response to desiccation.

6. Control of Salmonella in Sesame Seeds, Tahini, and Tahini-Based Products

Both thermal and nonthermal treatments of low-moisture foods or their raw materials can be used to control the presence of Salmonella. In recent years, there has been intensive research efforts into postproduction lethality treatments of tahini and tahini-based products. The intent is to eliminate Salmonella without compromising the quality properties of the food products. Some of the inactivation treatments tested on sesame seeds, tahini, or halva are presented below.

6.1. Thermal Treatment

Roasting of the sesame seeds is a key step to control Salmonella during the manufacturing of tahini, as described in detail in Section 4.2.
Some manufacturers may also include a thermal treatment applied to the tahini as a final step [77]. Szpinak and colleagues evaluated the efficacy of a final heat treatment by testing the survival of Salmonella ser. Typhimurium in tahini treated at temperatures of 70 °C, 80 °C, and 90 °C. Regardless of the test conditions, the Salmonella cells had a high rate of survival with a maximal reduction of 3 log CFU/mL after one hour at 90 °C. The inactivation profiles demonstrated a rapid decline in the first two minutes of treatment, followed by a tailing curve at all tested temperatures, suggesting the applied thermal treatments were only able to inactivate a subset of the Salmonella population [77].

6.2. Natural Antimicrobials

Some studies evaluated the impact of incorporating natural antimicrobials into tahini in order to control Salmonella [72,87,94]. Ten plant essential oils were tested for their antimicrobial activity against four different Salmonella serotypes (Typhimurium, Aberdeen, Cubana, and Paratyphi A) using a disc diffusion assay method [87]. In that study, thyme oil and cinnamon oil showed the highest antimicrobial activity. When added to tahini, 2.0% cinnamon oil reduced the numbers of Salmonella between 2.4 and 2.8 log CFU/mL, whereas 2.0% thyme oil led to a reduction between 2.2 and 3.3 log CFU/mL by 28 days, depending on the storage temperature (10 °C, 25 °C, or 37 °C). However, the addition of essential oil extracts reduced the quality and consumer acceptability of the tahini, as assessed by a sensory panel [87]. Another study investigated the use of 3% oregano oil in tahini, which led to a reduction of 1.4 and 0.80 log CFU/g after 7 days at 25 °C and 4 °C, respectively, compared to the control [94].
The antibacterial effects of organic acids, such as acetic and citric acids, have also been tested in tahini. The addition of acetic and citric acids at a concentration of 0.5% reduced Salmonella ser. Typhimurium by 2.7–4.8 log CFU/mL and 2.5–3.8 log CFU/mL, respectively, in tahini after 28 days at tested temperatures of 10 °C, 21 °C, and 37 °C [72]. Similarly, Xu and colleagues confirmed a reduction in Salmonella levels with the use of 0.5% citric acid (0.8 log CFU/g reduction after 7 days at 4 °C) [94].
Antimicrobial substances, such as metals, chemicals, essential oils, enzymes, and bacteriocins, can also be used in packaging materials [95]. More research is needed to evaluate their potential effect on Salmonella spp. in tahini and tahini-based products.

6.3. Irradiation

Ionizing radiation can effectively eliminate microbes that cause foodborne illness, including Salmonella. Three types of radiation can be used on bulk or packaged products: gamma rays, X-rays, and electron beams [96]. D’Oca and colleagues evaluated the inactivation of Salmonella ser. Montevideo by gamma irradiation of sesame seeds. Their results showed that the use of 5 kGy was able to reduce Salmonella counts by 5.53 log CFU/g on sesame seeds [51]. The inactivation of Salmonella using gamma irradiation was also tested in tahini [97] and halva [98]. In halva, an irradiation dose of 4.0 kGy resulted in a reduction of 2.1 log CFU/g of Salmonella, whereas in tahini, an irradiation dose of 2.0 kGy led to a reduction of 4.7 log CFU/g of Salmonella [97,98]. In tahini, the irradiation dose of 2.0 kGy did not affect the physical and chemical properties of the product (i.e., color, peroxide, p-anisidine, and acid values) [97].

6.4. Energy-Based Technologies

Two recent studies tested energy-based technologies on sesame seeds and tahini [99,100]. Xu and colleagues tested the use of radiofrequency heating, in combination with cinnamon oil vapor, on sesame seeds. A radio frequency heating at 80 °C for 5 min combined with 0.83 μL/mL of cinnamon oil vapor achieved a reduction of greater than 5 log CFU/g of Salmonella ser. Montevideo on sesame seeds. No synergistic effect of the combined treatments was observed, nor was there any reduction in the quality of the seeds [100].
The efficiency of 2450 MHz microwave heating at 220, 330, 440, 550, and 660 W for the inactivation of Salmonella was assessed in tahini. Salmonella reductions ranging from 3.6 to 4.7 log CFU/g were observed after treatment. After two minutes of treatment, the core temperatures of the tahini samples reached, 45 °C, 70 °C, 103 °C, 119 °C, and 144 °C at 220, 330, 440, 550, and 660 W, respectively. The authors noted that microwave heating did not affect acid, peroxide, p-anisidine, or color values of the tahini up to 90 °C [99].

6.5. Fumigation and Gas Treatment

Fumigants, such as ethylene oxide and propylene oxide, have shown to be effective for achieving significant reductions in microbial populations in low-moisture foods. More precisely, ethylene oxide is used to treat spices, whereas propylene oxide is used with a variety of foods such as nuts, spices, cocoa beans, and dried fruits [101].
In some countries, including the European Union, the use of ethylene oxide in foods is not permitted. In recent years, multiple recalls of sesame seed products due to the presence of ethylene oxide residues occurred in the European Union. It is believed that ethylene oxide was used for fumigating sesame seeds to eradicate Salmonella contamination [102].
Golden and colleagues tested the use of chlorine dioxide (ClO2) to reduce Salmonella levels on sesame seeds. A treatment with 500 mg ClO2/kg reduced the number of Salmonella from 7.6 log CFU/g to 4.9 log CFU/g on sesame seeds [103].

7. Monitoring

There are many challenges associated with the detection of Salmonella in sesame seeds, tahini, and tahini-based products. The low numbers of pathogen and heterogeneous distribution patterns necessitates large sample sizes, often beyond the capacity of many food-testing laboratories [104]. Further, the physiological state of Salmonella in the low-moisture food matrix requires consideration to prevent false-negative results. As an adaptation to the low-moisture environment, Salmonella cells may become injured, enter a period of dormancy (such as a viable but not culturable state), or adopt a filamentous shape [105,106]. Primary enrichment in a nonselective broth encourages cells to recover from these states and multiply to detectable levels. Approaches such as the addition of protectants or applying slower rates of rehydration to the primary enrichment may be employed to prevent cytolysis and increase the level of viable Salmonella [107,108]. Rapid methods that forgo secondary enrichment and/or plating in favour of molecular methods to detect Salmonella such as PCR should be used in conjunction with a primary enrichment step [104]. The requirement for primary enrichment often delays the time to result, and further research is required to understand how the enrichment period can be optimized for low-moisture foods. Given the issues with product testing, process and environmental monitoring are essential to ensure the hygiene of the tahini manufacturing process [109].

8. Areas for Further Research

In the course of preparing this review, the following knowledge gaps concerning Salmonella and tahini were identified. Research directed in these areas can provide information required to mitigate the public health risks associated with the presence of Salmonella in tahini and tahini-based products:
  • Understanding the ecology and potential virulence of Salmonella serovars associated with sesame seeds, tahini, and tahini-based products;
  • Knowledge of the response of sesame and tahini-associated serovars, and whether findings from different serovars can be generalized to the genus;
  • Survival of Salmonella in tahini and other colloidal foods, particularly the impact of rheological and physical properties (i.e., particle size);
  • Salmonella adaptations to high-fat, low-moisture foods such as tahini (e.g., biofilms, filaments, viable but not culturable) and the potential impact on detection and lethality treatments;
  • The impact of interventions, alone and in combination, throughout the tahini manufacturing process, particularly at the seed soaking and roasting steps;
  • Salmonella response in commercial settings to typical sesame seed roasting parameters, in order to understand the physiology of cells that survive the roasting process;
  • Improved traceability and environmental/process monitoring of sesame seeds, tahini, and tahini-based products to allow for a more detailed root cause analysis of food safety incidents;
  • Salmonella growth dynamics during primary enrichment to improve detection and enumeration methods, with an emphasis on reducing the time to result.

9. Conclusions

The issue of Salmonella in tahini and tahini-based products is one of global concern. The tahini production continuum from sesame seed to consumption is one that transcends multiple borders, and requires international cooperation for effective management, trace-back, and source attribution. Several features of the Salmonella–tahini relationship make it an intractable food–pathogen combination as demonstrated by the spate of recent food safety incidents associated with it. The long shelf life and the ready-to-eat nature of tahini make it an ideal vehicle for a long and sustained exposure to Salmonella. Further, the high fat, low-moisture environment of tahini improves Salmonella survival and resiliency to a variety of lethality treatments. Given the low infectious dose of Salmonella, complete elimination from a batch of contaminated tahini would be required to prevent illness, a goal that is difficult to achieve in this food matrix.
The difficulty in eliminating Salmonella to safe levels in tahini underscores the importance of preventing contamination. For many tahini producers, roasting is the only lethal step applied in the manufacturing process. A validated roasting procedure with strict ingredient and parameter control is key. Similarly, given the high potential for contamination after roasting, process verification and environmental monitoring of the production facility is important. Correlations between total aerobic mesophile/Enterobacteriaceae/coliform/E. coli counts and Salmonella presence have not been observed, but enumeration of the former groups can provide information on the hygiene of the production process. Verification and monitoring of the entire production continuum, from sesame seed production to tahini distribution, may not be possible given the reliance on imported products and the complexity of supply chains. This complexity also complicates food safety investigations and root cause analyses in the event of food safety incidents. Therefore, it is important for the implicated countries to adhere to a set of internationally agreed-upon standards and procedures to ensure the safe manufacture and consumption of this global food product.

Author Contributions

G.C. and S.T.: conceptualization; writing—original draft preparation, review, and editing. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Acknowledgments

The authors would like to thank Alex Gill and Angela Catford for their critical review of the manuscript and Mariola Mascarenhas (Public Health Agency of Canada) for her assistance with compiling the data included in Table 1.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Majowicz, S.E.; Musto, J.; Scallan, E.; Angulo, F.J.; Kirk, M.; O’Brien, S.J.; Jones, T.F.; Fazil, A.; Hoekstra, R.M.; International Collaboration on Enteric Disease “Burden of Illness” Studies. The Global Burden of Nontyphoidal Salmonella Gastroenteritis. Clin. Infect. Dis. 2010, 50, 882–889. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  2. WHO. Salmonella (Non-Typhoidal). Available online: https://www.who.int/news-room/fact-sheets/detail/salmonella-(non-typhoidal) (accessed on 13 October 2022).
  3. Painter, J.A.; Hoekstra, R.M.; Ayers, T.; Tauxe, R.V.; Braden, C.R.; Angulo, F.J.; Griffin, P.M. Attribution of Foodborne Illnesses, Hospitalizations, and Deaths to Food Commodities by using Outbreak Data, United States, 1998–2008. Emerg. Infect. Dis. 2013, 19, 407–415. [Google Scholar] [CrossRef] [PubMed]
  4. Lehmacher, A.; Bockemühl, J.; Aleksic, S. Nationwide outbreak of human salmonellosis in Germany due to contaminated paprika and paprika-powdered potato chips. Epidemiol. Infect. 1995, 115, 501–511. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  5. Niizuma, T.; Terada, K.; Matsuda, K.; Ogita, S.; Kataoka, N. Intrafamilial transmission of Salmonella oranienburg. Pediatr. Int. 2002, 44, 391–393. [Google Scholar] [CrossRef]
  6. Sheth, A.N.; Hoekstra, M.; Patel, N.; Ewald, G.; Lord, C.; Clarke, C.; Villamil, E.; Niksich, K.; Bopp, C.; Nguyen, T.-A.; et al. A National Outbreak of Salmonella Serotype Tennessee Infections From Contaminated Peanut Butter: A New Food Vehicle for Salmonellosis in the United States. Clin. Infect. Dis. 2011, 53, 356–362. [Google Scholar] [CrossRef] [PubMed]
  7. International Food Safety Authorities Network. Unusual sources of Salmonella; International Food Safety Authorities Network: Rome, Italy, 2004. [Google Scholar]
  8. Public Health Agency of Canada; (Ottawa, ON, Canada). Personal Communication., 2022.
  9. Canadian Food Inspection, Agency. Recalls and Safety Alerts. Available online: https://recalls-rappels.canada.ca/en (accessed on 13 October 2022).
  10. Canadian Food Inspection, Agency. Food Recall Warning—Achva and S&F Brand Tahini Products Recalled due to Salmonella. Available online: https://inspection.canada.ca/food-recall-warnings-and-allergy-alerts/2018-11-28/eng/1543459555660/1543459556655 (accessed on 13 October 2022).
  11. Tooby, M.; Morton, V.; Nesbitt, A.; Ciampa, N.; Thomas, M.K. Consumption of High-Risk Foods in the Canadian Population, Foodbook Study, 2014 to 2015. J. Food Prot. 2021, 84, 1925–1936. [Google Scholar] [CrossRef] [PubMed]
  12. Centers for Disease, Control and Prevention. 1995 Foodborne Outbreak Line Listing. Available online: https://www.cdc.gov/foodsafety/pdfs/1995_linelist.pdf (accessed on 13 October 2022).
  13. Brockmann, S. International outbreak of Salmonella Typhimurium DT104 due to contaminated sesame seed products—Update from Germany (Baden-Württemberg). Wkly. Releases (1997–2007) 2001, 5, 1699. [Google Scholar] [CrossRef]
  14. Aavitsland, P.; Alvseike, O.; Guérin, P.J.; Stavnes, T.L. International outbreak of Salmonella Typhimurium DT104—Update from Norway. Wkly. Releases (1997–2007) 2001, 5, 1701. [Google Scholar] [CrossRef]
  15. De Jong, B.; Andersson, Y.; Fisher, I.S.; A O’Grady, K.; Powling, J. International outbreak of Salmonella Typhimurium DT104—Update from Enter-net. Wkly. Releases (1997–2007) 2001, 5, 1705. [Google Scholar] [CrossRef]
  16. De Jong, B.; Andersson, Y.; Giesecke, J.; Hellström, L.; Stamer, U.; Wollin, R. Salmonella Typhimurium outbreak in Sweden from contaminated jars of helva (or halva). Wkly. Releases (1997–2007) 2001, 5, 1715. [Google Scholar] [CrossRef]
  17. Little, C. International outbreak of Salmonella Typhimurium DT104—Update from the United Kingdom. Wkly. Releases (1997–2007) 2001, 5, 1700. [Google Scholar] [CrossRef]
  18. Unicomb, L.E.; Simmons, G.; Merritt, T.; Gregory, J.; Nicol, C.; Jelfs, P.; Kirk, M.; Tan, A.; Thomson, R.; Adamopoulos, J.; et al. Sesame seed products contaminated with Salmonella: Three outbreaks associated with tahini. Epidemiol. Infect. 2005, 133, 1065–1072. [Google Scholar] [CrossRef] [PubMed]
  19. OzFoodNet Working, Group. Foodborne Disease Investigation across Australia: Annual Report of the Ozfoodnet Network, 2003. Commun. Dis. Intell. Q. Rep. 2004, 28, 359–389. [Google Scholar]
  20. Centers for Disease, Control and Prevention. Surveillance for Foodborne Disease Outbreaks—United States, 2007. Morb. Mortal. Wkly. Rep. 2010, 59, 973–979. [Google Scholar]
  21. Harker, K.S.; Lane, C.; Gormley, F.J.; Adak, G.K. National Outbreaks of Salmonella Infection in the UK, 2000–2011. Epidemiol. Infect. 2014, 142, 601–607. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  22. Torres, M.I.; Lewis, P.; Cook, L.; Cook, P.; Kardamanidis, K.; Shadbolt, C.; Campbell, B. An outbreak of Salmonella Typhimurium linked to a kebab takeaway shop. Commun. Dis. Intell. Q. Rep. 2012, 36, 101–106. [Google Scholar] [PubMed]
  23. Centers for Disease Control and Prevention. Multistate Outbreak Of salmonella serotype Bovismorbificans Infections Associated with Hummus and Tahini—United States, 2011. Morb. Mortal. Wkly. Rep. 2012, 61, 944–947. [Google Scholar]
  24. Centers for Disease Control and Prevention. National Outbreak Reporting System (NORS). Available online: https://wwwn.cdc.gov/norsdashboard/ (accessed on 13 October 2022).
  25. Paine, S.; Thornley, C.; Wilson, M.; Dufour, M.; Sexton, K.; Miller, J.; King, G.; Bell, S.; Bandaranayake, D.; Mackereth, G. An Outbreak of Multiple Serotypes of Salmonella in New Zealand Linked to Consumption of Contaminated Tahini Imported from Turkey. Foodborne Pathog. Dis. 2014, 11, 887–892. [Google Scholar] [CrossRef] [PubMed]
  26. Centers for Disease Control and Prevention. Salmonella Mbandaka Infections Linked to Tahini Sesame Paste. 2013. Available online: https://www.cdc.gov/salmonella/montevideo-tahini-05-13/ (accessed on 13 October 2022).
  27. European Food Safety Authority and European Centre for Disease Prevention and Control. Multi-Country Outbreak of New Salmonella enterica 11:Z41:E,N,Z15 Infections Associated with Sesame Seeds. Available online: https://www.ecdc.europa.eu/sites/default/files/documents/rapid-outbreak-assessment-salmonella-enterica-Greece-14-Jun-2017.pdf (accessed on 13 October 2022).
  28. Centers for Disease Control and Prevention. Salmonella Infections Linked to Tahini from Achdut Ltd. 2018. Available online: https://www.cdc.gov/salmonella/concord-11-18/index.html (accessed on 13 October 2022).
  29. Centers for Disease Control and Prevention. Salmonella Infections Linked to Karawan brand Tahini. Available online: https://www.cdc.gov/salmonella/concord-05-19/index.html (accessed on 13 October 2022).
  30. Maryland Department of, Health. Maryland Department of Health investigating Cluster of Salmonella Infections. 2019. Available online: https://health.maryland.gov/newsroom/Pages/Maryland-Department-of-Health-investigating-cluster-of-salmonella-infections.aspx (accessed on 13 October 2022).
  31. Lambton Public, Health. Salmonellosis Outbreak Investigation Closed Locally. Available online: https://lambtonpublichealth.ca/salmonellosis-outbreak-investigation-closed-locally/ (accessed on 13 October 2022).
  32. European Food Safety Authority. Multi-Country Outbreak of Multiple Salmonella enterica Serotypes Linked to Imported Sesame-Based Products. Available online: https://www.efsa.europa.eu/en/supporting/pub/en-6922 (accessed on 13 October 2022).
  33. Ministry of Health. Monthly Notifiable Disease Surveillance Report—July 2022. Available online: https://surv.esr.cri.nz/index.php?we_objectID=5232 (accessed on 13 October 2022).
  34. Centers for Disease, Control, and Prevention. Salmonella. Available online: https://www.cdc.gov/salmonella/general/index.html (accessed on 13 October 2022).
  35. U. S. Food and Drug Administration. Get the Facts about Salmonella. Available online: https://www.fda.gov/animal-veterinary/animal-health-literacy/get-facts-about-salmonella (accessed on 13 October 2022).
  36. D’Aoust, J.Y.; Maurer, J. Salmonella Species. In Food Microbiology: Fundamentals and Frontiers; Doyle, M.P., Beauchat, L.R., Montville, T.J., Eds.; AMS Press: Washington, DC, USA, 2007; pp. 187–236. [Google Scholar]
  37. United States Food and Drug Administration. Bad Bug Book. Available online: https://www.fda.gov/media/83271/download (accessed on 7 October 2021).
  38. Aviles, B.; Klotz, C.; Smith, T.; Williams, R.; Ponder, M. Survival of Salmonella enterica Serotype Tennessee during Simulated Gastric Passage Is Improved by Low Water Activity and High Fat Content. J. Food Prot. 2013, 76, 333–337. [Google Scholar] [CrossRef] [PubMed]
  39. Codex Alimentarius, Commission. Code of Hygienic PRACTICE for low-Moisture Foods CXC 75-2015. Available online: https://www.fao.org/fao-who-codexalimentarius/sh-proxy/en/?lnk=1&url=https%253A%252F%252Fworkspace.fao.org%252Fsites%252Fcodex%252FStandards%252FCXC%2B75-2015%252FCXC_075e.pdf (accessed on 13 October 2022).
  40. Greenwood, M.H.; Hooper, W.L. Chocolate bars contaminated with Salmonella napoli: An infectivity study. BMJ 1983, 286, 1394. [Google Scholar] [CrossRef] [Green Version]
  41. Kapperud, G.; Gustavsen, S.; Hellesnes, I.; Hansen, A.H.; Lassen, J.; Hirn, J.; Jahkola, M.; A Montenegro, M.; Helmuth, R. Outbreak of Salmonella typhimurium infection traced to contaminated chocolate and caused by a strain lacking the 60-megadalton virulence plasmid. J. Clin. Microbiol. 1990, 28, 2597–2601. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  42. Vought, K.J.; Tatini, S.R. Salmonella enteritidis Contamination of Ice Cream Associated with a 1994 Multistate Outbreak. J. Food Prot. 1998, 61, 5–10. [Google Scholar] [CrossRef] [PubMed]
  43. FAOSTAT. Crops and Livestock Products. Available online: https://www.fao.org/faostat/en/#data/QCL (accessed on 29 August 2022).
  44. Van Doren, J.M.; Blodgett, R.J.; Pouillot, R.; Westerman, A.; Kleinmeier, D.; Ziobro, G.C.; Ma, Y.; Hammack, T.S.; Gill, V.; Muckenfuss, M.F.; et al. Prevalence, level and distribution of Salmonella in shipments of imported capsicum and sesame seed spice offered for entry to the United States: Observations and modeling results. Food Microbiol. 2013, 36, 149–160. [Google Scholar] [CrossRef]
  45. Agricultural Marketing Resource Center. Sesame Profile. Available online: https://www.agmrc.org/commodities-products/grains-oilseeds/sesame-profile (accessed on 6 October 2022).
  46. Terefe, G.; Adugna, W.; Muez, B.; Hagos, T. Sesame Production Manual; Ethiopian Institute of Agricultural Research Embassy of the Kingdom of the Netherlands: 2012; ISBN 978-99944-53-80-8. Available online: https://www.researchgate.net/publication/301771324_Sesame_production_manual (accessed on 18 November 2022).
  47. Podolak, R.; Enache, E.; Stone, W.; Black, D.G.; Elliott, P.H. Sources and Risk Factors for Contamination, Survival, Persistence, and Heat Resistance of Salmonella in Low-Moisture Foods. J. Food Prot. 2010, 73, 1919–1936. [Google Scholar] [CrossRef] [PubMed]
  48. Juarez Arana, C.D.; Peniche, R.A.M.; Martinez, M.G.; Iturriaga, M.H. Microbiological Profile, Incidence, and Behavior of Salmonella on Seeds Traded in Mexican Markets. J. Food Prot. 2021, 84, 99–105. [Google Scholar] [CrossRef]
  49. Compaore, M.K.A.; Yougbara, V.M.; Dembala, R.; Nikiama, F.; Elie, K.; Barro, N. Retrospective Study of the Contamination of Exported Sesame by Salmonella Species from 2007 to 2017 in Burkina Faso. Afr. J. Agric. Res. 2020, 16, 1141–1147. [Google Scholar]
  50. Lake, R.; King, N.; Cressey, P.; Gilbert, S. Risk Profile: Salmonella (Non typhoidal) in High Lipid Foods. Available online: https://www.mpi.govt.nz/dmsdocument/24248-Salmonella-non-typhoidal-in-high-lipid-foods-made-from-sesame-seeds-peanuts-or-cocoa-beans (accessed on 13 October 2022).
  51. D’Oca, M.C.; di Noto, A.M.; Bartolotta, A.; Parlato, A.; Nicastro, L.; Sciortino, S.; Cardamone, C. Assessment of Contamination of Salmonella spp. In Imported Black Pepper and Sesame Seed and Salmonella Inactivation by Gamma Irradiation. Ital. J. Food Saf. 2021, 10, 8914. [Google Scholar] [CrossRef]
  52. Zhang, G.; Hu, L.; Pouillot, R.; Tatavarthy, A.; Van Doren, J.M.; Kleinmeier, D.; Ziobro, G.C.; Melka, D.; Wang, H.; Brown, E.W.; et al. Prevalence of Salmonella in 11 Spices Offered for Sale from Retail Establishments and in Imported Shipments Offered for Entry to the United States. J. Food Prot. 2017, 80, 1791–1805. [Google Scholar] [CrossRef]
  53. Van Doren, J.M.; Kleinmeier, D.; Hammack, T.S.; Westerman, A. Prevalence, serotype diversity, and antimicrobial resistance of Salmonella in imported shipments of spice offered for entry to the United States, FY2007–FY2009. Food Microbiol. 2013, 34, 239–251. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  54. Haendiges, J.; Blessington, T.; Zheng, J.; Davidson, G.; Miller, J.D.; Hoffmann, M. Complete Genome Sequences of Four Salmonella enterica subsp. enterica Serovar Senftenberg and Montevideo Isolates Associated with a 2016 Multistate Outbreak in the United States. Genome Announc. 2018, 6, e00630-18. [Google Scholar] [CrossRef] [Green Version]
  55. Harvey, R.R.; Marshall, K.E.H.; Burnworth, L.; Hamel, M.; Tataryn, J.; Cutler, J.; Meghnath, K.; Wellman, A.; Irvin, K.; Isaac, L.; et al. International Outbreak of Multiple Salmonella Serotype Infections Linked to Sprouted Chia Seed Powder—USA and Canada, 2013–2014. Epidemiol. Infect. 2017, 145, 1535–1544. [Google Scholar] [CrossRef] [Green Version]
  56. Jones, G.; de la Gandara, M.P.; Herrera-Leon, L.; Herrera-Leon, S.; Martinez, C.V.; Hureaux-Roy, R.; Abdallah, Y.; Nisavanh, A.; Fabre, L.; Renaudat, C.; et al. Outbreak of Salmonella enterica serotype Poona in infants linked to persistent Salmonella contamination in an infant formula manufacturing facility, France, August 2018 to February 2019. Eurosurveillance 2019, 24, 1900161. [Google Scholar] [CrossRef] [Green Version]
  57. Silva, D.; Nunes, P.; Melo, J.; Quintas, C. Microbial quality of edible seeds commercially available in southern Portugal. AIMS Microbiol. 2022, 8, 42–52. [Google Scholar] [CrossRef] [PubMed]
  58. Compaoré, M.K.A.; Bazie, B.S.R.; Nikiema, M.E.M.; Dakené, V.M.; Dembélé, R.; Kpoda, D.S.; Kabré, E.; Barro, N. Assessment of the Sanitary Quality of Ready to Eat Sesame, a Low Moisture Street Food from Burkina Faso. BMC Microbiol. 2021, 21, 207. [Google Scholar] [CrossRef] [PubMed]
  59. Willis, C.; Little, C.L.; Sagoo, S.; de Pinna, E.; Threlfall, J. Assessment of the microbiological safety of edible dried seeds from retail premises in the United Kingdom with a focus on Salmonella spp. Food Microbiol. 2009, 26, 847–852. [Google Scholar] [CrossRef] [PubMed]
  60. Ayaz, M.; Sawaya, W.N.; Al-Sogair, A. Microbiological Quality of Tehineh Manufactured in Saudi Arabia. J. Food Prot. 1986, 49, 504–506. [Google Scholar] [CrossRef] [PubMed]
  61. Alaouie, Z.; Hallal, N.; AlKhatib, A.; Khachfe, H.M. Assessing the Microbial Quality of Tahini (Sesame Paste) in Lebanon. In Global Health 2017: The Sixth International Conference on Global Health Challenges; IARIA: Barcelona, Spain, 2017. [Google Scholar]
  62. Canadian Food Inspection Agency. Targeted Survey Investigating Salmonella, Listeria Monocytogenes and Generic E. coli in Tahini 2012–2014. Available online: https://inspection.canada.ca/food-safety-for-industry/food-chemistry-and-microbiology/food-safety-testing-bulletin-and-reports/salmonella-listeria-monocytogenes-and-generic-e-co/eng/1645637293925/1645637294253 (accessed on 13 October 2022).
  63. Canadian Food Inspection Agency. 2010–2011 Salmonella and Generic E. coli in Tahini. Available online: https://inspection.canada.ca/food-safety-for-industry/food-chemistry-and-microbiology/food-safety-testing-bulletin-and-reports/salmonella-and-generic-e-coli-in-tahini/eng/1430919384198/1430919384776 (accessed on 13 October 2022).
  64. Canadian Food Inspection Agency. 2011–2012 Salmonella and Generic E. coli in Tahini and Sesame Seeds. Available online: https://inspection.canada.ca/food-safety-for-industry/food-chemistry-and-microbiology/food-safety-testing-bulletin-and-reports/salmonella-and-generic-e-coli-in-tahini-and-sesame/eng/1430919620350/1430919620865 (accessed on 13 October 2022).
  65. Var, I.; Uzunlu, S.; Mavis, F.G. Microbial Quality of a Confection (Tahini Halva) Manufactured in Turkey. J. Food Saf. Food Qual. 2020, 71, 124–128. [Google Scholar]
  66. Kahraman, T.; Issa, G.; Ozmen, G.; Buyukunal, S. Microbiological and chemical quality of tahini halva. Br. Food J. 2010, 112, 608–616. [Google Scholar] [CrossRef]
  67. Sengun, I.Y.; Hancioglu, O.; Karapinar, M. Microbiological profile of helva sold at retail markets in Izmir city and the survival of Staphylococcus aureus in this product. Food Control 2005, 16, 840–844. [Google Scholar] [CrossRef]
  68. Kotzekidou, P. Microbial Stability and Fate of Salmonella Enteritidis in Halva, a Low-Moisture Confection. J. Food Prot. 1998, 61, 181–185. [Google Scholar] [CrossRef]
  69. Abu-Jdayil, B.; Al-Malah, K.; Asoud, H. Rheological characterization of milled sesame (tehineh). Food Hydrocoll. 2002, 16, 55–61. [Google Scholar] [CrossRef]
  70. World Health, Organization. Hazard Analysis and Critical Control Point Generic Models for Some Traditional Foods: A manual for the Eastern Mediterranean Region. Available online: https://apps.who.int/iris/handle/10665/119885 (accessed on 13 October 2022).
  71. Yamani, M.I.; Isa, J.K. Microbiological Quality of Tehena and Development of a Generic HACCP Plan for Its Production. World J. Agric. Sci. 2006, 2, 290–297. [Google Scholar]
  72. Al-Nabulsi, A.A.; Olaimat, A.N.; Osaili, T.M.; Shaker, R.R.; Elabedeen, N.Z.; Jaradat, Z.W.; Abushelaibi, A.; Holley, R.A. Use of acetic and citric acids to control Salmonella Typhimurium in tahini (sesame paste). Food Microbiol. 2014, 42, 102–108. [Google Scholar] [CrossRef] [PubMed]
  73. Technavio. Tahini Market by Application and Geography—Forecast and Analysis 2021–2025. Available online: https://www.technavio.com/report/tahini-market-industry-analysis (accessed on 13 October 2022).
  74. Zion Market Research. Tahini Market—Global Industry Analysis. 2019. Available online: https://www.zionmarketresearch.com/report/tahini-market (accessed on 13 October 2022).
  75. Public Health Agency of Canada. Foodbook Report; Public Health Agency of Canada: Ottawa, Canada, 2015; ISBN 978-0-660-03357-0. [Google Scholar]
  76. Zhang, Y.; Keller, S.E.; Grasso-Kelley, E.M. Fate of Salmonella throughout Production and Refrigerated Storage of Tahini. J. Food Prot. 2017, 80, 940–946. [Google Scholar] [CrossRef] [PubMed]
  77. Szpinak, V.; Ganz, M.; Yaron, S. Factors affecting the thermal resistance of Salmonella Typhimurium in tahini. Food Res. Int. 2022, 155, 111088. [Google Scholar] [CrossRef] [PubMed]
  78. Kahyaoglu, T.; Kaya, S. Modeling of moisture, color and texture changes in sesame seeds during the conventional roasting. J. Food Eng. 2006, 75, 167–177. [Google Scholar] [CrossRef]
  79. El-Adawy, T.A.; Mansour, E.H. Nutritional and Physicochemical Evaluations of Tahina (Sesame Butter) Prepared from Heat-Treated Sesame Seeds. J. Sci. Food Agric. 2000, 80, 2005–2011. [Google Scholar] [CrossRef]
  80. Torlak, E.; Sert, D.; Serin, P. Fate of Salmonella during sesame seeds roasting and storage of tahini. Int. J. Food Microbiol. 2013, 163, 214–217. [Google Scholar] [CrossRef] [PubMed]
  81. The Association of Food, Beverage and Consumer Products Companies. Control of Salmonella in Low-Moisture Foods. Available online: https://graphics8.nytimes.com/packages/pdf/business/20090515_moss_ingredients/SalmonellaControlGuidance.pdf (accessed on 13 October 2022).
  82. Finn, S.; Condell, O.; McClure, P.; Amézquita, A.; Fanning, S. Mechanisms of survival, responses and sources of Salmonella in low-moisture environments. Front. Microbiol. 2013, 4, 331. [Google Scholar] [CrossRef] [Green Version]
  83. Osaili, T.; Al-Nabulsi, A.; Nazzal, D.; Al-Holy, M.; Olaimat, A.; Obaid, R.; Holley, R. Effect of water activity and storage of tahini on the viability of stressed Salmonella serovars. Food Sci. Technol. 2021, 41, 144–150. [Google Scholar] [CrossRef]
  84. Osaili, T.M.; Al-Nabulsi, A.A.; Nazzal, D.S.; Shaker, R.R. Effect of Storage Temperatures and Stresses on the Survival of Salmonella spp. In Halva. Lett. Appl. Microbiol. 2017, 65, 403–409. [Google Scholar] [CrossRef] [PubMed]
  85. Burnett, S.L.; Gehm, E.R.; Weissinger, W.R.; Beuchat, L.R. Survival of Salmonella in Peanut Butter and Peanut Butter Spread. J. Appl. Microbiol. 2000, 89, 472–477. [Google Scholar] [CrossRef] [PubMed]
  86. Delamarre, S.; Batt, C. The microbiology and historical safety of margarine. Food Microbiol. 1999, 16, 327–333. [Google Scholar] [CrossRef]
  87. Al-Nabulsi, A.A.; Osaili, T.M.; Olaimat, A.N.; Almasri, W.E.; Ayyash, M.; Al-Holy, M.A.; Jaradat, Z.W.; Obaid, R.S.; Holley, R.A. Inactivation of Salmonella spp. in tahini using plant essential oil extracts. Food Microbiol. 2019, 86, 103338. [Google Scholar] [CrossRef] [PubMed]
  88. Deng, X.; Li, Z.; Zhang, W. Transcriptome sequencing of Salmonella enterica serovar Enteritidis under desiccation and starvation stress in peanut oil. Food Microbiol. 2012, 30, 311–315. [Google Scholar] [CrossRef]
  89. Chen, W.; Golden, D.; Critzer, F. Salmonella survival and differential expression of fatty acid biosynthesis-associated genes in a low-water-activity food. Lett. Appl. Microbiol. 2014, 59, 133–138. [Google Scholar] [CrossRef]
  90. Marmion, M.; Macori, G.; Whyte, P.; Scannell, A.G.M. Stress response modulation: The key to survival of pathogenic and spoilage bacteria during poultry processing. Microbiology 2022, 168, 001184. [Google Scholar] [CrossRef]
  91. White, A.P.; Gibson, D.L.; Kim, W.; Kay, W.W.; Surette, M.G. Thin Aggregative Fimbriae and Cellulose Enhance Long-Term Survival and Persistence of Salmonella. J. Bacteriol. 2006, 188, 3219–3227. [Google Scholar] [CrossRef] [Green Version]
  92. Maserati, A.; Fink, R.C.; Lourenco, A.; Julius, M.L.; Diez-Gonzalez, F. General Response of Salmonella enterica Serovar Typhimurium to Desiccation: A New Role for the Virulence Factors sopDand sseD in Survival. PLoS ONE 2017, 12, e0187692. [Google Scholar] [CrossRef] [Green Version]
  93. Norberto, A.P.; Alvarenga, V.O.; Hungaro, H.M.; Sant’Ana, A.S. Desiccation resistance of a large set of Salmonella enterica strains and survival on dry- and wet-inoculated soybean meal through storage. LWT 2022, 158, 113153. [Google Scholar] [CrossRef]
  94. Xu, Y.; Guan, X.; Lin, B.; Li, R.; Wang, S. Oregano Oil, Epsilon-Polylysine and Citric Acid Assisted Inactivation of Salmonella in Two Kinds of Tahini during Thermal Treatment and Storage. Foods 2021, 10, 1272. [Google Scholar] [CrossRef] [PubMed]
  95. Mauriello, G. Control of Microbial Activity Using Antimicrobial Packaging. In Antimicrobial Food Packaging; Barros-Velázquez, J., Ed.; Academic Press: San Diego, CA, USA, 2016; pp. 141–152. [Google Scholar]
  96. Niemara, B.A. Irradiation, Microwave, and Alternative Energy-Based Treatments for Low-Water Activity Foods. In The Microbiological Safety of Low Water Activity Foods and Spices; Gurtler, J.B., Doyle, M.P., Kornacki, J.L., Eds.; Springer: New York, NY, USA, 2014; pp. 389–402. [Google Scholar]
  97. Osaili, T.M.; Al-Nabulsi, A.A.; Abubakar, S.A.; Alaboudi, A.R.; Al-Holy, M.A. Feasibility of Using Gamma Irradiation for Inactivation of Starvation-, Heat-, and Cold-Stressed Salmonella in Tahini. J. Food Prot. 2016, 79, 963–969. [Google Scholar] [CrossRef]
  98. Osaili, T.M.; Al-Nabulsi, A.A.; Aljaafreh, T.F. Use of Gamma Radiation for Inactivating Salmonella spp., Escherichia coli O157: H7 and Listeria monocytogenes in Tahini Halva. Int. J. Food Microbiol. 2018, 278, 20–25. [Google Scholar] [CrossRef] [PubMed]
  99. Osaili, T.M.; Al-Nabulsi, A.A.; Al Sheikh, Y.M.; Alaboudi, A.R.; Olaimat, A.N.; Al-Holy, M.; Al-Rousan, W.M.; Holley, R. Inactivation of Salmonella spp., Escherichia coli O157: H7 and Listeria monocytogenes in Tahini by Microwave Heating. Foods 2021, 10, 2972. [Google Scholar] [CrossRef] [PubMed]
  100. Xu, Y.; Li, R.; Li, K.; Yu, J.; Bai, J.; Wang, S. Inactivation of inoculated Salmonella and natural microflora on two kinds of edible seeds by radio frequency heating combined with cinnamon oil vapor. LWT 2021, 154, 112603. [Google Scholar] [CrossRef]
  101. Anderson, N.M. Recent advances in low moisture food pasteurization. Curr. Opin. Food Sci. 2018, 29, 109–115. [Google Scholar] [CrossRef]
  102. European Parliamentary Research Service. Recalls of Sesame Seed Products Due to Pesticide Residues. Available online: https://www.europarl.europa.eu/RegData/etudes/ATAG/2021/679077/EPRS_ATA(2021)679077_EN.pdf (accessed on 13 October 2022).
  103. Golden, C.E.; Berrang, M.E.; Kerr, W.L.; Harrison, M.A. Slow-release chlorine dioxide gas treatment as a means to reduce Salmonella contamination on spices. Innov. Food Sci. Emerg. Technol. 2019, 52, 256–261. [Google Scholar] [CrossRef]
  104. Bell, R.L.; Jarvis, K.G.; Ottesen, A.R.; McFarland, M.A.; Brown, E.W. Recent and emerging innovations in Salmonella detection: A food and environmental perspective. Microb. Biotechnol. 2016, 9, 279–292. [Google Scholar] [CrossRef]
  105. Ryan, G.; Roof, S.; Post, L.; Wiedmann, M. Evaluation of Rapid Molecular Detection Assays for Salmonella in Challenging Food Matrices at Low Inoculation Levels and Using Difficult-to-Detect Strains. J. Food Prot. 2015, 78, 1632–1641. [Google Scholar] [CrossRef]
  106. Mattick, K.L.; Jørgensen, F.; Legan, J.D.; Cole, M.B.; Porter, J.; Lappin-Scott, H.M.; Humphrey, T.J. Survival and Filamentation of Salmonella enterica Serovar Enteritidis PT4 and Salmonella enterica Serovar Typhimurium DT104 at Low Water Activity. Appl. Environ. Microbiol. 2000, 66, 1274–1279. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  107. Enache, E.; Podolak, R.; Kataoka, A.; Harris, L.J. Persistence of Salmonella and Other Bacterial Pathogens in Low-Moisture Foods. In Control of Salmonella and Other Bacterial Pathogens in Low Moisture Foods; John Wiley & Sons: Hoboken, NJ, USA, 2017; pp. 67–86. [Google Scholar]
  108. Lang, E.; Zoz, F.; Iaconelli, C.; Guyot, S.; Alvarez-Martin, P.; Beney, L.; Perrier-Cornet, J.-M.; Gervais, P. Recovery Estimation of Dried Foodborne Pathogens Is Directly Related to Rehydration Kinetics. PLoS ONE 2016, 11, e0160844. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  109. Bourdichon, F.; Betts, R.; Dufour, C.; Fanning, S.; Farber, J.; McClure, P.; Stavropoulou, D.A.; Wemmenhove, E.; Zwietering, M.H.; Winkler, A. Processing Environment Monitoring in Low Moisture Food Production Facilities: Are We Looking for the Right Microorganisms? Int. J. Food Microbiol. 2021, 356, 109351. [Google Scholar] [CrossRef] [PubMed]
Table
Table 2. Prevalence of Salmonella in sesame seeds, tahini, and halva.
Table 2. Prevalence of Salmonella in sesame seeds, tahini, and halva.
ProductLocationYearNumber of PositivesTotal SamplesPrevalenceReference
Sesame seedGermany200321612.5%[13]
Sesame seedUK2007–2008137711.7%[59]
Sesame seedUSA2006–20092017711.3%[53]
Sesame seedUSA2010232339.9[44]
Sesame seedUSA2013–201405260[52]
Sesame seedUSA2012–2015 b121557.7[52]
Sesame seedMexico2018–20191210012%[48]
Sesame seedBurkina Faso2007–20179535926.5%[49]
Sesame seedBurkina Faso2021 a0250[58]
Sesame seedSicily2021 a3638.3[51]
Sesame seedPortugal2022 a0180%[57]
TahiniSaudi Arabia1982–19832 c10 c20%[60]
TahiniGermany20031128.3%[13]
TahiniLebanon2015–201774217%[61]
TahiniCanada2010–2014923150.4%[62,63,64]
HalvaGermany200387111.3%[13]
HalvaTurkey2010–20152204 d1%[65]
HalvaTurkey2007–200801200[66]
HalvaTurkey2004 a068 d0[67]
HalvaGreece1997 a04 c0[68]
a year of publication, year of sampling is not known; b collected at import; c number of production plants sampled from; d 10 g analytical unit.
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Coulombe, G.; Tamber, S. Salmonella enterica Outbreaks Linked to the Consumption of Tahini and Tahini-Based Products. Microorganisms 2022, 10, 2299. https://doi.org/10.3390/microorganisms10112299

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Coulombe G, Tamber S. Salmonella enterica Outbreaks Linked to the Consumption of Tahini and Tahini-Based Products. Microorganisms. 2022; 10(11):2299. https://doi.org/10.3390/microorganisms10112299

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Coulombe, Geneviève, and Sandeep Tamber. 2022. "Salmonella enterica Outbreaks Linked to the Consumption of Tahini and Tahini-Based Products" Microorganisms 10, no. 11: 2299. https://doi.org/10.3390/microorganisms10112299

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