International Journal of Food Microbiology 163 (2013) 214–217

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International Journal of Food Microbiology

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Fate of Salmonella during sesame seeds roasting and storage of tahini

Emrah Torlak a,⁎, Durmuş Sert b, Pınar Serin c

a Necmettin Erbakan University, Faculty of Science, Department of Biology, Konya, Turkeyb Necmettin Erbakan University, Faculty of Engineering and Architecture, Department of Food Engineering, Konya, Turkeyc Gesaş Food Company, Konya, Turkey

⁎ Corresponding author at: Necmettin Erbakan Universityof Biology, 42090, Meram, Konya, Turkey. Tel.: +90 544 544

E-mail address: torlakemrah@yahoo.com (E. Torlak)

0168-1605/$ – see front matter © 2013 Elsevier B.V. Alhttp://dx.doi.org/10.1016/j.ijfoodmicro.2013.03.010

a b s t r a c t

a r t i c l e i n f o

Article history:Received 11 January 2013Received in revised form 6 March 2013Accepted 9 March 2013Available online 21 March 2013

Keywords:SalmonellaSesame seedsTahiniRoastingSurvival

Tahini is usually consumed without further heat treatment, and roasting of sesame seeds is the only Salmonellainactivation step in its traditional production process. This study examined the efficiency of the roasting processin the elimination of Salmonella from sesame seeds and the survival of Salmonella in tahini during storage.Sesame seed and tahini samples were inoculated with a cocktail of three serotypes of Salmonella(S. Typhimurium, S.Newport and S.Montevideo). Complete inactivation of Salmonella in sesame seeds, inoculatedwith 5.9 log cfu/g, was achieved by roasting at 110 °C for 60 min, 130 °C for 50 min, or 150 °C for 30 min.Salmonella levels in tahini (aw = 0.17) inoculated with 5.6 log cfu/g and stored for 16 weeks at 22 or 4 °Cdecreased by 4.5 and 3.3 log, respectively. Results of this study demonstrated that the standard roasting processis sufficient to inactivate Salmonella in sesame seeds and low water activity of tahini prevents microbial growth,but its composition allows Salmonella to survive for at least 16 weeks. Therefore, prevention of cross-contamination after roasting is crucial for food safety.

© 2013 Elsevier B.V. All rights reserved.

1. Introduction

Foodborne outbreaks of salmonellosis are usually associated withthe consumption of contaminated animal products such as eggs orpoultry meat or fecally contaminated raw vegetables. However, inthe last few decades, high fat-low moisture colloidal foods such astahini have been identified several times as unusual sources ofsalmonellosis outbreaks (WHO, 2004; Shachar and Yaron, 2006).Presence of both high fat content and lowwater activity has a protectiveeffect against the inactivation of Salmonella (Shachar and Yaron, 2006;Podolak et al., 2010).

Tahini, also called sesame paste, produced by milling from dehulledand roasted sesame seeds, is a popular foodstuff in Middle Eastern andeastern Mediterranean countries and is used as an ingredient in manykinds of foods such as halva and hummus (El-Adawy and Mansour,2000; Lokumcu and Ak, 2005). Contamination of tahini with pathogensis particularly important, since it is usually consumed without anyadditional heat treatment (Lake et al., 2010). Furthermore, its high fatcontent protects the pathogen from gastric acidity resulting in a reduc-tion of the dose–response curve (Nascimento et al., 2012). In recentyears there have been a number of reports of Salmonella outbreaksrelated to the consumption of contaminated tahini. In 2001, an outbreakof S. Typhimurium due to contaminated halva, a traditional low-moisture confectionery produced from tahini, was reported in Sweden

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(Brockmann, 2001). Following this outbreak, Brockmann et al. (2004)examined in total 117 sesame seed products for the occurrence of theSalmonella and 11 of these were found to be contaminated. In 2002and 2003, three outbreaks of S. Montevideo infection associated with ta-hini were reported in Australia and New Zealand (Unicomb et al., 2005).Very recently, a multistate outbreak of Salmonella Bovismorbificansinfections associated with tahini was reported in the USA (CDC, 2012).

Contamination of sesame seeds with Salmonella can occur duringgrowth, storage or processing (Podolak et al., 2010). During growth,the crops are likely to be exposed to a wide range of microbialcontamination from many sources including soil, manure, irrigationwater, wild birds and animals. Further potential for microbialcontamination may occur during post-harvest processing due to poorsanitation practices (Doyle and Erickson, 2008). In a comprehensivesurvey study conducted in the UK, the prevalence of Salmonella insesame seed samples was determined as 1.7% (Willis et al., 2009). Inanother survey study conducted in the USA, 177 sesame seed sampleswere investigated for Salmonella contamination and 20 (11%) sampleswere found to be contaminated (Van Doren et al., 2012).

Roasting of sesame seeds is a basic operation for the productionof tahini. Sesame seeds are roasted in order to promote the flavor,desired color and changes in texture which ultimately increase theoverall palatability of the product (Kahyaoglu and Kaya, 2006). Severaltemperature–time combinations were reported for roasting of sesameseeds during tahini production. Ozcan and Akgul (1994) reported thatsesame should be roasted at 110–150 °C for 2.5–3 h. The optimumroasting range for production of tahini to obtain the desired color andtexture was given as 155–170 °C for 40–60 min (Kahyaoglu and Kaya,2006). Brockmann et al. (2004) concluded that the Salmonella should

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not survive during the sesame seeds roasting. Therefore, they alsoconcluded that the likely cause of the Salmonella outbreaks linked tosesame seed products was cross contamination of the products afterthe heat treatment. However, these conclusions are based on the resultsof studies performed on matrices other than sesame seeds.

There are no published data on the efficiency of the roastingprocess in the elimination of Salmonella from sesame seeds and thesurvival of Salmonella in tahini during storage. Therefore, the objectiveof this study was to assess the fate of Salmonella during the sesameseeds roasting for 60 min at 110 °C, 130 °C and 150 °C and storage oftahini for 16 weeks at 22 and 4 °C.

2. Material and methods

2.1. Salmonella strains

A cocktail of three S. enterica serotypes was used for inoculationof sesame seed and tahini samples: S. Typhimurium, S. Newport andS. Montevideo. These three serotypes have already been involvedin outbreaks of salmonellosis associated with the consumption ofoilseeds and sesame seed products.

Lyophilized cultures of S. Typhimurium (ATCC 14028) and S.Newport (ATCC 6962) were supplied from Microbiologics Inc. (SaintCloud, USA). Culture of S.Montevideo (ATCC 5747)was kindly providedby National Public Health Agency (Ankara, Turkey). Stock cultures ofmicroorganisms were stored in Brain Heart Infusion Broth (Merck,Darmstadt, Germany) supplemented with 20% glycerol at −18 °C.Working cultures were grown on Nutrient Agar (Merck) slantsand kept at 4 °C.

2.2. Inoculum preparation

Each Salmonella strain was transferred into Tryptic Soy Broth(Lab M, Bury, UK) and incubated overnight at 37 °C. Then, a cocktailof the 3 strains was prepared by mixing an equal volume of eachculture in the same tube. The mixed culture was centrifuged at 3600 gfor 10 min at 5 °C (Hettich, Tuttlingen, Germany) and washed threetimes with Phosphate-Buffered Saline (PBS). The final cell pellet wasresuspended in PBS and the cell density of suspension was adjustedto 0.5 McFarland turbidity standard.

2.3. Inoculation of sesame seeds

The wet dehulled sesame seeds were used for inoculation sincedehulling process with water is a step prior to roasting in traditionalproduction of tahini. Nigeria cultivars white sesame seeds deter-mined as Salmonella-negative by the reference culture method (ISO,2002) were dehulled as follows; firstly seeds were sieved and thensoaked in water at ambient temperature for 12 h. The soaked seedswere strained off and passed through amechanical peeler for removingof hulls from seed. The hulls and other foreignmaterials were separatedfrom seeds by using salt solution (1.5% NaCl). The seeds were takenfrom the surface of the salt solution and then washed four times withwater to remove the salt (Kahyaoglu and Kaya, 2006).

Inoculation of wet dehulled sesame seeds was carried out usinga mesh bag (Buchholz and Matthews, 2010). A mesh bag filled with300 g wet dehulled seeds was immersed into Salmonella cell suspensionprepared by diluting the inoculum in Maximum Recovery Diluent(Lab M) to obtain cell density of approximately 107 cfu/ml. The bag ofseed sample was agitated for 10 min by moving bag using draw stringand removed from the cell suspension. Then the inoculated bag of seedsamplewas allowed to drain for 30 min on a stainless steel screenwithina biosafety cabinet (Faster, Ferrara, Italy). After inoculation, the initialinoculation level and water activity (Novasina, Lachen, Switzerland)of sesame seeds were determined.

2.4. Roasting of sesame seeds

The inoculated seed sample was divided into six portions. Sesameseed portions were arranged, as far as was possible, in a single layer inpyrex petri dishes and then dishes were placed in a forced-air oven(Nüve, Ankara, Turkey) which was pre-heated to the respective roastingtemperature. Roasting was carried out at three different temperatures(110, 130 and 150 °C) for 60 min. During the roasting, temperature ofoven air was checked with K-type thermocouple connected to digitalthermometer (Fluke, Everett, WA, USA). Every 10 min during theroasting process, one portion was removed as quickly as possible tominimize changes in the temperature of the oven air, cooled to roomtemperature and assayed for Salmonella and water activity.

2.5. Inoculation of tahini

Commercially produced tahini sample, containing 58.2% crude fat,23.5% crude protein, 13.5% carbohydrate, 4.2% ash and 0.6% moisture,was kindly provided by Gesaş Food Company (Konya, Turkey). It wasdetermined as Salmonella-negative by the reference culture method(ISO, 2002). Twenty five grams of tahini sample was placed in sterilestomacher bags and inoculated with 200 μl of the inoculum. Inoculatedsub-samples in stomacher bags were gently mixed by hand squeezingfor 2 min. Then, bags were sealed and stored at 4 °C or 22 °C for up to16 weeks. Inoculated tahini sample was assayed for Salmonella at thebeginning and end of weeks 1, 2, 4, 8 and 16 during the storage period.

2.6. Salmonella assay

Salmonella enumeration was performed by plate count techniqueon Xylose Lysine Deoxycholate (XLD) Agar (Lab M). Initial suspensionswere prepared with adding 225 ml Buffered PeptoneWater (BPW, LabM) into stomacher bags containing 25 g sample. Sample suspensionswere homogenized using a stomacher (IUL, Barcelona, Spain) and addi-tional ten-fold dilutions were made by Peptone Salt Diluent (Merck).Then, in total 1 ml of initial suspension and dilutions were surfaceplated on three plates of XLD agar. After incubation at 37 °C for 24 h,characteristic colonies with a black center on plates were countedand Salmonella counts were calculated as log cfu/g. Occasionally,characteristic colonies were confirmed using biochemical identificationtest system (Microgen Bioproducts, Camberley, UK).

The enrichment method (ISO, 2002) was performed concurrentlywith the enumeration method starting from initial suspensions inorder to achieve a detection limit of 1 cfu/25 g. After incubation ofinitial suspensions at 37 °C for 22 h, 0.1 ml preenrichment BPWwas added to 10 ml Rappaport Vassiliadis Soy (RVS) broth (Lab M),and 1 ml was added to 10 ml Muller-Kauffmann Tetrathionate-Novobiocin (MKTTn) broth (bioMérieux, Marcyl l'Etoile, France).RVS broth was incubated at 41.5 °C for 24 h and MKTTn broth wasincubated at 37 °C for 24 h. Each selective enrichment broth wasstreaked onto XLD agar. Following incubation at 37 °C for 24 h,presumptive Salmonella colonies were confirmed.

2.7. Statistical analysis

Three independent trials were conducted. Results were analyzedby one-way analysis of variance (ANOVA) using statistical software(SPSS Inc., Chicago, USA). Mean counts were compared using theDuncan grouping test at P b 0.05.

3. Results and discussion

3.1. Survival of Salmonella in sesame seeds subjected to roasting

Thermal inactivation curves of a cocktail of three serotypes ofSalmonella in inoculated sesame seeds roasted at three different

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temperatures (110, 130 and 150 °C) for up to 60 min are given inFig. 1. The initial inoculation level of Salmonella determined as 5.9 logcfu/g was decreased by 1.7, 2.1 and 2.9 log after 10 min of roasting at110, 130 and 150 °C, respectively. Reductions in the counts of Salmonellaranging from 2.9 to 4.4 log were achieved after 20 min of roasting.Enumeration results indicated that reductions in the levels of Salmonellaat 150 °C after 10 and 20 min were significantly (P b 0.05) higher thanthose at 110 and 130 °C. Roasting at 110 and 130 °C for 30 min yieldedreductions of 3.8 and 4.8 log respectively, whereas Salmonella wasnot detected after 30 min roasting at 150 °C. Complete inactivation ofSalmonella in sesame seeds was achieved after 60 min roasting at110 °C. These results showed that all treatments were sufficient toproduce over 5 log reduction in Salmonella counts during the 60 minof roasting. A thermal treatment protocol capable of reducing theSalmonella level in oilseeds and nuts by a minimum 5 log is generallyaccepted as sufficient to provide an appropriate level of consumerprotection (GMA, 2009).

Thermal inactivation results obtained were in accordance with theprevious studies dealing with the inactivation of Salmonella in similarmatrices during the roasting. Nascimento et al. (2012) reported thatthe complete reduction of a pool of five Salmonella serotypes incocoa beans inoculated at level of 6 log cfu/g was achieved after30 min at 120 °C and 40 min at 110 °C. They also reported thatthe type of matrix, the process temperature and the initial countinfluenced the Salmonella resistance. Doyle (2009) demonstratedthat the roasting of peanuts at 129 °C for 45 min, at 146 °C for15 min, and at 163 °C for 10 min caused the reductions of 4.3, 4.9and 5.3 log in Salmonella counts, respectively. Beuchat and Mann(2011) achieved 5 log cfu/g reduction of Salmonella in inoculatedpecan halves by roasting performed at 140 °C for 20 min.

Enumeration results revealed that reduction in the viable cellnumbers achieved after the first 10 min at each of the three differenttemperatures were significantly (P b 0.05) higher than those achievedafter further 10 min intervals of the roasting process. Similarly,Archer et al. (1998) reported that thermal inactivation curves ofS.Weltevreden in flour were biphasic, indicating an initial rapid declinein the viable cell numbers during the first 5–10 min followed by slowerdeath rates. This period coincided with a rapid decrease in the wateractivity of all the samples tested. In this study, the water activity ofinoculated sesame seeds was decreased from 0.98 up to 0.14 duringthe first 10 min of roasting. Izurieta and Komitopoulou (2012) studiedthe effect of moisture on heat resistance of Salmonella in cocoa andhazelnut shells and reported that the addition of moisture (7% w/w)markedly reduced D80°C values of S. Oranienburg and S. Enteritidisranging between 2 and 4.5 min in the twomatrices. A study conductedby Liu et al. (1969) demonstrated that D60°C value of S. Senftenberg insimulated naturally contaminated feed at 5% moisture level was aboutthree times as great as at the respective moisture level of 10%.

-7

-6

-5

-4

-3

-2

-1

00 10 20 30 40 50 60

log

(N

/N0)

roasting time (min)

110°C 130°C 150°C

Fig. 1. Inactivation of Salmonella in sesame seeds during roasting (N: number of survivingcells, cfu/g; N0: initial inoculation level, cfu/g).

Increase in the thermal resistance of Salmonella during the roastingprocess can be explained by cell protein–water interactions. Vibrationof the water molecules during heating causes breakage of disulfideand hydrogen bonds in the surrounding proteins, altering the three-dimensional configuration of the proteins. Vibration effect and proteindenaturation decrease while water content of sesame seeds decreasesduring the roasting. Additionally, a decrease in water content inducesa conformational modification (rigidification) of proteins due todecrease in number of dipoles between polar groups in the peptidechains of proteins and the dipoles of the protein interact (Earnshawet al., 1995; Larochea et al., 2005).

3.2. Survival of Salmonella in tahini

Survival curves of a cocktail of three serotypes of Salmonella ininoculated tahini during storage at room and refrigerator temperaturesare shown in Fig. 2. The initial inoculation level of Salmonella in tahinidetermined as 5.6 log cfu/g decreased by 3.3 and 4.5 log during thestorage at 4 and 22 °C for 16 weeks, respectively. At the end of thestorage period at 4 and 22 °C, cell counts of Salmonella in tahini weredetermined as 2.3 and 1.1 log cfu/g, respectively.

Our results revealed that Salmonella serotypes tested did not grow,but survived in tahini during the 4 months of storage at both roomand refrigerator temperatures. The ability of Salmonella to survive inlow water activity environment of tahini sample (aw = 0.17) can beattributed to several mechanisms including accumulation of betaine viaspecific transporters (Abee andWouters, 1999), accumulation of proline(Neidhardt, 1987), modification of the outer membrane (Rychlikand Barrow, 2005) and the function of σE and σS regulated genes(McMeechan et al., 2007). Previously, several studies demonstratedthat Salmonella has the ability to survive in high fat-lowmoisture colloi-dal foods like tahini during the extended period of storage (Podolak et al.,2010). Burnett et al. (2000) evaluated that survival characteristics of afive-serotype mixture of Salmonella in commercial peanut butters andpeanut butter spreads. They were able to detect Salmonella from peanutbutter and spread samples after 24 weeks of storage. Park et al. (2008)documented the viability of S. Tennessee in commercial brands of peanutbutter for 14 d. In another study (Kotzekidou, 1998), the survival ofS. Enteritidis in halva was investigated and the microorganism wasfound to be capable of surviving up to 8 months' storage.

Reduction values obtained indicated that viability of Salmonellaserotypes at 4 °C was significantly higher compared to at 22 °C. Itwas previously documented that the storage temperature affected theviability of Salmonella in colloidal food products. A study by Hollidayet al. (2003) demonstrated that counts of Salmonella decreased morerapidly in butter, yellow fat spreads, and margarine stored at 21 °C,compared to those at 4.4 °C. Burnett et al. (2000) obtained considerablylower Salmonella counts frompeanut butter and spreads stored at 21 °C

-6

-5

-4

-3

-2

-1

00 2 4 6 8 10 12 14 16

log

(N

/N0)

storage time (week)

4°C 22°C

Fig. 2. Survival of Salmonella in tahini during storage (N: number of surviving cells,cfu/g; N0: initial inoculation level, cfu/g).

217E. Torlak et al. / International Journal of Food Microbiology 163 (2013) 214–217

compared to those at 5 °C. Similarly, Park et al. (2008) reported asignificant difference between levels of Salmonella in peanut buttersamples stored at 4 and 22 °C.

In addition to extrinsic factors, viability of Salmonella in highfat-low moisture colloidal foods is influenced by the sizes of waterdroplets which affect nutrient availability for microbial growth(Park et al., 2008). Salmonella cells inoculated into colloidal foodstend to aggregate or clump within or near the water phase (Burnettet al., 2000). Therefore, a finer emulsion provides a more limitedenvironment and a lower quantity of nutrients available in a dropletfor microbial growth (Catteau, 1985).

4. Conclusions

Thermal inactivation curves of a cocktail of three serotypes ofSalmonella indicate that the standard roasting condition is sufficientto inactivate Salmonella in contaminated sesame seeds. However, itshould be noted that negative consumer attitude towards dark colortahini (Kahyaoglu and Kaya, 2006) may lead producers to preferdifferent roasting conditions, which may be insufficient for theelimination of Salmonella. Therefore, Salmonella contamination intahini may be attributed to both insufficient roasting of contaminatedsesame seeds and to contamination after heat treatment due to poorhygienic conditions during grinding, packaging and transport.

Results of the storage experiment showed that Salmonella counts intahini considerably reduce during an extended storage period; however,results also revealed that Salmonella can survive in tahini for atleast 16 weeks. It was previously documented that small numbers ofSalmonella in tahini can cause a large outbreak of salmonellosis(Unicomb et al., 2005). Therefore, in order to minimize the risk ofsalmonellosis relating to the consumption of contaminated tahini, goodhygiene practices, such as implementation of equipment disinfectionand environmental hygiene control protocols, should be employedduring the production process to control various risk factors that maylead to cross contamination.

Acknowledgment

The authors would like to thankMetisan Serin, Production Managerof Gesaş Food Company, for his valuable contributions.

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