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. 2010 Dec 22;49(5):601–607. doi: 10.1007/s13197-010-0200-4

Fate of some pathogenic bacteria and molds in Turkish Tarhana during fermentation and storage period

Fulya Turantaş 1,✉, Kemal Kemahlıoğlu 1
PMCID: PMC3550847  PMID: 24082272

Abstract

The survival of the molds and some pathogenic bacteria such as E. coli O157:H7, S. aureus, S. typhimurium and B. cereus during fermentation and storage period of tarhana (traditional Turkish fermented food) was investigated. Tarhana batches were produced with two different yogurt/flour ratio 0.5 (T1) and 0.75 (T2). The pH and Eh values of samples were around 4.0–4.5 and 130–160 mV during fermentation and storage period in both batches, respectively. Moisture and aw values in T1 and T2 samples significantly decreased (p < 0.05) between the 3rd–7th days of production at 11.2–11.6% and 0.52–0.54, respectively. The numbers of S. aureus and S. typhimurium significantly decreased (p < 0.05) during the 1st and 2nd days of fermentation period, respectively and this decline gradually proceeded in both batches. No significant differences (p > 0.05) were observed in both tarhana batches among the molds, E. coli O157:H7 counts during the 1st, 2nd days of fermentation, and B. cereus counts during the all days of fermentation and storage periods, except the16th day of storage.

Keywords: Tarhana, Pathogen survival, Fermented foods, Acid-resistant pathogens

Introduction

Traditional fermented foods appear to be a cheap, practical, convenient and nutritious alternative for the modern world where famine is a great threat. Among the Turkish cultural and traditional foods, tarhana has an important place in daily diet especially for the people who live in rural parts of the Turkey. It is produced with flour, yogurt, salt, onion, tomato, pepper and spices (mint, red pepper). In winter time, Turkish people prefer traditionally prepared foods more in their diets. Furthermore, the dried tarhana slices are consumed in different ways such as nugget or snack in local regions of Anatolia. Baker’s yeast is generally added to the tarhana dough, leading to the lactic acid and alcohol fermentation (İbanoğlu and İbanoğlu 1999; Çopur et al. 2001; Erbaş et al. 2006). Therefore, tarhana has an acidic taste and yeast aroma.

The important nutrients such as organic acids, ascorbic acid, niacin, folic acid, pantothenic acid, minerals and different amino acids are produced during tarhana fermentation (Nout 1993; Svanberg and Lorri 1997; Nout and Motarjemi 1997; Steinkraus 2002). Because of its high nutritional value and bioavailability, tarhana is generally used for feeding children and elderly people (İbanoğlu and İbanoğlu 1999; Dağlıoğlu 2000; Ekinci 2005; Ekinci and Kadakal 2005; Özdemir et al. 2007; Bozkurt and Gürbüz 2008; Dalgıç and Belibağlı 2008; Bilgiçli 2009).

The effects of different ingredients, fermentation and storage conditions on the chemical, nutritional, rheological and functional properties of tarhana have been studied (Temiz and Pirkul 1990; Temiz and Pirkul 1991; İbanoğlu et al. 1995; İbanoğlu et al. 1999; Dağlıoğlu 2000; Köse and Çağındı 2002; Erbaş et al. 2005; Erbaş et al. 2006; Bilgiçli et al. 2006a; Bozkurt and Gürbüz 2008; Bilgiçli 2009). There are limited microbiological data about on the survival of some pathogenic bacteria during production of tarhana (Aytaç 1996; Dağlıoğlu 2000; Sağdıç et al. 2005). Lactic antagonism is an important example of the microbial interference. Among antimicrobial factors, pH depression is generally known as the primary factor for inhibition of microorganisms. However, in recent years several studies have been carried out on the acid tolerance and survival characteristics of some pathogenic bacteria in different acidic and/or acidic-fermented foods (Skovgaard 2007; Stopforth et al. 2007; Alvarez-Ordonez et al. 2009; Montet et al. 2009). From this perspective, it is important to determine the surviving conditions of some pathogenic bacteria and molds in acidic-fermented foods such as tarhana. Some of the researches have focused on Lactococcus, Lactobacillus, Streptococcus, and other species which are the dominant organisms in starter cultures used for different fermented foods which contain milk and yogurt (Smit et al. 2005). Yogurt added to tarhana dough contains mixed cultures of Streptococcus salivarius subsp. thermophilus and Lactobacillus delbrueckii subsp. bulgaricus in a 1:1 ratio. Lactic acid bacteria (LAB) produce lactic acid and a small amount of other organic acids, which have an antimicrobial and antagonistic effect on pathogenic and spoilage microorganisms in foods (Bozkurt and Gürbüz 2008; Buyong et al. 1998; Dağlıoğlu 2000; El-Ziney et al. 1999; Jay et al. 2005; Kang and Fung 2000). However, no information is published regarding to the lactic antagonism on the survival of some pathogenic bacteria and molds during tarhana production.

The objective of this research was to determine the survival of molds and some pathogenic bacteria as indicators such as Escherichia coli (E. coli) O157:H7, Staphylococcus aureus (S. aureus), Salmonella typhimurium (S. typhimurium) and Bacillus cereus (B. cereus) which contaminated from different habitats in home-style domestic production during fermentation and storage period of tarhana.

Materials and methods

Materials

Wheat flour (moisture 14%, protein 12%, ash 0.5% on dry basis), full fat yogurt (3.2% wet basis), tomato paste (double concentrated, brix 28–30%) and paprika paste (brix 18–19%) onion, mint, red pepper, salt and baker’s yeast (Saccharomyces cerevisiae, press form) were purchased from local markets in Izmir, Turkey. Before processing, all the ingredients were appropriately handled and onion was peeled and chopped.

Test cultures

The cultures of E. coli O157:H7 ATCC 43895, S. aureus ATCC 4012, S. typhimurium ATCC 7823, and B. cereus FCI 11778 obtained from Safe Spice and Food Control Institute of Izmir were used in the experiments. These microorganisms were maintained on slopes of nutrient agar (Oxoid).

Production of tarhana

All ingredients of tarhana (wheat flour 1000 g, yogurt 500 g or 750 g, tomato paste 150 g, paprika paste 100 g, onion 150 g, salt 25 g, baker’s yeast 25 g, red pepper 10 g, mint 10 g and water 100 g) were mixed. Two different tarhana doughs (T1 and T2) were prepared using the same ingredients and quantities with two different yogurt/flour ratio (0.5- T1 and 0.75- T2). Tomato and paprika paste, onion and salt were blended by using Waring blender. All other ingredients were added to the tarhana dough and kneaded in a Hobart mixer (A120-10, Hobart MFG, London) for 5 min at the highest speed. After kneading tarhana, herb (Echinobhora sibthorpiana) was added in dough to provide special aroma, and then the tarhana doughs (T1 and T2) were divided into two parts for microbiological and chemical analysis and placed in two sealed plastic containers (27 × 27 × 5 cm) to a depth of 2 cm. First part was inoculated with 5 ml of suitable dilutions of 24 h nutrient broth cultures. The initial numbers of cultures in T1 and T2tarhana doughs were 3.6–3.5/5.3–5.8/6.1–6.8 and 4.1–4.8 log cfu/g for E. coli O157:H7, S. aureus, S. typhimurium and B. cereus, respectively. Following inoculations tarhana doughs were manually kneaded by hand using disposable gloves (5 ml culture/500 g tarhana dough). Second part of the tarhana doughs was used for chemical analysis. Tarhana samples were fermented at 28 °C for 4 days in an incubator. It was manually mixed every 12 h by a spoon to prevent surface drying and dough rising.

The numbers of E. coli O157:H7, S. aureus, S. typhimurium, B. cereus, molds, LAB and pH, Eh (oxidation-reduction potential), water activity (aw) and moisture were determined at 0, 1st, 2nd, 3rd and 4th days of fermentation and 7th, 9th and 16th days of storage.

At the end of the fermentation period, tarhana doughs were divided into small pieces and dried at ambient temperature for a few days (between 4th–7th days) similar to home-style natural drying conditions (on the bench in the laboratory) and finally ground in a blender. The dried samples were kept in the screw-capped glass jar at ambient temperature until analysed. All analyses were carried out in triplicate.

Microbiological analysis

Ten g of tarhana samples were aseptically homogenised for 2 min in a stomacher model 400 (Seward Medical, London, UK) with 90 ml of 0.1% peptone (Oxoid) water and serial decimal dilutions were made using the same diluent. Salmonella–Shigella agar, Baird Parker agar and MacConkey agar (Oxoid) were used for enumeration of S. typhimurium, S. aureus and E. coli O157:H7 by using spread plate method, respectively. The numbers were determined after incubation at 32 °C for 24–48 h (Tadesse et al. 2005). For B. cereus count, the serial dilutions were plated on Phenol-Red Egg Yolk Polymyxin Agar (Oxoid) incubated at 35–37 °C for 24 h (Rhodehamel and Harmon 2001). The mold count was determined by the pour plate method using Oxytetracycline Glucose Yeast Extract Agar (Oxoid) and incubated at 20–25 °C for 3–5 days (Ünlütürk and Turantaş 2002). LAB were enumerated on Man-Rogosa and Sharp agar (MRS, Oxoid) with an overlay of the same agar and incubated for three days at 30 °C (Dağlıoğlu et al. 2002; Ünlütürk and Turantaş 2002). All microbiological analyses were performed in triplicate samples.

Chemical analysis

A 10 g of tarhana sample was dissolved in 100 ml of distilled water. The pH and Eh of the samples was measured using a portable pH/Eh meter (Sartorious AG, PT-10, Germany) during fermentation (0, 1st, 2nd, 3rd and 4th days) and 7th, 9th and 16th days of storage. At the end of the 16th day of storage, the total titratable acidity of the samples were expressed as percent lactic acid on dry base (İbanoğlu et al. 1999). aw values of tarhana samples was measured using a water activity measurement device (Testo 400, Lenzkirch, Germany) with an accuracy of ±0.001 at 25 °C during fermentation and storage period (0, 1, 2, 3, 4, 7, 9 and 16th days). Moisture content was measured by drying samples to a constant weight (AOAC, 1990), and calculating the percentage of weight loss during fermentation and storage period (0, 1, 2, 3, 4, 7, 9 and 16th days). All assays were performed in triplicate samples and results were given as means.

Statistical analysis

All statistical calculations were performed by SAS Statistical Software (release 7.00 for windows, SAS Institute Inc., Cary, NC, USA). Significance were evaluated with the analyses of variance (p < 0.05).

Results and discussion

The pH and Eh values of tarhana samples during the fermentation were shown in Fig. 1. The tarhana doughs used in these experiments had the pH of 4.43–4.45 and the Eh values of 131.6–132.8 mV immediately after kneading in 0.50 (T1) and 0.75 (T2) yogurt/flour ratio tarhana samples, respectively. The pH values of the T1 and T2tarhana samples varied from 4.43 to 3.97 and 4.45 to 3.88, Eh values of T1 and T2 samples varied from 131.6 to 160.7 mV and 132.8 to 161.3 mV, respectively during the fermentation period. The pH values of T1 and T2 significantly decreased (p < 0.05) at the 4th day of fermentation from 4.43 to 3.97 and from 4.45 to 3.88, respectively. The pH values gradually decreased (p < 0.05) and the Eh values increased after the 4th day of fermentation and the final pH and Eh values of T1 and T2 samples after the 16th day of storage reached to 4.54–4.53 and 131.9–130.8 mV, respectively. Moisture and aw values in T1 and T2 samples significantly decreased (p < 0.05) in drying stage (between 4th and 7th days), from 33.2–35.5% to 11.2–11.6% and from 0.63–0.66 to 0.52–0.54, respectively (Fig. 1).

Fig. 1.

Fig. 1

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pH, Eh, moisture and aw values of tarhana samples during the fermentation* and storage** period. Yogurt/flour ratio 0.5 ● T1 and 0.75 ∆ T2, the values are the average of triplicate measurements (n = 3). (* at 28 º C, ** at ambient temperature)

Similar to our findings, Sağdıç et al. (2005) and Erbaş et al. (2005) reported that the pH values of tarhana doughs were around 4.0–4.5 during 3 days of fermentation. At the beginning of the fermentation, relatively low pH value (around 4.5) of fresh tarhana samples (T1 and T2) is attributed to different organic acids present and/or produced in dough by means of LAB and yeasts in our research. However, Erbaş et al. (2006) determined that lactic, acetic and propionic acids were found in fresh tarhana.

As shown in Fig. 2, during the first 3 days of fermentation period, the numbers of E. coli O157:H7 slightly inclined from 3.6 to 3.3 log cfu/g in T1 and T2tarhana samples. Although there was no consistent and appreciable difference between the numbers of E. coli O157:H7 at 1st, 2nd and 3rd days of fermentation in the T1 and T2 samples, these differences were found to be not significant either between days in the same tarhana sample or between two different tarhana samples for the same days (p > 0.05). In contrast, the viable numbers of E. coli O157:H7 in T1 and T2 samples showed more than 2.5 log unit reduction within 1 day (from third to fourth day) at pH 3.97 and 3.88, at 160.7 and 161.3 mV of Eh values, respectively. The numbers of E. coli O157:H7 decreased below detectable level (<100 cfu/g) at the 4th day of storage in both tarhana batches (Fig. 2).

Fig. 2.

Fig. 2

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Microbiological changes during tarhana fermentation* and storage** period. Yogurt/flour ratio 0.5 ● T1 and 0.75 ∆ T2, the values are the average of triplicate measurements (n = 3). (* at 28 º C, ** at ambient temperature)

Sağdıç et al. (2005) determined that the growth of E. coli O157:H7 was inhibited at the end of the 2nd day of fermentation of seven different tarhana samples (control and added different spices). Aytaç (1996) reported that E. coli O157:H7 was able to survive on the 8th day of fermentation in tarhana at pH 3.10. In our research, E. coli O157:H7 was inhibited between the 4th and 7th days of storage period of T1 and T2tarhana samples at approx. pH 4 (3.9/4.0/3.8). Similar to our findings, Dağlıoğlu et al. (2002) determined that E. coli O157:H7 survived until the 3rd day of fermentation in the inoculated samples; it was inhibited after the 5th day. This phenomena can be explained by the inexistence of a standardized production process for tarhana production. Application of different ingredients, the bacterial strains used and the fermentation conditions might lead to varying results and survivability of microorganisms. From the stand point of the inhibition pathogenic and spoilage bacteria, it is clear that low pH, moisture, aw and high Eh values were very important inhibitory factors in dry fermented foods.

It is determined that the conditions of fermentation are attributed to failure of some pathogenic bacteria such as Salmonella, S. aureus, Listeria monocytogenes and E. coli O157:H7. A wide variety of food-borne pathogens are either inhibited or killed and many spoilage microorganisms are affected similarly in fermented foods. Lactic antagonism has been attributed to the production of organic acids, hydrogen peroxide, bacteriocins, diacetyl and antibiotics by means of LAB. Organic acids reduce the pH value below 4.0–4.5, making it difficult for some spoilage and pathogenic microorganisms contaminated from different sources to survive. Many researchers observed a correlation between the decline in pH and antagonistic effect of LAB (Dağlıoğlu 2000; Blandino et al. 2003; Jay et al. 2005). However, Huang et al. (2001) demonstrated that the fermentation by-products decreased the viability of both E. coli O157:H7 and S. aureus depending on the concentrations and the lactic antagonism has received extensive attention and several reviews have been published, the most contemporary researches are listed as Fang et al. (1996), Nazef et al. (2008) and Singh and Ramesh (2008).

The number of S. aureus decreased from 5.32 to 3.78 and from 5.85 to 3.92 during the first 24 h of fermentation period of T1 and T2tarhana samples. Significant (p < 0.05) decline in the number of S. aureus of T1 and T2tarhana samples continued until the 3rd day of fermentation and the number of S. aureus decreased under the detectable level (<100 cfu/g, Fig. 2). This decline differed from the other test organisms which survived until the 4th, 7th, 9th and 16th days.

In the both tarhana batches (T1 and T2), the number of microorganisms decreased to undetectable level at the 3 rd, 4th, 4th, 4th, and 16th days of fermentation and storage period of tarhana for S. aureus, molds, E. coli O157:H7, S. typhimurium and B. cereus, respectively (Fig. 2). It could be concluded that the numbers of S. aureus and S. typhimurium had shown gradual and significant decline (p < 0.05) during the fermentation and storage period of tarhana batches (T1 and T2) differed from E. coli O157:H7 and B. cereus. In spite of, several researches have reported that S. aureus can grow and survive in environments with relatively low pH and high salt concentration (Koening and Marth 1982; Halpin-Dohnalek and Marth 1989; Brunner and Wong 1992; Dağlıoğlu et al. 2002), in our research, the number of S. aureus significantly decreased (p < 0.05) during the first day of fermentation and then gradual decline had continued until the 3rd day of fermentation (undetectable level) for both the tarhana batches. Similarly, surviving numbers of S. typhimurium showed a tendency to decline (p < 0.05) starting from the second day of fermentation and decreased below the detectable level (<100 cfu/g) at the 4th day of storage while the E. coli O157:H7 and B. cereus counts did not significantly change (p > 0.05) during the 3rd and 9th days of fermentation and storage period, respectively. It could be explained that B. cereus is a spore forming bacterium and can resist and survive for long periods under unfavorable conditions and E. coli O157:H7 used in this research can be relatively a low pH resistant strain. However, it is reported that the some food-borne pathogens like S. typhimurium, E. coli O157:H7 are able to survive under extremely low pH (pH 2–3) conditions (de Jonge et al. 2003).

A large number of investigators have shown that the normal saprophytic flora in foods offers protection against staphylococcal growth through antagonism; in addition, competition for nutrients and the modification of environmental conditions are less favourable for S. aureus and Salmonella. In addition to, the antagonistic effect of other bacteria such as Acinetobacter, Aeromonas, Bacillus, Pseudomonas, S. epidermidis, the Enterobacteriaceae, the Lactobacillaceae, enterococci and others create unfavourable conditions for S. aureus and Salmonella (Caplice and Fitzgerald 1999; Jay et al. 2005). Finally, it can be said that S. aureus and Salmonella are not competitive enough in tarhana and in many food systems.

The results of this research showed that the important food-borne pathogens in tarhana ingredients survived after the fermentation period. Especially, competitive and resistant pathogens such as B. cereus can survive under unfavourable conditions in wet and dry-fresh tarhana during storage period.

The gradual decline of the LAB counts continued until the 16th day of storage and the numbers of LAB decreased from 7.6 to 5.1 log cfu/g in all final T1-T2tarhana samples (Fig. 2). Different researches had determined that the number of the LAB was nearly around 6.5–7.0 log cfu/g at the beginning of the fermentation period of tarhana containing 0.35 and 0.50 ratio of yogurt (Sağdıç et al. 2005; Erbaş et al.2005). The surviving numbers of molds showed a tendency to decline (p < 0.05) starting from the second day of fermentation and decreased below the detectable level (<10 cfu/g) at the 4th day of fermentation due to the restricting factors such as Eh, aw, acid content. Similar results were founded in the previous work (İbanoğlu et al. 1999).

Similarly, the total titratable acidity (as lactic acid) of the dried and ground tarhana samples was nearly around at 1.8–2.5% were reported (İbanoğlu et al. 1999; Erbaş et al. 2005; Bilgiçli et al. 2006b). In our research, total acidity was 2.3 and 2.5% for dried samples on the 16th storage day of T1 and T2 samples, respectively. Similar to our findings, Bozkurt and Gürbüz (2008) reported that the total acidity was generally (17%) higher when yogurt ratio was increased from 0.5 to 0.75 in tarhana dough. It can be concluded from the results of this study that increasing ratio of yogurt in the tarhana dough did not significantly affect the surviving of pathogens at the end of the 16th storage day. According to Bozkurt and Gürbüz (2008), high percentage yogurt (75%) containing tarhana samples involve higher amounts of lactic acid; but increased moisture and oil content would create a shelf-life risk in the long-term storage. Although researches did not contain any microbiological data, they can give an idea about some factors (such as acidity, moisture) affected by growth and survival of microorganisms. According to our findings, there was not any important pH, aw, moisture content and total acidity differences (p > 0.05) between two batches of tarhana containing different ratio of yogurt (0.5 and 0.75) at the end of the 16th day of storage period.

It should be kept in mind that there is no standardized production process for tarhana which is traditionally produced at different regions of Turkey, and different food-borne pathogens generally contaminate during the home-style domestic production period from the human, ingredients and environments. It should be noted that the numbers for a particular contamination source reported by different researchers do not always reflect the microbiological status of the product correctly under ideal production, handling and storage conditions.

Conclusion

Microbial flora of fermented foods is primarily created by the natural flora of raw foods. In addition to these microorganisms, especially in home-style domestic production, the seconder flora can be contaminated from the different environmental sources. From the stand point of the human health protection and the food spoilage prevention, some foods gain importance after the determination of acid-resistant pathogenic bacteria in the acid-fermented foods. Sometimes tarhana is consumed before drying. As a consequence, consumption of wet fresh tarhana is not recommended in the first 7 days of production the period of which microorganisms inactivate.

References

  1. Alvarez-Ordonez A, Fernandez A, Bernardo A, Lopez M. Comparison of acids on the induction of an acid tolerance response in Salmonella typhimurium consequences for food. Meat Sci. 2009;81(1):65–70. doi: 10.1016/j.meatsci.2008.06.019. [DOI] [PubMed] [Google Scholar]
  2. Official methods of analysis. 15. Washington DC: Association of Official Analytical Chemists; 1990. [Google Scholar]
  3. Aytaç SA. Fate of Escherchia coli O157:H7 and Yersinia enterocolitica in preparation of tarhana. Adv Food Sci. 1996;18:28–31. [Google Scholar]
  4. Bilgiçli N. Effect of buckwheat flour on chemical and functional properties of tarhana. LWT Food Sci Technol. 2009;42:514–518. doi: 10.1016/j.lwt.2008.09.006. [DOI] [Google Scholar]
  5. Bilgiçli N, Elgün A, Herken EN, Türker S, Ertaş N, İbanoğlu Ş. Effect of wheat germ/bran addition on the chemical, nutritional and sensory quality of tarhana, a fermented wheat flour-yogurt product. J Food Eng. 2006a;77:680–686. doi: 10.1016/j.jfoodeng.2005.07.030. [DOI] [Google Scholar]
  6. Bilgiçli N, Elgün A, Türker S. Effects of various phytase sources on phytic acid content, mineral extractability and protein digestibility of tarhana. Food Chem. 2006;98:329–337. doi: 10.1016/j.foodchem.2005.05.078. [DOI] [Google Scholar]
  7. Blandino A, Al-Aseeri ME, Pandiella SS, Cantero D, Webb C. Cereal-based fermented foods and beverages. Food Res Int. 2003;36:527–543. doi: 10.1016/S0963-9969(03)00009-7. [DOI] [Google Scholar]
  8. Bozkurt O, Gürbüz O. Comparison of lactic acid contents between dried and frozen tarhana. Food Chem. 2008;108:198–204. doi: 10.1016/j.foodchem.2007.10.063. [DOI] [Google Scholar]
  9. Brunner K, Wong ACL. Staphylococcus aureus growth and enterotoxin production in mushrooms. J Food Sci. 1992;57:700–703. doi: 10.1111/j.1365-2621.1992.tb08076.x. [DOI] [Google Scholar]
  10. Buyong N, Kok J, Luchansky JB. Use of genetically enhanced, pedio-producing starter culture, Lactococcus lactis subsp lactis MM217, to control Listeria monocytogenes in cheddar cheese. Appl Environ Microbiol. 1998;64:4842–4845. doi: 10.1128/aem.64.12.4842-4845.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Caplice E, Fitzgerald GF. Food Fermentations: role of microorganisms in food production and preservation. Int J Food Microbiol. 1999;50:131–149. doi: 10.1016/S0168-1605(99)00082-3. [DOI] [PubMed] [Google Scholar]
  12. Çopur OU, Göçmen D, Tamer CE, Gürbüz O. Tarhana Üretiminde Farklı Uygulamaların Ürün Kalitesine Etkisi. Gıda. 2001;26:339–346. [Google Scholar]
  13. Dağlıoğlu O. Tarhana as a traditional Turkish fermented cereal food: Its recipe, production and composition. Nahrung. 2000;44(2):85–88. doi: 10.1002/(SICI)1521-3803(20000301)44:2&#x0003c;85::AID-FOOD85&#x0003e;3.0.CO;2-H. [DOI] [PubMed] [Google Scholar]
  14. Dağlıoğlu O, Arıcı M, Konyalı M, Gumus T. Effects of tarhana fermentation and drying methods on the fate of Escherichia coli O157:H7 and Staphylococcus aureus. Eur Food Res Technol. 2002;215:515–519. doi: 10.1007/s00217-002-0584-0. [DOI] [Google Scholar]
  15. Dalgıç AC, Belibağlı KB. Hazard analysis critical control points implementation in traditional foods: a case study of tarhana processing. Int J Food Sci Technol. 2008;43:1352–1360. doi: 10.1111/j.1365-2621.2007.01619.x. [DOI] [Google Scholar]
  16. de Jonge R, Ritmeester WS, Van Leusden FM. Adaptive responses of Salmonella enterica serovar typhimurium DT104 and other S typhimurium strains and Escherichia coli O157H7 to low pH environments. J Appl Microbiol. 2003;94:625–632. doi: 10.1046/j.1365-2672.2003.01875.x. [DOI] [PubMed] [Google Scholar]
  17. Ekinci R. The effect of fermentation and drying on the water-soluble vitamin content of tarhana, a traditional Turkish cereal food. Food Chem. 2005;90:127–132. doi: 10.1016/j.foodchem.2004.03.036. [DOI] [Google Scholar]
  18. Ekinci R, Kadakal C. Determination of seven water-soluble vitamins in tarhana, a traditional Turkish cereal food, by high-performance liquid chromatography. Acta Chromatogr. 2005;15:289–297. [Google Scholar]
  19. El-Ziney MG, Van Den Tempel MGT, Debevere J. Application of reuterin produced by Lactobacillus reuteri 12002 for meat decontamination and preservation. J Food Protect. 1999;62:257–261. doi: 10.4315/0362-028x-62.3.257. [DOI] [PubMed] [Google Scholar]
  20. Erbaş M, Certel M, Uslu MK. Microbiological and chemical properties of tarhana during fermentation and storage as wet-sensorial properties of tarhana soup. Swiss Soc Food Sci and Technol. 2005;38:409–416. [Google Scholar]
  21. Erbaş M, Uslu MK, Erbaş MO, Certel M. Effects of fermentation and storage on the organic and fatty acid contents of tarhana, a Turkish fermented cereal food. J Food Compos Anal. 2006;19:294–301. doi: 10.1016/j.jfca.2004.12.002. [DOI] [Google Scholar]
  22. Fang W, Shi M, Huang L, Chen J, Wang Y. Antagonism of lactic acid bacteria towards Staphylococcus aureus and Escherichia coli on agar plates. Vet Res. 1996;27:3–12. [PubMed] [Google Scholar]
  23. Halpin-Dohnalek MI, Marth EH. Staphylococcus aureus: Production of extracellular compounds and behavior in foods—a review. J Food Protect. 1989;52:267–282. doi: 10.4315/0362-028X-52.4.267. [DOI] [PubMed] [Google Scholar]
  24. Huang LS, Weng YM, Chidu RYY. Survival of Staphylococcus aureus and Escherichia coli as affected by ethanol and NaCl. J Food Prot. 2001;64:546–550. doi: 10.4315/0362-028x-64.4.546. [DOI] [PubMed] [Google Scholar]
  25. İbanoğlu E, İbanoğlu Ş. Rheological properties of cooked tarhana, a cereal-based soup. Food Res Int. 1999;32:29–33. doi: 10.1016/S0963-9969(99)00069-1. [DOI] [Google Scholar]
  26. İbanoğlu Ş, Ainsworth P, Wilson G, Hayes GD. The effect of fermentation conditions on the nutrients and acceptability of tarhana. Food Chem. 1995;53:143–147. doi: 10.1016/0308-8146(95)90779-7. [DOI] [Google Scholar]
  27. İbanoğlu Ş, İbanoğlu E, Ainsworth P. Effect of different ingredients on the fermentation activity in tarhana. Food Chem. 1999;64:103–106. doi: 10.1016/S0308-8146(98)00071-5. [DOI] [Google Scholar]
  28. Jay JM, Loessner MJ, Golden DA. Modern food microbiology. 7. New York: Springer; 2005. [Google Scholar]
  29. Kang DH, Fung DYC. Stimulation of starter culture for further reduction of food-borne pathogens during salami fermentation. J of Food Protect. 2000;63:1492–1495. doi: 10.4315/0362-028x-63.11.1492. [DOI] [PubMed] [Google Scholar]
  30. Koening S, Marth EH. Behavior of Staphylococcus aureus in Cheddar cheese made with sodium chloride or mixture of sodium chloride and potassium chloride. J Food Protect. 1982;45:996–1002. doi: 10.4315/0362-028X-45.11.996. [DOI] [PubMed] [Google Scholar]
  31. Köse E, Çağındı ÖS. An investigation into the use of different flours in tarhana. Int J Food Sci Technol. 2002;37:219–222. doi: 10.1046/j.1365-2621.2002.00559.x. [DOI] [Google Scholar]
  32. Montet MP, Christieans S, Thevenot D, Coppet V, Ganet S, Muller MLD, Duniere L, Vernozy-Rozand C. Fate of acid-resistant and non-acid resistant Shiga toxin producing. Int J Food Microbiol. 2009;129:264–270. doi: 10.1016/j.ijfoodmicro.2008.12.002. [DOI] [PubMed] [Google Scholar]
  33. Nazef L, Belguesmia Y, Tani A, Prévost H, Drider D. Identification of lactic acid bacteria from poultry feces: evidence on anti-campylobacter and anti-listeria activities. Poultry Sci. 2008;87:329–334. doi: 10.3382/ps.2007-00282. [DOI] [PubMed] [Google Scholar]
  34. Nout MJR. Processed weaning foods for tropical climates. Int J Food Sci Nutr. 1993;43:213–221. doi: 10.3109/09637489309027545. [DOI] [Google Scholar]
  35. Nout MJR, Motarjemi Y. Assessment of fermentation as a household technology for improving food safety: a joint FAO/WHO workshop. Food Control. 1997;8:221–226. doi: 10.1016/S0956-7135(97)00021-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Özdemir S, Göçmen D, Kumral AY. A traditional Turkish fermented cereal food: tarhana. Food Rev Int. 2007;23:107–121. doi: 10.1080/87559120701224923. [DOI] [Google Scholar]
  37. Rhodehamel EJ, Harmon SM (2001) Bacillus cereus Bacteriological Analytical Manual Online, Chapter 14 Center for Food Safety and Applied Nutrition US Food and Drug Administration http://wwwcfsanfdagov/ebam/bam-14html. Accessed 14 May (2009)
  38. Sağdıç O, Soyyiğit H, Özçelik S, Gül H. Viability of Escherichia coli O157:H7 during the fermentation of tarhana produced with different spices. Ann Microbiol. 2005;55(2):97–100. [Google Scholar]
  39. Singh AK, Ramesh A. Succession of dominant and antagonistic lactic acid bacteria in fermented cucumber: insights from a PCR-based approach. Food Microbiol. 2008;25:278–287. doi: 10.1016/j.fm.2007.10.010. [DOI] [PubMed] [Google Scholar]
  40. Skovgaard N. New trends in emercing pathogens. Int J Food Microbiol. 2007;120:217–224. doi: 10.1016/j.ijfoodmicro.2007.07.046. [DOI] [PubMed] [Google Scholar]
  41. Smit G, Smit BA, Engels WJM. Flavour formation by lactic acid bacteria and biochemical flavour profiling of cheese products. FEMS Microbiol Rev. 2005;29:591–610. doi: 10.1016/j.fmrre.2005.04.002. [DOI] [PubMed] [Google Scholar]
  42. Steinkraus KH. Fermentations in world food processing. Compr Rev Food Sci and Food Safety. 2002;1:23–30. doi: 10.1111/j.1541-4337.2002.tb00004.x. [DOI] [PubMed] [Google Scholar]
  43. Stopforth JD, Skandamis PN, Geornaras I, Sofos JN. Acid tolerance of acid-adapted and nonacid-adapted E. coli O157:H7 strains in beef decontamination runoff. Food Microbiol. 2007;24(5):530–538. doi: 10.1016/j.fm.2006.05.007. [DOI] [PubMed] [Google Scholar]
  44. Svanberg U, Lorri W. Fermentation and nutrient availability. Food Control. 1997;8:319–327. doi: 10.1016/S0956-7135(97)00018-2. [DOI] [Google Scholar]
  45. Tadesse G, Ashenafi M, Ephraim E. Survival of E. coli O157:H7 Staphylococcus aureus, Shigella flexneri and Salmonella spp in fermenting ‘Borde’, a traditional Ethiopian beverage. Food Control. 2005;16:189–196. doi: 10.1016/j.foodcont.2004.01.011. [DOI] [Google Scholar]
  46. Temiz A, Pirkul T. Tarhana fermantasyonunda kimyasal ve mikrobiyolojik değişimler. Gıda. 1990;15:119–126. [Google Scholar]
  47. Temiz A, Pirkul T. Farklı bileşimlerde üretilen tarhanaların kimyasal ve duyusal özellikleri. Gıda. 1991;16:7–13. [Google Scholar]
  48. Ünlütürk A, Turantaş F. Gıdaların Mikrobiyolojik Analizi, 2 nd edn. Bornova: Meta Basım Matbaacılık; 2002. [Google Scholar]

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