Prevalence of foodborne pathogens in Turkish Van otlu (Herb) cheese

Food Control 17 (2006) 707–711 www.elsevier.com/locate/foodcont

Prevalence of foodborne pathogens in Turkish Van otlu (Herb) cheese ¨ zdemir K. Kaan Tekinsßen *, Zeki O Department of Dairy Technology, University of Nigˇde, 68100 Aksaray, Turkey Received 18 September 2004; received in revised form 11 April 2005; accepted 11 April 2005

Abstract The survey was conducted on 50 unripened Van otlu cheese samples obtained in Van and Hakkari markets at retail level to determine the microbial characteristics with special emphasis on Staphylococcus aureus, Escherichia coli, E. coli O157:H7 and Salmonella spp. The results revealed that S. aureus and E. coli were present in extremely high numbers, with a mean 6.10 and 3.68 log CFU/g, respectively. S. aureus was found in all samples ranging from 2.48 to 7.15 log CFU/g and was present in more than 5.0 · 105 CFU/g in 54% of the samples whereas E. coli was found in 62% of the samples. None of the samples contained E. coli O157:H7; but 3 of the 50 samples had Salmonella spp. The results indicate that Van otlu cheese presents a potential hazard for public health; and the necessary precaution will have to be taken to improve the sanitary practices and cheese manufacturing technique.  2005 Elsevier Ltd. All rights reserved. Keywords: Van otlu cheese; Staphylococcus aureus; Escherichia coli; E. coli O157:H7; Salmonella spp.

1. Introduction Foodborne diseases are still one of the major public health problems world wide and account for considerably high cases of illness. Recent reports indicate that Staphylococcus aureus, Salmonella spp., L. monocytogenes and pathogenic Escherichia coli are considered the most frequent pathogens (Mead et al., 1999; White, Zhao, Simjee, Wagner, & Dermott, 2002); and they are responsible for outbreaks mainly associated with raw milk and raw or inadequately heated milk products (De Buyser, Dufour, Maire, & Lafarge, 2001; Deibel, 1987; IFST, 1998). There have been some reports on the levels of S. aureus and E. coli (Tables 3 and 4) and the incidence of Sal¨ zalp, Kaymaz, & Aksßehirli, 1978; Turantasß, monella (O ¨ nlu¨tu¨rk, & Go¨ktan, 1989) and E. coli O157:H7 (Aksu, U Arun, Aydın, & Ugˇur, 1999; Aslantasß & Yıldız, 2002; Go¨nu¨l, 1997) in various native cheeses in Turkey; but relatively little attention was given to the prevalence of

*

Corresponding author.

0956-7135/$ - see front matter  2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.foodcont.2005.04.007

these organisms in the Van otlu cheese (Kıvanc¸, 1989). Recently, the microbiological status of some native cheeses has reviewed by Turantasß et al. (1989) and Hayalogˇlu et al. (2002). Van otlu cheese is one of the most characteristic of traditional Turkish cheeses and widely consumed in southeastern Anatolia and it has an increasing popularity all over the country. It is a semi hard, dry salted cheese mainly manufactured artisanally from whole unpasteurised eweÕs, cowÕs and/or goatÕs milk without any addition of any starter cultures and contains 0.1– 1.5 % (w/w) a mixture of herbs (e.q. some species of Allium, Choerophyllum, Calamintha, Thymus and Ferula) which is added to the curd. But there is not yet a well defined standardized commercial procedure (Akyu¨z & Tunc¸tu¨rk, 1992; Tekinsßen & Tekinsßen, 2005). It has peculiar characteristics. It is rindless, white coloured and close textured with a salty and piquant flavour. The study of the Van otlu cheese is of interest from a public health point of view since it is produced from raw milk, mainly in small primitive dairies under poor hygienic practices and marketed while fresh or after ripening (Akyu¨z & Tunc¸tu¨rk, 1992). Recent outbreaks of

708

¨ zdemir / Food Control 17 (2006) 707–711 K. Kaan Tekinsßen, Z. O

foodborne illnesses associated with milk and dairy products indisputably revealed that cheeses, particularly made from unpasteurized or improperly pasteurized milk are main sources of salmonellosis, staphylococcal food poisoning and possibly E. coli infections (ACMSF, 1995; Deibel, 1987; Doyle, 1991; IFST, 1998; Meng & Doyle, 1998). Consequently, investigations have focused on the hazard to consumers health due to the potential presence of pathogenic bacteria in raw-milk cheeses. The present study was undertaken to gain some knowledge on the contamination level with S. aureus and E. coli and the occurrence of Salmonella and E. coli O157:H7 in Van otlu cheese consumed in southeastern Anatolia. The information to be obtained should allow a better control of the manufacturing process of the cheese, mainly with regard to the cheese-milk and the handling of the cheese during the manufacturing with the aim of reducing the possible risks associated with pathogens.

2. Materials and methods 2.1. Materials In the period from May 2003 to September 2003 inclusive 50 unripened Van otlu cheese samples were randomly collected weekly from retail outlets, most of which had insufficient storage condition in Van and Hakkari provinces. The samples were transported in 200–250 g quantities to the laboratory under refrigerated (5 ± 1 C) conditions and analyzed upon arrival. 2.2. Methods For the analyses the initial emulsion of the samples were prepared by diluting 10 in 90 g with 2% (w/v) sodium citrate solution at 45 C (Harrigan, 1998) and homogenized in Colworth Stomacher. Serial dilutions were prepared with the use of 0.1% (w/v) pepton water (Oxoid CM 9) (Bridson, 1998; Harrigan, 1998). All of the analyses were duplicated. Presumptive E. coli: These organisms were enumerated in trypton bile X-glucuronide (TBX) medium (Oxoid CM 945). The plates for the counts were incubated for 4 h at 30 C then 18 h at 44 C. The number of blue/green colonies on the plates were evaluated (Bridson, 1998). S. aureus: Baird–ParkerÕs medium (Oxoid CM 275) was used. Surface inoculated plates were incubated at 37 C for 24 and 48 h. The typical S. aureus colonies (black, convex, shiny with narrow white entire margin surrounded by clear zone) were counted and tested for coagulase reaction (Oxoid Staphytect Plus DR 850 M) (Bridson, 1998).

E. coli O157:H7 (VTEC/EHEC): For the detection of E. coli O157:H7 the method recommended by FDA/ BAM AOAC was used (Hitchins, Feng, Watkins, Rippey, & Chandler, 2000, Chapter 4). To detect small numbers, 25 g cheese samples were added to 225 ml m tryptic soy broth (TSB) with novobiocin (20 mg l 1) (Merck 1.09205) and homogenized. After incubation at 37 C for 16–24 h the enrichment culture was streaked on the dry surface of sorbitol Mac Conkey agar (SMAC) with BCIG (5-bromo-4-chloro-3-indol-b-Dglucuronide) (Oxoid CM 0981) containing cefixime-tellurite supplement (Oxoid SR 172). After incubation at 37 C for 16–24 h, the plates were examined for non-fermenting colonies. The pale yellow colonies were confirmed by using the Dryspot E. coli O157 Latex test (Oxoid DR 120 M) for agglutination (Hemakim, 1999). Salmonella spp.: Oxoid Salmonella Rapid Test (SRT) (Oxoid FT 201) was used for the detection of Salmonella spp. The pre-enrichment of the samples was prepared by inoculating 25 g of the samples to 225 ml buffered pepton water (Oxoid CM 509) and homogenized. After incubating at 35 C for 18 h, the Salmonella Rapid test was performed by inoculating 1 ml pre-enrichment culture of the sample to culture vessels containing Salmonella Rapid Test elective medium (Oxoid CM 857) and novobiocin (Oxoid FT 207) with two tubes each of which has a selective and indicator media, namely tube A (Rappaport–Vassiliadis medium and lysine iron cystine neutral red medium) and tube B (modified lysine iron desoxycholate medium and modified brilliant green medium). After incubation of the culture vessel at 41 C for 24 h a loopful of presumptive Salmonella culture was removed from the top of the positive tube and tested by Salmonella Latex Test (Oxoid FT 203) for agglutination (Bridson, 1998; Harrigan, 1998).

3. Results and discussion S. aureus and E. coli in cheese are frequently used as indicators of hygienic quality and show lack of microbiological safety (Doyle & Padhye, 1989; IFST, 1998; Lu¨ck & Dunkled, 1981). Some strain of these organisms are known to cause diseases in humans. Therefore they are undesirable in high numbers. The summarized results of the microbiological analysis of the Van otlu cheese samples are shown in Table 1; while the frequency distribution of the numbers of S. aureus and presumptive E. coli in the samples is given in Table 2. Of the samples analysed all contained generally high numbers of S. aureus with the mean count of 6.1 log CFU/g varying between 2.48 and 7.15 log CFU/ g. In this study S. aureus counts were generally higher than those reported in various Turkish cheeses (Table 3). This may be due to a certain extent to the use of raw milk and manufacturing process carried out under

¨ zdemir / Food Control 17 (2006) 707–711 K. Kaan Tekinsßen, Z. O Table 1 The Results of microbiological analysis of Van otlu cheese samples Microorganism

Number Count of of sample microorganisms (log CFU/g)

S. aureus Presumptive E. coli E. coli O157:H7 Salmonella

50 50

6.10 6.41 2.48–7.15 50 3.68 3.93 0–4.53 31

50 50

– –

x

S

– –

Positive sample

Range

– –

Number %

0 3

100 62 0 6

x: Mean S: Standard deviation. Table 2 Frequency distribution of the numbers of microorganisms in 50 Van otlu cheese samples Number (CFU/g)

S. aureus

Presumptive E. coli

<1.0 · 10 1.0 · 10–9.9 · 10 1.0 · 102–9.9 · 102 1.0 · 103–9.9 · 103 1.0 · 104–9.9 · 104 1.0 · 105–9.9 · 105 1.0 · 106–9.9 · 106 1.0 · 107–9.9 · 107

– (0) – (0) 1 (2) 11 (22) 11 (22) 14 (28) 12 (24) 1 (2)

19 (38) 1 (2) 7 (14) 16 (32) 7 (14) – (0) – (0) – (0)

Figures in parentheses are the per cent of samples.

unhygienic conditions and can be partially explained by rather high salt (6.5% w/w) and low acid contents (0.71% lactic acid) of Van otlu cheese (Yetisßmeyen, Yıldırım, & Yıldırım, 1992) when compared to other native cheeses. Since S. aureus can grow and dominate most other bacteria in the presence of 5–10% salt concentration (Banwart, 1983) and occurs in low acid cheeses (Anonymous, 1995). The results are contradictory to the findings of Kıvanc¸ (1989) who reported that only 30% of the Van otlu cheese contained S. aureus with the highest level of 1.04 log CFU/g. This appears to be related to the different source and ripening period of the samples and/ or extreme diversity of manufacturing conditions since the samples at the present work were unripened, and

709

S. aureus should decline to low levels during ripening (Chapman & Sharpe, 1981; Erkmen, 1995; IDF, 1980). S. aureus counts of the samples showed a large range of variation from 102 to 9.9 · 107/g. However 54% of the samples contained more than 105 S. aureus/g pointing out a potential hazard as some strains are produce toxins. The occurrence of S. aureus more than 102/g in all samples may indicate the use of milk from infected (clinical and subclinical mastitic) udder, which is frequently associated with this organism and/or an extensive contamination by personnel possibly involved in milk production and cheese making as human beings are common carriers (Hobbs & Gilbert, 1979). It has also been well documented that these organisms may reach high numbers in milk during manufacturing operations and cheeses with low acidity (Chapman & Sharpe, 1981; IDF, 1980; Johnson, Nelson, & Johnson, 1990) and present a potential hazard to the consumers (Hobbs & Gilbert, 1979). The samples had presumptive E. coli with a mean of 3.68 log CFU/g (Table 1). Significant variations on the frequency distribution of this organism were observed. Thus, the counts ranged from less than 10–105 60% was contained in excess of 102 CFU/g (Table 2); but none at higher than 4.53 log CFU/g. Varying levels of presumptive E. coli counts in the samples may indicate the extreme diversity of hygienic practices undertaken throughout the milk and cheese productions. The incidence and presumptive E. coli counts are similar to those reported by Sancak and Sancak (1995) in S ß avak cheeses (Table 4) generally made from raw milk. Despite the high level and incidence of S. aureus, 38% of the samples were presumptive E. coli free. This indicates a weak relationship between the occurrence of these organisms and is probably explained by relatively high salt content of Van otlu cheese. However the incidence of S. aureus and presumptive E. coli in more than 50% of the samples reveals an extensive deficiency of satisfactory sanitary practices during milk production and

Table 3 S. aureus in main traditional Turkish cheeses Cheese variety

Number of sample

Positive (%)

Counts (log CFU/g) Mean

White

5.52

2.04–4.26 3.46 1.30–1.70 1.00–1.90 2.96–6.86

Uraz and Gu¨ndogˇan (1998) Kıvanc¸ (1989) Turantasß et al. (1989) C ¸ elik et al. (1998) Ganemogˇlu (1991)

40 60 90

2.52 4.13

2.00–5.70 2.49 5.54

Tekinsßen and C ¸ elik (1979) Kıvanc¸ (1989) Sancak and Sancak (1995)

38

68

3.92

3.81–5.75

Bostan et al. (1992)

20 50

30 100

0.95 6.10

1.04 2.48–7.15

Kıvanc¸ (1989) Present study

12 20 38 16 30

100 35 8 19 40

40 20 50

Tulum Van otlu

S ß avak

References

Range

3.79 2.62

¨ zdemir / Food Control 17 (2006) 707–711 K. Kaan Tekinsßen, Z. O

710

Table 4 Presumptive E. coli in main traditional Turkish cheeses Cheese variety

Number of sample

Positive (%)

Counts (log CFU/g)

White

38 50 75 21 30

73.7 22 36.8 42.5 93.3

2.40 3.40

45 50

71.1 62

Tulum

17

32.9

Van otlu

50

62

Mean

S ß avak

3.82

3.68

cheese manufacturing and/or post production handling of the Van otlu cheese because these organisms are killed by pasteurization and are found in a wide variety of habitats (Kloos & Banner, 1999). When compared to other native cheeses (Tables 3 and 4), rather high level of S. aureus and presumptive E. coli in the Van otlu cheeses may be attributable to the use of raw milk. It is because Van otlu cheese is produced from raw milk possibly with a high initial count under artisanal conditions and handled at various stages of manufacturing. Another aspect to be taken into account is the addition of various herbs which may contribute to high S. aureus and E. coli loads in the cheese. Information on the incidence and prevalence of E. coli O157:H7 and Salmonella organisms is just developing on traditional cheeses in Turkey. Very few studies have been conducted on the presence of these pathogens in some cheeses. In the present study E. coli O157:H7 was not isolated in 50 Van otlu cheese samples. Similar results in 50 Kasßar and 10 Tulum cheeses were recently stated by Aslantasß and Yıldız (2002). However the isolation of E. coli O157:H7 was reported in 6.6% (1/15) of Tulum cheese (Go¨nu¨l, 1997), 2% (1/50) (Aksu et al., 1999) and 1% (1/ 100) (Aslantasß & Yıldız, 2002) of White cheese samples. The results of Go¨nu¨l (1997) are disputable as the method used is only sufficient to define E. coli O157. The disagreement with the others is most probably related to very low incidence of E. coli O157:H7 and the different microbiological and chemical characteristics of Van otlu cheese from White cheese. This needs further investigation. As pointed out by IFST (1998) the occurrence and survival characteristics of pathogenic bacteria vary as widely as the type of cheeses they contaminate. Salmonella organisms were detected in 6% (3/50) of Van otlu cheese samples. These findings are contradictory to the ¨ zalp et al. (1978) and Turantasß et al. (1989) results of O who did not find Salmonella spp. in 26 Tulum cheese and 38 White cheese samples, respectively. This can be partly explained by the use of raw milk in the production of Van otlu cheese under improper sanitary practices and

References

Range 0.60–5.15 2.04–4.38

4.38

Turantasß et al. (1989) Kalkan et al. (1991) Kıvanc¸ (1990) ¨ zc¸elik (1996) Digrak and O Sert and Kıvanc¸ (1984)

0.60–5.06

Tekinsßen et al. (1993) Sancak and Sancak (1995)

3.81–5.75

¨ zc¸elik (1996) Digrak and O

1.85–4.53

Present study

of unripened samples for analyses. Since raw milk is considered as a likely source of Salmonella spp. (Deibel, 1987; Hobbs & Gilbert, 1979). The current Turkish microbiological standards for cheese at retail point permit a maximum count of S. aureus 102 CFU per gram and E. coli 2 MPN per gram, but not the presence of Salmonella in 25 g of sample (Anonymous, 2001). On the basis of these limits, of 50 Van otlu cheese samples analysed all for S. aureus, at least 21 for E. coli and 3 for Salmonella failed to meet the national standard. 4. Conclusions Van otlu cheese contains S. aureus and presumptive E. coli at rather high levels but appears to be free from E. coli O157:H7 and has limited level of Salmonella organisms. These results indicate that the cheese represents a potential hazard for consumer and the low bacteriological quality of Van otlu cheese seems to be closely related with the use of raw milk and inadequate processing and storage conditions. But the extent to which Van otlu cheese play a role in food borne pathogens needs further research. More data on the incidence of Salmonella and pathogenic E. coli in other traditional cheeses on a national basis are also required in the understanding of the epidemiology of food borne pathogens. Due to the potential presence of some pathogenic bacteria, attempts will have to be made for the development of production techniques (e.q. adequate heat treatment of cheese-milk and the use of appropriate starter culture) and improvements in hygienic practices during manufacturing and storage, paying attention to the ripening period for the cheese prior to sale. References ACMSF. (1995). Report on verocytotoxin—Producing Escherichia coli. Report by the advisory committee on the microbiological safety of food. HMSO, London.

¨ zdemir / Food Control 17 (2006) 707–711 K. Kaan Tekinsßen, Z. O ¨.O ¨ ., Aydın, A., & Ugˇur, M. (1999). Escherichia coli Aksu, H., Arun, O O157:H7Õnin hayvansal ko¨kenli gıda maddelerinde varlıgˇı. Pendik Veteriner Mikrobiyoloji Dergisi, 30(2), 77–81. Akyu¨z, N., & Tunc¸tu¨rk, Y. (1992). Van ilinin genel su¨tc¸u¨lu¨k durumu ¨ niversitesi Ziraat Faku¨ltesi u¨zerinde bir arasßtırma. Yu¨zu¨ncu¨ Yıl U Dergisi, 2(2), 1–12. Anonymous. (1995). The dairy products (hygiene) regulations 1995. (S.I. No 1086). HSMO, London. Anonymous. (2001). Tu¨rk Gıda Kodeksi. Mikrobiyolojik kriterler Tebligˇi. Tebligˇ No: 2001/19. Resmi Gazete; Tarih 02.09.2001, Sayı: 24511. ¨ , & Yıldız, P. (2002). Kars yo¨resinde hayvansal kaynaklı Aslantasß, O gıdalarda Escherichia coli O157:H7 izolasyonu. Veteriner Bilimleri Dergisi, 18(1–2), 107–111. Banwart, G. (1983). Basic food microbiology (3rd ed.). Wesport, CT: AVI Publishing Com. Inc., p. 231. Bostan, K., Ugˇur, M., & Aksu, H. (1992). Deri ve plastik bidonlar ic¸inde satısßa sunulan tulum peynirlerinin duyusal kimyasal ve mikrobiyolojik o¨zellikleri. Pendik Hayvan Hastahanesi Merkezi Arasßtırma Enstitu¨su¨ Dergisi, 23(1), 78–83. Bridson, E. Y. (1998). The oxoid manual (8th ed.). Basingstoke: Oxoid Ltd. ¨ zdemir, C ¨ zdemir, S., & Sert, S. (1998). Diyarbakır C ¸ elik, S ¸ ., O ß ., O yo¨resinde tu¨ketime sunulan salamura beyaz peynir o¨rneklerinin ¨ ru¨nleri mikrobiyolojik, fiziksel ve kimyasal o¨zellikleri. V. Su¨t ve U ¨ ru¨nleri, MPM Sempozyumu. 21–22 Mayıs 1998, Geleneksel Su¨t U Yay. No: 621, Mert Matbaası, Ankara. Chapman, H. R., & Sharpe, M. E. (1981). Microbiology of cheese. In R. K. Robinson (Ed.). Dairy microbiology (Vol. 2, pp. 157–243). London: Applied Science. De Buyser, M. L., Dufour, B., Maire, M., & Lafarge, V. (2001). Implication of milk and milk products in food-borne diseases in France and in different industrialised countries. International Journal of Food Microbiology, 67, 1–17. Deibel, R. H. (1987). Cheese recalls associated with pathogenic bacteria. 24th Annual Marschall invitational Italian cheese seminar, September 16–17, 1987, Madison, WI. ¨ zc¸elik, S. (1996). ElazıgˇÕda satısßa sunulan peynirlerden Digrak, M., & O izole edilen koliform grubu bakterilerin tanımlanması. Gıda, 21(1), 3–7. Doyle, M. P. (1991). Escherichia coli O157:H7 and its significance in foods. International Journal of Food Microbiology, 12, 289–301. Doyle, M. P., & Padhye, V. V. (1989). Escherichia coli. In M. P. Doyle (Ed.), Foodborne bacterial pathogens (pp. 235–271). New York: Marcel Dekker Inc. Erkmen, O. (1995). Behavior of Staphylococcus aureus in Turkish feta cheese during manufacture and ripening. Journal of Food Protection, 58(11), 1201–1205. Ganemogˇlu, E. N. (1991). Adana Piyasasında Tu¨ketime Sunulan ¨ zerinde Beyaz Peynirlerde Enterotoksijenik StaphylococcusÕlar U ¨ niv. Fen Bil. Enst., Bir Arasßtırma. Yu¨ksek Lisans Tezi, C ¸ ukurova U Adana. Go¨nu¨l, A. (1997). C ¸ igˇ su¨t ve peynir o¨rneklerinde enterohemorajik E. ¨ KEM Dergisi, 20(2), 69–73. coliÕye (O157:H7) rastlanma sıklıgˇı. KU Harrigan, W. F. (1998). Laboratory methods in food microbiology (3rd ed.). London: Academic Press. Hayalogˇlu, A. A., Gu¨ven, M., & Fox, P. F. (2002). Microbiological, biochemical and technological properties of Turkish white cheese ‘‘Beyaz Peynir’’. International Dairy Journal, 12, 635–648. Hemakim (1999). Mikrobiyolojik Analiz Yo¨ntemlerinde Yeni Yak_ ¨ ru¨nler Tic. Ltd. lasßımlar. Istanbul: Hemakim Tıbbi U Hitchins, A. D., Feng, P., Watkins, W. D., Rippey, S. R., & Chandler, L. A. (2000). Escherichia coli and the coliform bacteria. Food and drug administration (8th ed.). Washington, DC: AOAC International, p. 4.01–4.29.

711

Hobbs, B. C., & Gilbert, R. J. (1979). Food poisoning and food hygiene (4th ed.). London: Edward Arnold Ltd. IDF. (1980). Behavior of pathogens in cheese. IDF document 122. Bruxelles: International Dairy Federation. IFST (1998). Food safety and cheese. Food Science and Technology Today, 12(2), 117–122. Johnson, E. A., Nelson, J. H., & Johnson, M. (1990). Microbiological safety of cheese made from heat-treated milk. Part II. Microbiology. Journal of Food Protection, 53, 519–540. ¨ lgen, T., & Mutluer, B. Kalkan, A., Aktan, H. T., Kamber, U., U (1991). Beyaz peynirlerde koliform bakteriler (E. coli ve K. ¨ niverpneumoniae)Õin bulunusßu u¨zerinde arasßtırmalar. Ankara U sitesi Veteriner Faku¨ltesi Dergisi, 38(1–2), 108–113. Kıvanc¸, M. (1989). A survey on the microbiological quality of various cheeses in Turkey. International Journal of Food Microbiology, 9, 73–77. Kıvanc¸, M. (1990). Peynirlerden izole edilen koliform grubu bakterilerin tanımlanması. Gıda, 15(2), 93–99. Kloos, W., & Banner, T. (1999). Staphylococcus and Micrococcus. In P. R. Murray, E. J. Baron, M. A. Pfaller, Tenover, & R. H. Yolken (Eds.), Manual of clinical microbiology (7th ed., pp. 264–271). Washington, DC: ASM Press. Lu¨ck, H., & Dunkled, M. (1981). Enterobacteriaceae in cheese. South African Journal of Dairy Technology, 31(1), 9–14. Mead, P. S., Slutsker, L., Dietz, V., McCaig, L. F., Bresee, J. S., & Shapio, C. (1999). Food-related illness and death in the United States. Emergency Infectious Diseases, 5607–5625. Meng, J., & Doyle, M. P. (1998). Microbiology of Shiga toxin producing Escherichia coli O157:H7 in foods. In J. B. Kaper & A. D. OÕBrien (Eds.), Escherichia coli O157:H7 and other Shiga Toxin producing E. coli strains (pp. 92–108). Washington, DC: ASM. ¨ zalp, E., Kaymaz, S O ß , & Aksßehirli, E. (1978). Erzincan tulum peynirlerinde enterotoksijenik stafilokoklar ve salmonellalar ¨ niversitesi Veteriner Faku¨ltesi yo¨nu¨nden bir arasßtırma. Ankara U Dergisi, 25(1), 55–61. Sancak, H., & Sancak, Y. C. (1995). Van piyasasında tu¨ketime sunulan salamura beyaz peynirlerin mikrobiyolojik, kimyasal, fiziksel ve ¨ niversitesi Sagˇlık duyusal niteliklerinin incelenmesi. Yu¨zu¨ncu¨ Yıl U Bilimleri Enstitu¨su¨ Dergisi, 7, 106–113. Sert, S., & Kıvanc¸, M. (1984). Erzurum piyasasında taze olarak tu¨ketime sunulan beyaz peynirlerin hijyenik kaliteleri u¨zerinde bir arasßtırma. Ziraat Dergisi, 15(3–4), 79–89. Tekinsßen, O. C., & C ¸ elik, C. (1979). S ß avak peynirinde Staphylococ¨ niversitesi Veteriner Faku¨ltesi cusÕlar ve MicrococcusÕlar. Ankara U Dergisi, 16(3–4), 47–63. Tekinsßen, O. C., Patır, B., & Alkan, M. (1993). S ß avak peynirinde koliform grubu mikroorganizmalar u¨zerinde arasßtırmalar. Selc¸uk ¨ niversitesi Veteriner Faku¨ltesi Dergisi, 9, 9–13. U ¨ ru¨nleri: Temel Tekinsßen, O. C. & Tekinsßen, K. K. (2005). Su¨t ve Su¨t U ¨ niv. Basımevi, Bilgiler, Teknoloji, Kalite Kontrolu. Selc¸uk U Konya, p. 240. ¨ nlu¨tu¨rk, A., & Go¨ktan, D. (1989). Microbiological and Turantasß, F., U compositional status of Turkish white cheese. International Journal of Food Microbiology, 8(1), 19–24. Uraz, G., & Gu¨ndogˇan, N. (1998). Beyaz peynirlerin mezofil florasında bulunan koliform, stafilokok, LLP, stafilokok ve basillusların bulunma sıklıkları. Gıda, 23(6), 391–401. White, D. G., Zhao, S., Simjee, S., Wagner, D. D., & Dermott, P. F. (2002). Antimicrobial resistance of food borne pathogens. Microbes and Infection, 4, 405–412. Yetisßmeyen, A., Yıldırım, M., & Yıldırım, Z. (1992). Ankara piyasasında tu¨ketime sunulan otlu peynirin kimyasal, mikrobiyo¨ niv. Zir. Fak. lojik ve duyusal niteliklerinin belirlenmesi. Ankara U Yay, Ankara, p. 1273.