Turkish Journal of Veterinary & Animal Sciences 
Volume 28 Number 5 Article 22 
1-1-2004 
A Study on Survival of Listeria monocytogenes during 
Manufacture and Ripening of Kashar Cheese 
FİGEN ÇETİNKAYA 
G. ECE SOYUTEMİZ 
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ÇETİNKAYA, FİGEN and SOYUTEMİZ, G. ECE (2004) "A Study on Survival of Listeria monocytogenes 
during Manufacture and Ripening of Kashar Cheese," Turkish Journal of Veterinary & Animal Sciences: 
Vol. 28: No. 5, Article 22. Available at: https://journals.tubitak.gov.tr/veterinary/vol28/iss5/22 
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Turk J Vet Anim Sci
28 (2004) 927-932
© TÜB‹TAK
Research Article
A Study on Survival of Listeria monocytogenes during Manufacture
and Ripening of Kashar Cheese
Figen ÇET‹NKAYA, G. Ece SOYUTEM‹Z
Department of Food Hygiene and Technology, Faculty of Veterinary Medicine, Uluda¤ University, Görükle, Bursa- TURKEY
Received: 09.05.2003
Abstract: This study was performed to determine the survival of Listeria monocytogenes during the manufacture and ripening of
Kashar, a popular cheese in Turkey. Raw milk was inoculated at 4 different levels with L. monocytogenes serotype 4b (ca. 3, 4, 5,
and 6 log cfu ml-1 for group 1, 2, 3 and 4 cheeses, respectively) and made into Kashar cheese using the traditional technique.
Following dry salting for 10 days at 18 ± 2 ºC, the Kashar cheese was ripened for 20 days at the same temperature and then stored
at 5 ± 1 ºC for 3 months. Samples of milk, coagulum, curd and cheese were tested for Listeria numbers by surface plating on Oxford
Agar. In all groups the numbers of pathogens remained nearly constant during the initial stages of cheese production. However, an
approximately 1 log cfu g-1 increase was detected in L. monocytogenes counts, while the pH decreased from 6.37-6.40 to 5.03-
5.07, during curd acidification. Heat treatment of ripe curd at 75 ºC for 5 min greatly influenced viability, but was not enough to
destroy all the bacteria, especially when inoculated at high levels. The pathogen was not isolated on the 60th and 120th days of
ripening in group 2 and 3 cheeses, respectively. Meanwhile, 1.83 log cfu g-1 bacteria remained viable in group 4 even after 120
days of ripening. As a consequence, it was determined that in conjunction with the heat treatment of curd, a ripening period of 4
months was necessary to eliminate L. monocytogenes when its levels were lower than 6 log cfu ml-1. It was concluded that the
techniques used in the production stages of Kashar cheese are not sufficient to eliminate high contamination (6 log cfu ml-1) by L.
monocytogenes and the cheese may pose a risk of food-borne listeriosis.
Key Words: Kashar cheese, Listeria monocytogenes, survival 
Kaflar Peynirinin Üretimi ve Olgunlaflmas› S›ras›nda Listeria monocytogenes’in Canl›l›¤›n›
Sürdürmesi Üzerine Bir Araflt›rma
Özet: Bu çal›flma, Türkiye’de yayg›n olarak tüketilen kaflar peynirinin üretimi ve olgunlaflmas› s›ras›nda Listeria monocytogenes’in
canl›l›¤›n› saptamak amac›yla gerçeklefltirildi. Çi¤ süt dört farkl› düzeyde (1., 2., 3. ve 4. grup peynirler için s›ras›yla 3, 4, 5, 6 log
kob ml-1) L. monocytogenes serotip 4b ile inokule edildi ve geleneksel tekni¤e göre kaflar peyniri üretildi. 18 ± 2 ºC’de 10 gün süreyle
kuru tuzlamay› takiben ayn› ›s›da 20 gün olgunlaflmaya b›rak›lan kaflar peynirleri, daha sonra 5 ± 1 ºC’de 3 ay boyunca depoland›.
Süt, p›ht›, teleme ve peynir örnekleri, Oxford agar’a uygulanan yüzey ekim tekni¤i ile Listeria say›lar› aç›s›ndan analiz edildi. Tüm
gruplarda, peynir üretiminin bafllang›ç aflamalar›nda patojenin say›lar› nispeten sabit kald›. Bununla birlikte p›ht›n›n fermentasyonu
s›ras›nda, pH 6,37-6,40’dan 5,03-5,07’ye azal›rken, L. monocytogenes say›lar›nda yaklafl›k 1 log kob g-1’l›k bir art›fl belirlendi.
Telemeye 75 ºC’de 5 dakika süreyle uygulanan ›s› ifllemi etkenin canl›l›¤›n› önemli ölçüde etkilemesine ra¤men, özellikle yüksek
inokulasyonlu peynirlerde bakteriler yeterince inhibe edilmedi. 2. ve 3. grup peynirlerde s›ras›yla olgunlaflman›n 60. ve 120.
günlerinde izole edilmeyen etken, 4. grup peynirlerde olgunlaflman›n 120. gününde bile 1,83 log kob g-1 düzeyinde canl› kald›. Sonuç
olarak, 6 log cfu ml-1’den daha düflük L. monocytogenes seviyelerini ortadan kald›rmak için telemeye uygulanan ›s› ifllemiyle birlikte
dört ayl›k olgunlaflma süresinin gerekli oldu¤u belirlendi. Ayr›ca, kaflar peynirinin üretim aflamalar›nda yararlan›lan tekniklerin yüksek
L. monocytogenes kontaminasyonunu (6 log cfu ml-1) elimine etmedi¤i ve bu peynirin g›da kökenli listeriosis için bir risk
oluflturabilece¤i sonucuna var›ld›.
Anahtar Sözcükler: Kaflar peyniri, Listeria monocytogenes, canl›l›¤›n› sürdürme
Introduction It is produced from either sheep’s or cow’s milk, or a
Kashar cheese has been one of the most popular semi- mixture of the two. It is subjected to a stretching process
hard cheeses produced in the Balkan countries since the at 75 ºC during manufacture and a to ripening period of
11th and 12th centuries. Kachkaval, Kaser, Kackavaly, 4 months. Kashar cheese contains an average of 24.2%
Kacekavalo, Dobrogen, Pirdop, Epir, Sarplaninski and protein, 4.2% ash, 41.9% moisture, 25.1% fat, and
Pirotski are some local names for the same product (1). 4.6% salt (2). Its pH and acidity level (LA%) are between
927
A Study on Survival of Listeria monocytogenes during Manufacture and Ripening of Kashar Cheese
4.9 and 5.4 and 0.8 and 2.3, respectively (3,4). While rennet diluted in cold water was added to induce
Kashar is the second most popular cheese in Turkey, coagulation. The coagulum (usually 45-60 min after
there are no standardized techniques used in its rennet addition) was cut into approximately 4 cm cubes
manufacture. In traditional techniques, given the fact that and remained quiescent for ca. 15 min. The temperature
no pasteurization process is applied, pathogen of the vat content was gradually raised to 41 ºC under
microorganisms can be eliminated by heat treatment at continuous stirring. Thereafter, the coagulum was
75 ºC during the curd stretching stage as well as by collected in cheesecloth and pressed for syneresis (2 h).
antimicrobials and metabolic acids produced by lactic acid Subsequently, the curd was cut into blocks (25-35 cm)
bacteria from the natural flora (4,5).  and kept at room temperature for 16 h. At the end of this
period, the curd assumed an elastic form and its pH
Several outbreaks and cases associated with the
reached 5.03-5.07. At this stage, heat treatment of the
consumption of foods, including milk and dairy products,
curd at 75 ± 1 ºC for 5 min was performed. For this
have provided evidence of the importance of L.
purpose, the curd was cut into long strips and placed in a
monocytogenes in the food industry (6,7). In recent
water bath in a stainless steel bucket containing several
years, studies have revealed that soft and semi-soft
holes (5 mm diameter). After heat treatment, the curd
cheeses provide suitable conditions for the survival and was manually kneaded for 5 min to eliminate air bubbles
development of this pathogen (8,9). It has been reported and was moulded in plastic moulds (20 cm in diameter and
that 17 of the 68 traditional hard and semi-hard cheeses 16 cm in height). The next day, cheese wheels
(25%) manufactured in Alentejo (a region in Southern (approximately 3 kg) were removed from the plastic
Portugal) were contaminated with Listeria spp. and 8 of moulds and dry salted. For this, salt (average 13-15 g)
these (11.8%) were identified as L. monocytogenes (10). was spread on the top surface of the wheels once every 2
Outbreaks of cheese-borne listeriosis and conflicting days at room temperature for a period of 10 days. The
reports regarding its heat resistance (11,12) prompted wheels were turned over during each salting process.
us to investigate this pathogen in Kashar cheese Thereafter, they were stored at room temperature for 20
manufactured according to traditional techniques.  days and transferred to the ripening room (5 ± 1 ºC) for
3 months (2).
Materials and Methods Sampling
Bacterial cultures Duplicate samples were taken from inoculated milk,
coagulum, acidified curd, heat-treated curd and cheese
L. monocytogenes strain SLCC 2375 serotype 4b used samples on days 1, 10, 30, 60, 90 and 120 of ripening. 
in this study was kindly provided by Dr. Ch. Jacquet,
Microbiological analysis
Institut Pasteur, Centre National de Reference des
Listeria, Paris, France. Stock cultures were maintained on For enumeration of L. monocytogenes, samples (10
Tryptone Soya Agar (TSA) (no. CM131, Oxoid) slants at ml or g) were homogenized in 90 ml of 0.1% peptone
4 ºC, and were subcultured monthly. For intermediate water using a Seward Stomacher 80 Lab System (~2 min)
cultures, stock cultures were transferred into Tryptone and a 0.1 ml portion of the homogenate was plated on
Soya Broth (TSB) (no. CM129, Oxoid) and incubated at the surface of Oxford Agar medium (no. CM856, Oxoid)
35 ºC for 24 h. with supplement (no. SR140E, Oxoid). To increase the
detection level to 10 organisms/g, 0.2 ml of the initial
Inoculation of cheese-milk with L. monocytogenes 1:10 dilution was surface plated on each of 5 plates of
and cheese manufacture Oxford Agar, and the resulting Listeria counts were
The raw milk (60 l) to be used in the cheese making combined. All plates were incubated aerobically at 37 ºC
was first tested for the presence of L. monocytogenes for 48 h and the typical colonies were counted. Samples
before inoculation. Confirmed milk samples were in which L. monocytogenes was not detected by direct
inoculated with L. monocytogenes to obtain a final plating were subjected to an enrichment procedure. This
concentration of ca. 3, 4, 5, and 6 log cfu ml-1 for groups included incubation of 25 g cheese samples in 225 ml of
1, 2, 3 and 4, respectively. Inoculated milks were heated Tryptone Soya Broth + 0.6% yeast extract (TSB, no.
up to 35 ºC in a stainless steel cheese vat and 4 ml of calf CM129, Oxoid; YE, no. L21, Oxoid) at 35 ºC for 48 h.
928
F. ÇET‹NKAYA, G. E. SOYUTEM‹Z
The enrichment culture was then plated on Oxford Agar Kashar cheese, which is usually produced from raw milk
medium and plates were examined for typical Listeria according to the traditional technique, are investigated.
colonies after 48 h incubation at 37 ºC. Selected colonies, To test the influence of cheese making technique and
which exhibited a gray-black color with a black halo, were ripening period on the survival of L. monocytogenes, 4
tested for morphology, catalase production, hemolysis, different inoculation levels were selected arbitrarily. The
motility, xylose, rhamnose and mannitol fermentation data on the behavior of L. monocytogenes during
(13,14). manufacture and ripening of Kashar cheese are shown in
Determination of pH the Table.
The pH was measured with an Orion pH-meter When the coagulum was heated at 41 ºC for ca. 30
(Ionalyzer model 399A/F, Cambridge, MA, USA) at 25 ± min, L. monocytogenes numbers remained nearly
1 ºC (15). constant. Following syneresis, with a decrease in pH to
5.03-5.07, the population in acidified curd was about
Statistical analysis 0.73-1.27 log cfu g-1 greater compared to that of the
The experiments were set up in a completely random inoculated milk. After heat treatment of curd at 75 ºC for
design with 3 replications. All data were subjected to approximately 5 min, L. monocytogenes inoculated in vat
analysis of variance using MSTAT-C (version 2.1- milk at levels of ca. 3 log cfu ml-1 was completely
Michigan State University 1991) and MINITAB (University eliminated. During heat treatment of curd (ca. 4, 5 and 6
of Texas at Austin) software. The significance of the log cfu ml-1) with initial high contamination of the cheese
differences between groups was determined at the 0.01 milk, a decrease in L. monocytogenes numbers of 1.77-
probability level, by the F-test. The F-protected least 2.34 log cfu g-1 was observed in groups 2, 3 and 4.
significant difference (LSD) was calculated at the 0.01 During the ripening period, L. monocytogenes was not
probability level. determined either by direct plating or enrichment
procedure in group 1. The pathogen numbers remained
nearly unchanged during the first 10 days of ripening in
Results
groups 2, 3 and 4. Meanwhile, L. monocytogenes counts
In the present study the survival and behavior of L. in the same groups decreased about 0.30-0.58 log cfu g-1
monocytogenes during the manufacture and ripening of on day 30 of ripening compared to populations of the 1-
Table. L. monocytogenes counts during manufacture stages and ripening period in Kashar cheese.
Group 1 Group 2 Group 3 Group 4
Mean ±  SEM Mean ±  SEM Mean ±  SEM Mean ±  SEM
Inoculated milk 3.43c ± 0.12 4.71b ± 0.07 5.22b ± 0.14 6.45a ± 0.12
Coagulum 3.58d ± 0.20 4.72c ± 0.08 5.54b ± 0.16 6.61a ± 0.20
Acidified curd 4.32d ± 0.09 5.44c ± 0.19 6.49b ± 0.18 7.48a ± 0.19
Heat-treated curd NDc 2.48b ± 0.32 3.45ab ± 0.32 4.11a ± 0.29
1 NDc 2.38b ± 0.32 3.45ab ± 0.31 4.14a ± 0.29
10 NDc 2.52b ± 0.34 3.58ab ± 0.33 4.24a ± 0.33
30 NDc 1.83b ± 0.44 2.87ab ± 0.15 3.84a ± 0.14
60 NDc NDb 2.14a ± 0.28 3.12a ± 0.34
90 NDc NDb 1.13b ± 0.58 2.87a ± 0.15
120 NDc NDb NDb 1.83a ± 0.09
a, b, c, d: Means having different letters within same row differ significantly (P < 0.01).
ND: L. monocytogenes not detected.                       SEM: Standard error of means.
929
Ripening period (day) Manufacture
stages 
A Study on Survival of Listeria monocytogenes during Manufacture and Ripening of Kashar Cheese
day-old cheese. Populations of the pathogen became During the ripening period, no bacteria were isolated
undetectable on days 60 and 120 of ripening in groups 2 on days 60 and 120 in groups 2 and 3, respectively,
and 3, respectively. Nevertheless, the pathogen counts whereas in group 4 even after 120 days of ripening 1.83
exhibited a 2.31 log cfu g-1 decrease at the end of log cfu g-1 bacteria remained viable. Decreases in viability
ripening in group 4, but the organism was still present in may be due to heat-injured L. monocytogenes becoming
cheese at a level of 1.83 log cfu g-1. more susceptible to the low pH of the cheese, which is
between 5.13 and 5.43 during the entire ripening
period. This phenomenon was also observed previously
Discussion
during the ripening of several cheese varieties. Patır and
As shown in the Table, we could not detect a clear Güven (21) indicated the survival of L. monocytogenes
difference in bacterial counts when the coagulum was for 120 days in brined fiavak cheese (pH 5.5 to 5.7)
heated to 41 ºC.  This can be explained by the prolonged produced from raw ewe’s milk, although the numbers of
lag phase of the bacteria in these conditions. In a previous the organism decreased gradually during cheese ripening
study, the authors determined that the lag phase for L. at 4 ºC. Ryser and Marth (17) also observed similar
monocytogenes strains Scott A, V7 and CA in sterile findings for Camembert cheese stored for 18 days at 6
whole milk incubated at 35 ºC was about 2 h (16). ºC. In that study, reductions in Listeria counts were
Therefore, growth during the early stages of cheese attributed to the pH of the cheese varying around 5.5.
manufacture would not be expected. Glass et al. (22) reported that L. monocytogenes counts
An approximately 1 log cfu g-1 increase was detected decreased by only 0.6 log10 cfu/g in cheese (pH 5.6 to
in L. monocytogenes counts in the curd kept at room 5.84, 2.3 to 2.6% salt) stored for 4 days at 30 ºC.
temperature for 16 h. The increase in L. monocytogenes However, Buchanan et al. (23) reported that the
counts can be correlated with the combination of a high organism exhibited a decrease of 4 log10 cfu/ml in brain
moisture content of curd and a pH value of around 6.0 at heart infusion broth (pH 5.0, acidified with 50 mM acetic
the beginning that decreased to 5.0 during curd acid) over 4 days at 28 ºC. These findings indicate that L.
acidification. Similarly, in studies on Camembert (17) and monocytogenes viability is dependent on incubation
Cheddar cheeses (18) L. monocytogenes counts increased temperature and medium composition; so the rate of
by 0.38-0.71 and 0.1-0.8 log cfu g-1, respectively, in the inactivation of the pathogen may also be affected by a
curd after pressing overnight at room temperature. combination of factors in cheese such as proteins, lipids,
Heat treatment of the curd in hot water (75 ºC) was water content, and pH. In addition, lactic flora during
found to constitute the most important barrier in the fermentation plays an important role in flavor, aroma
elimination of the pathogen. In group 1, where the initial and texture formation (24,25) and also in the
inoculation level was ca. 3 log cfu ml-1, no viable L. microbiological quality of cheese. Numerous reviews (26-
monocytogenes was found after this stage. In contrast, 31) have suggested that pathogens and spoilage
this heat treatment was not sufficient to eliminate the microorganisms in fermented foods may be inhibited
pathogen in groups 2, 3 and 4. This can be explained by during the growth of lactic acid bacteria. The major cause
the fact that although the temperature of the water used of this inhibition is suggested as being the production of
in heat treatment of curd is high enough to kill all the organic acids and, additionally, the secretion of metabolic
bacteria, heat transfer towards the curd core might be compounds such as hydrogen peroxide, diacetyl (26,32),
impeded by the massive structure of the curd block. In bacteriocins (33-36) and other low molecular weight
studies on Mozzarella cheese the authors reported that products (37).
even at high inoculation levels L. monocytogenes could be In conclusion, it can be stated that the temperature of
eliminated during the stretching process at 77 ºC for 1-4 curd heat treatment during Kashar cheese production
min (19,20). On the other hand, Villani et al. (14), does not represent a real control point for the complete
working on the elimination of L. monocytogenes during demise of the pathogen, especially when it is at the >3 log
the stretching of traditional Mozzarella cheese, reported cfu ml-1 level, and a combination of curd heat treatment
a decrease of about 2 log at 95 ºC. and a ripening period of at least 4 months is necessary to
930
F. ÇET‹NKAYA, G. E. SOYUTEM‹Z
eliminate L. monocytogenes when the cheese is produced contamination (6 log cfu ml-1) of L. monocytogenes and
from milk containing approximately 4-5 log cfu ml-1. that such cheese may pose an important risk to public
Furthermore, it is concluded that 4 months of ripening health.
for Kashar cheese is not sufficient to eliminate the high
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