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Some Microbiological and Pysico-Chemical Quality of Turkish Sucuk (Sausage)

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 Food Control 17 (2006) 923–928
www.elsevier.com/locate/foodcont

The microbiological quality and residual nitrate/nitrite levels

in turkish sausage (soudjouck) produced in Afyon Province, Turkey
a,*
Belgin Sırıken , Mehmet Özdemir b, Hidayet Yavuz b, Sebnem Pamuk c

a
Department of Food Hygiene and Technology, Faculty of Veterinary Medicine, University of Ondokuz Mayıs, Samsun, Turkey
b
Department of Pharmacology and Toxicology, Faculty of Veterinary Medicine, University of Afyon Kocatepe, Afyon, Turkey
c
Department of Food Hygiene and Technology, Faculty of Veterinary Medicine, University of Afyon Kocatepe, Afyon, Turkey

Received 3 March 2005; received in revised form 19 June 2005; accepted 20 June 2005

Abstract

To determine the microbiological quality, pH and residual nitrate/nitrite levels, a total of 100 soudjouck samples were randomly
purchased and analysed. Total number of aerobic bacteria and lactobacilli were found to be P107 and P108 cfu/g in 73% and 40% of
the samples, respectively. Twenty three percent of the samples contained P106 cfu/g micrococci/staphylococci while enterobacteri-
aceae, coliforms, enterococci and yeast/mould were detected in 15%, 11%, 41% and 17% of the samples, respectively at the level of
P104 cfu/g. Escherichia coli was found 5% of the samples. Nine percent of the samples contained coagulase positive staphylococci at
the level of 102 cfu/g. Bacillus cereus and sulphite-reducing anaerobic bacteria were not detected. The maximum levels of residual
sodium nitrate, sodium nitrite and pH values limited by Turkish Food Regulations are 250 ppm, 100 ppm and 5.8, respectively. In
this respect, 18% of samples for sodium nitrate, 11% of samples for sodium nitrite and 32% of samples for pH were found high.
 2005 Published by Elsevier Ltd.

Keywords: soudjouck; Microbiology; Residue; Nitrate; Nitrite

1. Introduction During fermentation, lactic acid-producing bacteria

(LAB) are important in controlling the bacterial growth
The Turkish sausage known as soudjouck is a kind of and toxin production. However, the fermentation pro-
fermented meat product and it is widely appreciated in cesses itself is not always capable to inhibit the growth
Turkey. Traditionally soudjouck preparation is based of pathogenic bacteria (Hill, OÕDriscoll, & Booth, 1995;
on natural fermentation by contamination of the envi- Leyer, Wang, & Johnson, 1995). An ability to resist acidic
ronmental flora of raw materials. Environmental con- conditions may allow food-borne pathogens to survive in
tamination occurs during slaughtering and increases fermented foods as well as in the gastrointestinal tract.
during manufacturing. Each processing facility has Increased resistance to acidic conditions of food-borne
own specific flora composed of various species of lactic pathogens such as Listeria (Hill et al., 1995; Uyttendaele
acid bacteria including enterococci and lactobacilli as & Debevere, 1999), Salmonella (Foster, 1991; Foster &
well as coagulase-negative staphylococci and yeasts, Hall, 1990) and E. coli O157:H7 (Garren, Harrison, &
etc. Thus, the characterization of the natural fermenta- Russel, 1998; Leyer et al., 1995) have been reported. Fur-
tive flora is crucial because safety and sensorial quality thermore, it has been also reported that the survival of
of the product. these food-borne pathogens have been demonstrated in
various kinds of sausage (Hill et al., 1995).
*
Corresponding author. Fax: +90 272 228 1235. Nitrite is a reactive chemical, and when used in
E-mail address: [email protected] (B. Sırıken). biologically complex meat systems undergo numerous

0956-7135/$ - see front matter  2005 Published by Elsevier Ltd.

doi:10.1016/j.foodcont.2005.06.011
924 B. Sırıken et al. / Food Control 17 (2006) 923–928

reactions. One of the reactive species formed subse- produced in various small-medium, large plants and
quently is nitric oxide, which is the active nitrosating butcher shops in Afyon or its vicinity. The samples were
agent. Most sausage formulas include sodium nitrite immediately analyzed for the presence of microorgan-
(NaNO2) as a curing agent. In rare instances, sodium isms, pH, and nitrate/nitrite values.
nitrate (NaNO3) is added during production rather than
sodium nitrite. The addition of nitrite to a meat product 2.2. Methods
inhibits the growth of the certain pathogens, particularly
Clostridium botulinum. Nitrite also functions as an anti- 2.2.1. Nitrate and nitrite
oxidant in cured meat and is responsible for the pink The nitrate and nitrite levels in soudjouck samples
coloration and a particular flavour to the sausage were determined by colorimetric method according to
(Cassens, Greaser, Ito, & Lee, 1979). Sen and Donaldson (1978).
Although useful as a curing agent, residual nitrite in
the meat poses a health risk to humans (Archer, 1982; 2.2.2. pH measurements
Borchert, 1998). The National Institute of Occupational Measurements were made using an electrode of pH
Safety and Health (NIOSH, 1997) reported that nitrite is metre (WTW, Inolab Level I, Germany) inserted
a primary irritant, carcinogen and mutagen and causes directly into soudjouck samples. Three independent
undesirable reproductive effects. If too much is added, measurements were made on each sample and mean
there is a risk for illness, even death of consumers values were calculated.
(Archer, 1982; Blot, Henderson, & Boice, 1999).
Traditionally manufactured soudjouck with long rip- 2.2.3. Microbiological analysis
ening time have more desirable sensory characteristics To determine the microbial counts of technological,
compared to those manufactured with starters and hygienic and pathogenic flora analysis of the soudjouck
produced in industrial scale as a consequence of the samples, the total aerobic bacteria, lactobacilli, micro-
composition and metabolic activity of the indigenous cocci/staphylococci, coagulase positive staphylococci,
microflora (Samelis, Metaxopoulos, Vlassi, & Pappa, enterobacteriaceae, coliforms, enterococci and mould/
1998). However, nowadays, traditional dry soudjouck yeast counts were obtained by the drop plating tech-
production has decreased in Turkey as well as in Afyon nique, B. cereus, and sulphite-reducing anaerobic bacte-
province that was a famous city for its traditional meat rial counts were carried out using the spread plating
products. soudjouck is today produced mostly by small, technique.
medium and large companies in Afyon province. Its For this purpose, 10 g soudjouck samples were asepti-
main ingredients are composed of ground beef, fat, salt, cally taken and transferred into sterile plastic bags
nitrate/nitrite, sugar, garlic, spices, starter culture and containing 90 ml peptone water (Oxoid CM 9,UK),
other additives. The mixture is stored at 4 C for 12– homogenized for 1–2 min (Interscience Bag Mixer
24 h and then finely ground before stuffing into natural 400). Following homogenization, 10-fold serial dilutions
cattle small intestine cases. After stuffing, the soudjouck were made in sterile peptone–salt water up to 10 7, and
is incubated overnight at room temperature for fermen- inoculated onto specific culture media for total aerobic
tation and then pasteurized by heating until its internal plate count (APC), lactobacilli (MRS), micrococci/
temperature reach to 65 C. Before its distribution and staphylococci (BP) (Baumgart, 1986), coagulase positive
sale, the soudjouck is let to cool down. staphylococci (Baird Parker Medium, Oxoid CM
Nowadays, consumersÕawareness of microbiological 275,UK), enterobacteriaceae (VG), coliforms (VL),
quality and residual nitrate/nitrite levels of soudjouck enterococci (SB), sulphite-reducing anaerobic bacterial
has increased in Turkey. Therefore, the present study counts (SPS), B. cereus (CSM) and moulds/yeasts
was designed to determine the microbiological quality, (RO). The culture media and incubation conditions
pH and residual nitrate/nitrite levels of widely consumed are shown in Table 1.
soudjouck because little data are available on these For the isolation of coagulase positive staphylococci,
parameters of the soudjouck produced in Afyon up to five typical colonies (black or grey colonies) grown
province. on BP agar were selected and, transferred to tubes con-
tained Brain Heart Infusion Broth (BHI-Oxoid CM
225,UK). The tubes were incubated at 37 C for 24 h.
2. Materials and methods After the incubation, coagulase tests were done (Thatcher
& Clark, 1978).
2.1. Materials For the isolation of E. coli, one presumptive colony
on VL agar was selected and directly streaked onto
A total of 100 fermented and heated natural gut Endo agar Base (EA, Oxoid CM 479, UK) and incu-
casing soudjouck samples were purchased from local bated for up to 48 h at 37 C. One suspected of being
butcher shops and retail markets. The sausages were E. coli on the EA was selected and identified by indole,
 B. Sırıken et al. / Food Control 17 (2006) 923–928 925

Table 1
The culture media for microbiological analysis and incubation conditions
Microorganisms Culture media Incubation Condition Anaerobic/
temperature C time (h) aerobic
Aerobic plate count Plate count agar (Oxoid, CM 325,UK) 30 C 48–72 Aerobic
Lactobacilli MRS agar (Oxoid CM 361) 30 C 24–72 Anaerobic
Micrococci/staphylococci Baird Parker agar (Oxoid CM 275, UK) 37 C 24–48 Aerobic
Enterobacteriaceae Violet red bile lactose glucose agar (Oxoid, CM 485, UK) 37 C 24–48 Anaerobic
Coliform Violet red bile agar (Oxoid CM 107) 37 C 24–48 Anaerobic
E. coli Endo agar base (Oxoid CM 479 UK) 37 C 24–48 Aerobic
Enterococci Slanetz and Bartley Medium (Oxoid CM 377) 37 C 24–48 Aerobic
B. cereus Bacillus cereus agar Base (Oxoid CM 617, suppl. SR 99) 30 C 24–48 Aerobic
Mould and yeast Rose Bengal Chloramphenicol agar (Oxoid CM 549, Suppl.SR 78) 25 C 3–5 d Aerobic
Sulphite-reducing Perfringens agar base (Oxoid CM 543), Supl. (A-SR 76, B SR 77) 37 C 24 h Anaerobic
anaerobic bacteria

methyl red, Voges Proskauer and Simmons citrate tests 41% of the samples, respectively at the level of P104
(IMViC tests). cfu/g. Escherichia coli was found 5% of the samples.
9% of the samples contained coagulase positive staphy-
lococci at the level of 102 cfu/g. However, B. cereus and
3. Results and discussion sulphite-reducing anaerobic bacteria were not detected.
Although S. aureus was suitably low in numbers, whilst
Various types of sausages are widely consumed in the E. coli (5%) were found to be above permitted Turkish
world and represent a source of some bacteria such as S. Food Regulations (2001) (Table 5). The maximum levels
aureus, E. coli, B. cereus, C. perfringens, enterobacteria- of residual sodium nitrate, sodium nitrite and pH values
ceae, coliforms and enterococci whose the presence have limited by Turkish Food Regulations (1997, 2001) are
been demonstrated by different studies (El-Gohary, 250 ppm, 100 ppm, and 5.8, respectively. In this respect,
1994; El-Khateib, 1997; Faith et al., 1998; Hill et al., 18% of the samples for sodium nitrate, 11% for sodium
1995; Leyer et al., 1995; Lotfi et al., 1998; Maciak & nitrite (Table 4), and 32% for pH (Table 3) were found
Sawicka-Wrzosek, 1996; Mousa, Awad, Yassien, & high.
Gouda, 1993; Sabioni, Pedrosa, & Leal, 1999; Simard, In the present study, 17% of the samples were found
Lee, Laleye, & Holley, 1983). In Turkey, there is little highly contaminated with yeast/mould at the level of
data of the microbial counts of technological, hygienic P104 cfu/g (Table 2) and 34% of the contaminated sam-
and pathogenic flora of the soudjouck. ples are considered as non-consumable products with
The microbiological results of analysis of the sou- relation to Turkish Food Regulations (2001) (Table 5).
djouck samples are showed in Table 2. Total number Several authors have reported the contamination of sau-
of aerobic bacteria and lactobacilli were found to be sage samples with moulds and mycotoxins in different
P107 and P108 cfu/g in 73% and 40% of the samples, countries. Mintzlaff, Ciegler, and Leistner (1972) re-
respectively. 23% of the samples contained P106 cfu/g ported that 88 out of 422 Penicillium, isolated from
micrococci/staphylococci while enterobacteriaceae, coli- mould-ripened sausages, were found to be toxin pro-
forms and enterococci were detected in 15%, 11%, and ducer. In another study, Hassan and Ragheb (1996)

Table 2
The microbiological results of analyzed soudjouck samples (%)
Number of microorganism (cfu/g) APC MRS BP CPS VG VL E. coli SB RO CSM SPS
2
<2.0 · 10 – 11 2 – 50 61 – 26 54 100 100
102–103 – 2 12 9 17 17 – 10 12 – –
103–104 – 2 14 – 18 11 – 23 17 – –
104–105 3 5 25 – 10 5 – 18 12 – –
105–106 12 7 24 – 5 5 – 13 5 – –
106–107 12 11 17 – – 1 – 4 – – –
107–108 13 22 5 – – – – 4 – – –
108–109 40 40 1 – – – – 2 – – –
109–1010 20 – – – – – – – – – –
Present – – – – – – 5 (5.0) – – – –
APC: Total aerobe mesophile plate count; MRS: Lactobacilli; BP: micrococci/staphylococci; CPS: Cagulase positive staphylococci; VG: entero-
bacteriaceae; VL: total coliforms; SB: enterococci; CSM: B. cereus; RO: mould and yeast count; SPS: Sulphite-reducing anaerobic bacterial counts.
926 B. Sırıken et al. / Food Control 17 (2006) 923–928

Table 3 bacteria, is inhibitory some food-borne pathogens such

Correlation between the number of Lactobacilli and final pH values of as Salmonella spp. and L. monocytogenes when they
soudjouck samples
reach at the level of 108 cfu/g (Baccus-Taylor, Glass,
Log10 of cfu/g of LAB pH value Total number Luchansky, & Maurer, 1993). Such food-borne patho-
(% of samples) of samples (%)
gens originally present in raw cured meat products are
7–8 (17.1) <5.1 20 not only inhibited but also decreased under unfavour-
4–8 (20.0) 5.1–5.4 28
5–8 (22.8) 5.4–5.9 20
able intrinsic factors during fermentation (Beumer, de
2–7 (31.4) 5.9–6.5 30 Giffel, de Boer, & Rombouts, 1996). However, in the
2 (8.5) 6.5–7.2 2 previous study, Salmonella spp. and L. monocytogenes
were detected in 7% of the samples when they contained
106–108 cfu/g of Lactobacillus spp. and their pH values
Table 4 varied from 4.9 to 6.5 (Siriken, Pamuk, Özakın, Gedi-
Nitrate and Nitrite Level of analyzed soudjouck samples (ppm) koǧlu, & Eyigör, in press). Similiar results have been re-
Level of nitrate Number of Level of Number of ported by Thévenot, Delignette-Muller, Christieans, and
samples nitrite samples Vernozy-Rozand (2005) and they showed that L. mono-
<50 3 <25 34 cytogenes counts remained unchanged from day 0 to day
51–100 15 26–50 18 5 during the fermentation. It is known that, weak acid
101–150 26 51–75 23 exists in pH-dependent equilibrium between undissoci-
151–200 29 76–100 14
ated and dissociated state (lactic acid pKa = 3.86). Lac-
201–250 9 101–278 11
251–300 8 tic acids produced by LAB in their undissociated form
301–367 10 can penetrate the microbial cell, reducing the intracellu-
lar pH (Baird-Parker, 1980) and thus disturb, in the case
of lower extracellular pH, the homeostasis of different
found that Aspergillus and Penicillium were the most pathogens (e.g. Salmonella spp., Clostridium spp.) as
predominant fungi isolated from sausages. well as spoilage bacteria (e.g. pseudomonads and entero-
The contamination of processed meat with myco- cocci) during fermentation (Lücke & Hechelmann, 1987;
toxin produced moulds is probably due to the addition Leistner, 2000). However, Lueck (1980) showed that
of spices to fresh meat, and it is also favoured by higher only 10% of lactic acid might remain undissociated,
pH (5.2–8.5), increased moisture (Hassan & Ragheb, resulting in a moderate inhibitory effect and a progres-
1996), and some curing agents such as sodium nitrite sive adaptation of the bacteria. According to the present
known as a stimulator of the aflatoxin production and previous studies, the high number of Lactobacillus
(Strzelecki, 1973). In our study, higher values of the and low pH value are not enough for eliminating or con-
pH and sodium nitrite, and the average moisture being trolling pathogenic bacteria during fermentation of
between 42 and 46% of the samples (data not shown) sausage.
indicate favourable environmental conditions for the In the present study, there is no correlation between
synthesis of mycotoxins. In this respect, the soudjouck the number of lactobacilli and final pH values (Table
represents a potential risk for the presence of mycotox- 3). This non-correlation might depend on different fac-
ins for consumers whilst potassium nitrate entirely tors; (i) addition of glucano delta lacton for decreasing
inhibited its synthesis (Strzelecki, 1973). the pH, (ii) addition of alkali phosphate for increasing
Minced muscle raw cured meat products such as dry the water holding capacity of the soudjouck, (iii) pasteur-
fermented sausage is in which the growth of lactic acid ization temperature for the elimination of pathogens in

Table 5
The Some microbiological criteria of soudjouck (heated) according to Turkish regulation
n c m M Maximum acceptable level of
Escherichia coli (cfu/g) 5 0 Not present pH Nitrate Nitrite
E. coli O157:H7 Not present 5.8 250 100
Staphylococcus aureus (cfu/g) 5 1 5.0 · 102 5.0 · 103 ppm ppm
Clostridium perfringens (cfu/g) 5 2 1.0 · 101 1.0 · 102
Salmonella (cfu) 5 0 25 gÕda Not present
Mould and yeast (cfu/g) 5 2 1.0 · 101 1.0 · 102
L. monocytogenes 5 0 Not present
n: number of samples;
c: the maximum number of acceptable samples contains microorganisms counts between m and M;
m: the maximum acceptable of microorganisms counts/1 g of number of samples (n–c);
M: the maximum acceptable of microorganisms counts/ 1 g of number of samples (c number).
 B. Sırıken et al. / Food Control 17 (2006) 923–928 927

the soudjouck, and (iv) addition of some antimicrobial targeted towards spoilage and pathogenic bacteria as
substances for eliminating microorganism, especially well as technological flora. In addition, it is necessary
yeast/moulds. Beside the number of LAB and low pH to improve hygiene in the processing facility by selecting
value, the characteristics of starter culture play an disinfection procedures adapted to fermentation
important role for controlling or eliminating pathogenic purposes.
bacteria during fermentation. In this respect, Meisel,
Gehlen, Fisher, and Hammes (1989) reported that mul-
tiplication of S. aureus in dry sausage can be markedly Acknowledgement
reduced by addition of adequate starter cultures. In
the contrary, Erol (1991) showed that the use of mixed This Project was supported by The Afyon Kocatepe
starter cultures for improving the microbiological stabil- University Research Fund.
ity of Turkish sausage was not an absolute safeguard
against food-borne bacteria. In addition to the use of
starter cultures, the pasteurization widely carried out References
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