MICROBIOLOGICAL PROPERTIES OF BEEF IN VARIOUS MEAT SHOPS

AT SEMARANG, INDONESIA

Nurwantoro, V. P. Bintoro, A. M. Legowo and A. Purnomoadi

Faculty of Animal Agriculture, Diponegoro University
Tembalang Campus, Semarang 50275 - Indonesia
Corresponding E-mail: [Link]@[Link]
Received March 30, 2012; Accepted May 14, 2012

ABSTRAK

Penelitian ini bertujuan untuk mengkaji kualitas bakteriologis daging sapi yang dijual di pasar-
pasar kota Semarang-Indonesia. Persyaratan kualitas daging sapi yang dijual di pasar-pasar Indonesia
adalah: (1) total plate count (TPC) maksimal 106 CFU/g, (2) total bakteri coliform maksimal 102
CFU/g, (3) total bakteri Escherichia coli maksimal 10 CFU/g, (4) total bakteri Staphylococcus aureus
maksimal 102 CFU/g dan (5) bakteri Salmonella negatif per 25 g (SNI 3932, 2008). Sampel-sampel
daging sapi yang diteliti diambil secara acak sederhana dari pasar tradisional, depot daging dan
supermarket. Hasil penelitian menunjukkan bahwa semua sampel daging sapi yang diuji tidak
memenuhi syarat secara mutlak berdasarkan ketentuan pemerintah Indonesia tentang kualitas daging
sapi. Semua sampel daging sapi yang diuji tidak diketemukan bakteri Salmonella. Kesimpulan, sampel
daging sapi yang diambil dari beberapa pasar, umumnya tidak dapat memenuhi lima syarat bakteriologis
secara mutlak.
Kata kunci: daging sapi, kualitas, mikrobiologis, pasar daging

ABSTRACT

The aim of the study was to assess microbiological properties of beef sold in various meat
shops in Semarang. There are five Indonesian goverment standard requirements to maintain the quality
of beef sold in Indonesia markets, as follows: (1) total plate count (TPC) for a maximum of 10 6 CFU/g,
(2) total coliform bacteria for a maximum of 10 2 CFU/g, (3) total Escherichia coli up to 10 CFU/g, (4)
total Staphylococcus aureus for a maximum of 102 CFU/g and (5) negative for Salmonella per 25 g
samples (SNI 3932, 2008). Beef samples were randomly taken from several traditional markets, meat
shops and supermarkets. The result showed that all samples did not contain Salmonella but still could
not meet one or some of the Indonesian government standard regulation. In conclusion, beef samples
gathered from some of the markets, generaly could not meet one or some of the five strictly
requirements of the bacteriological properties.
Keywords: beef, microbiological properties, meat shops

INTRODUCTION carcass washing equipments and water (Yoder et

al., 2010). Another microorganisms sources
Beef is a food that contains lots of nutrients, contamination were come from the workers at the
composed of water 73.1%; protein 23.2%; fat slaughterhouse, the process during distribution
2.8%; various minerals and vitamins (Williams, and until ready to consume (Aslam et al., 2009).
2007). The nutrients of beef is a suitable media Various researches in bacterial contamination
for microorganisms such as bacteria, molds and in beef have been done. Aslam et al. (2000)
yeasts (Aslam et al., 2000). Microorganisms reported that the number of coliform bacteria in
contamination in beef started from the ground beef in Pakistan varies from 1.7x10 5 to
slaughterhouse environment during slaughtering 3.2x105 CFU/g and mold from 1.0x104 to 3.2x104
(Whelehan et al., 1986) that was come from: the CFU/g. Sartika et al. (2005) reported that beef
cattle itself (skin and feces), manure, water and came from Cibinong and Bogor then being
feed as well as the transportation equipments measured in Bogor-Indonesia was containing E.
(Berry et al., 2010), rumen contents (bolus), coli bacteria; which 60% contamination came

Microbiological Properties of Beef (Nurwantoro et al.) 97

from water and 41.7% came from workers. Afterwards, beef samples were put in the cooler
Cohen et al. (2008) reported that 79 out of 150 box with the temperature about 5°C (Cohen et
beef samples contained fecal coliform bacteria, al., 2008). Beef samples were then examined at
[Link], S. aureus and Clostridium perfringens the microbilogy laboratory.
bacteria, also had aerobic bacteria 107 CFU/g.
Yanti et al. (2008) examined the bacteria content Bacteriological Analysis
in beef at Pekanbaru markets, Indonesia, that was Bacteria determination of beef samples was
about 9.7x105 CFU/g, while, the study in Bogor- done immediately after samples gathered (no
Indonesia was reported that beef contaminated by longer than 1 hour after sampling). The variables
coliform for 7.9x104 CFU/g and contaminated by for bacteria determination were included: total
E. coli bacteria for 3.0x104 CFU/g. Arifin et al. bacteria, total coliform bacteria, total E. coli
(2008) reported that the bacterial content in beef bacteria, total S. aureus bacteria and qualitative
samples were 1.0x107 CFU/g. Aslam et al. (2009) determination for Salmonella bacteria in
was successfully isolated E. coli bacteria from the accordance with the requirements of SNI 3932
slaughtering equipments and cow hide that have (2008). Bacterial culture was proceeded by serial
been skined. Masana et al. (2010) reported that 54 dilution. Mixed solution of 225 mL Buffered
samples of beef that come from the Peptone Water (BPW) 0.1% and 25 g ground beef
slaughterhouse in Argentina (slaughtering period samples were then diluted in a serial dilution with
of November 2006 up to April 2008) were dilution factor of 10 (Pao and Ettinger, 2009).
containing E. coli bacteria. Ingham et al. (2010) Pour plate method was used to determine
reported that beef has potential to get E. coli total bacteria. Nutrient Agar (NA) as a culture
bacteria and non fecal coliform bacteria media used for pour plate method was incubated
contamination at 35°C for 24-48 hours (Aslam et al., 2000). The
Indonesia government’s regulation on beef Most Probable Number (MPN) was used for
and carcass quality defined five strictly determination of total coliform bacteria. Brilliant
requirements as follows: TPC for a maximum 10 6 Green Lactose Bile Broth (BGLBB) as a culture
CFU/g, total coliform bacteria for a maximum 102 media used MPN method was incubated at 35°C
CFU/g, total E. coli bacteria up to 10 CFU/g, total for 24-48 hours. Afterwards, a confirmatory test
S. aureus bacteria for a maximum of 102 CFU/g was done using Lauryl Sulphate Tryptose Broth
and zero tolerant for Salmonella bacteria per 25 g (LSTB) as a culture media which had incubated at
samples (SNI 3932, 2008). If the bacteria content 35°C for 48 hours (SNI 2897, 2008). Pour plate
in beef samples exceeded from predetermined method also used for total E. coli bacteria
standard, therefore the beef is considered determination. Mac Conkey Agar (MCA) as a
prohibited to be consumed. A pathogenic bacteria culture media for pour plate method was
is also should be in zero tolerant contained in a incubated at 35°C for 24-48 hours (Fardiaz,
processed beef products due to it can cause food 1993). Confirmatory test was done using E. coli
intoxication for the consumer. The risk of broth (ECB) media which had been incubated at
potential bacteria contamination in beef is still 45.5°C for 48 hours (SNI 2897, 2008). The
threated the consumers. Therefore, the study was casting cup method was used for total S. aureus
done to give some information in microbilogical determination. Vogel-Johnson Agar (VJA) as a
properties in the meat shops at Semarang area. culture media for the casting cup method was
incubated at 35°C for 45 - 48 hours (Fardiaz,
MATERIALS AND METHODS 1993). Confirmatory test using Gram staining and
coagulate test were done afterwards (SNI 2897,
The samples collection 2008). There were two steps enrichment for
Beef samples were gathered from the qualitative Salmonella bacteria determination. Pre
traditional markets, meat shops and supermarkets enrichment using Lactose Broth (LB) as a culture
in Semarang city, Indonesia in February 2012. media had been incubated at 35°C for 24 hours,
Simple random method was used for gathered the followed by enrichment step using Selenite
beef samples (Mendenhall et al., 1971). Samples Cystine Broth (SCB) as a culture media that had
was collected two times. The first time was done been incubated at 43°C for 24 hours. Isolation and
at 15 selected locations and gathered in the identification method used Triple Sugar Iron Agar
morning. The second time was done at the three (TSIA) and Lysine Iron Agar (LIA) that had been
selected locations and gathered in the afternoon. incubated at 35°C for 24 hours. Salmonella

98 [Link] [Link]. 37(2) June 2012

Table 1. Total Bacteria and Salmonella Bacteria in the Qualitative Determination of Beef Samples in
the Morning

Total Bacteria Total Coliform Total E. coli Total S. aureus Salmonella

Source of Beef
(CFU/g) Bacteria (MPN/g) Bacteria (CFU/g) Bacteria (CFU/g) Bacteria
Traditional Markets
1. 2.8x106 >2.4x104 6.4x104 1.6x103 Negative
2. 2.9x106 >2.4x104 0 1.5x105 Negative
3. 3.1x107 >2.4x104 5.0x106 9.0x105 Negative
4. 1.1x107 >2.4x104 3.0x105 7.0x106 Negative
5. 1.5x107 >2.4x104 0 2.2x105 Negative
6. 5.2x107 >2.4x104 3.0x105 1.8x105 Negative
Meat Shops
1. 9.6x105 >2.4x104 0 8.4x104 Negative
2. 7.6x104 >2.4x104 0 0 Negative
3. 6.6x106 >2.4x104 8.0x104 3.2x105 Negative
Supermarkets
1. 2.3x104 2.3x102 0 6.0x103 Negative
2. 2.4x106 >2.4x104 1.1x106 1.4x104 Negative
3. 2.0x104 9.3x102 0 0 Negative
4. 5.8x104 9.3x102 0 1.5x105 Negative
5. 6.1x106 >2.4x104 2.4x104 1.2x105 Negative
6. 2.3x105 2.3x102 0 1.6x104 Negative

suspected colonies in a culture media were then 1.6x103 to 7.0x106 CFU/g, meat shops ranges
subjected to biochemical confirmatory tests (SNI from zero to 3.2x105 CFU/g and supermarkets
2897, 2008). ranges from zero to 1.5x105 CFU/g. Qualitative
test of Salmonella bacteria in all samples of beef
RESULTS AND DISCUSSIONS results are negative, whereas some bacterial
species identified are listed in Table 2. The most
Results frequent bacterial species identified were
Total viable bacteria calculated from samples Klebsiella pneumoniae. This study was also
of beef (morning samples) are presented in Table conducted on samples of beef in the afternoon,
1. Total bacteria in beef ranged from traditional from traditional market, meat shop and
markets 2.8x106 to 5.2x107 CFU/g, meat shops supemarket each as a single location (Table 3).
around 7.6x104 to 6.6x106 CFU/g and The results showed that the content of bacteria in
supermarkets around 2.0x104 to 6.1x105 CFU/g. ground beef samples were relatively higher in the
Total coliform bacteria in all samples of beef were afternoon than in the morning. Based on the
more than 102 MPN/g. Total E. coli bacteria in results of a qualitative test, all of beef samples
beef varied, from traditional markets ranged from were not found Salmonella bacteria, but based on
zero to 5.0x106 CFU/g, meat shops ranged from the testing it was identified several other bacterial
zero to 8.0x104 CFU/g and supermarkets ranged species (Table 3). The most frequent bacterial
from zero to 1.1x106 CFU/g. Total S. aureus species identified were Klebsiella pneumoniae.
bacteria in beef ranges from traditional markets

Microbiological Properties of Beef (Nurwantoro et al.) 99

Table 2. Bacteria Identified in Beef Samples in the Morning

Source of Beef Kinds of Bacteria

Traditional Markets
1. Staphylococos saprophyticus, Klebsiella pneumoniae, Enterobacter aglomerans
2. Proteus vulgaris, Staphylococcus saprophyticus, Citrobacter diversus,Enterobacter
aglomerans
3. Klebsiella pneumoniae, Staphylococcus saprophyticus,Citrobacter diversus
4. Klebsiella pneumoniae, Staphylococcus saprophyticus, Serratia liquefaciens
5. Pseudomonas aeruginosa, Klebsiella pneumoniae, Staphylococcus saprophyticus
6. Klebsiella pneumoniae, Pseudomonas aeruginosa, Citrobacter freundii,
Staphylococcus saprophyticus

Meat Shops
1. Proteus vulgaris, Staphylococcus saprophyticus, Klebsiella pneumoniae
2. Klebsiella pneumoniae, Enterobacter aerogenes
3. Klebsiella pneumoniae, Citrobacter diversus, Staphylococcus saprophyticus,
Streptococcus alpha

Supermarkets
1. Pseudomonas aeruginosa, Staphylococcus epidermidis, Staphylococcus saprophyticus
2. Klebsiella pneumoniae, Streptococcus alpha, Proteus vulgaris
3. Klebsiella pneumoniae, Citrobacter diversus
4. Klebsiella pneumoniae, Citrobacter diversus, Staphylococcus saprophyticus,
Staphylococcus epidermidis, Streptococcus alpha
5. Klebsiella pneumoniae, Providensia stuartii, Staphylococcus epidermidis
6. Klebsiella pneumoniae, Enterobacter aerogenes, Staphylococcus saprophyticus,
Proteus mirabilis

Discussions those from traditional markets. The system of

Based on the results, it can be concluded that meat sale in traditional markets is more open than
all of the beef samples which came from in the supermarkets. The consumer can easily
traditional markets, meat shops and supermarkets choose the meat by touching or holding it (Yanti
(in the morning and afternoon time gathered) et al., 2008). The system of meat sale in the
could not meet the five strictly requirements of supermarkets and meat shops are more strictly,
SNI 3932 (2008). Bacterial contamination in beef hygienic than in the traditional markets due to
that being sold in the markets were occurred from consumer had no opportunities to touch the meat.
the slaughterhouse. Yoder et al. (2010) reported The display room temperature in the
that the main source of bacterial contamination in supermarkets also always is maintained at the
carcasses at the slaughterhouse came from the temperature below 5°C. Whereas, the temperature
water and the slaughter equipments. Furthermore, for displaying in the meat shops and traditional
bacterial contamination would increase during markets is about 25°C. Low temperature proven
distribution of marketing. According to Aslam et can inhibit the growth of bacteria in meat.
al. (2000), the distribution methods, sales worker According to Birk et al. (2010) the majority of
and sale equipments are factors that can increase pathogenic bacteria in humans are sensitive to the
the number of bacteria contamination in beef media temperature of about 4°C. Jay et al. (2005)
samples. The quality of beef samples in general is reported that most of the meat microorganisms in
better from the meat shops and supermarkets than a refrigerator begin to grow in the temperature of

100 [Link] [Link]. 37(2) June 2012

Table 3. Bacteria Determination and Kinds of Bacteria Identified in the Afternoon

Total
Total Total E. coli Total S. aureus
Source of Coliform
Bacteria Bacteria Bacteria Kinds of Bacteria
Beef Bacteria
(CFU/g) (CFU/g) (CFU/g)
(MPN/g)
Traditional 7.2x107 >2.4x104 0 5.0x106 Klebsiella pneumoniae,
Market Staphylococcus epidermidis,
Enterobacter aglomerans
Meat Shop 3.0x107 >2.4x104 0 4.6x106 Klebsiella pneumoniae,
Providensia stuartii,
Streptococcus alpha,
Staphylococcus saprophyticus
Supermarket 1.2x106 2.4x103 1.0x103 1.6x106 Klebisella pneumoniae,
Providensia stuartii,
Staphylococcus epidermidis

5-7°C. Therefore, the display room temperature in Indarto who helped the bacteriological and
the markets should be always maintained at about chemical analysis of beef samples.
5°C to suppress the growth of microorganisms
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