Microbial contamination of raw meat and its environment in retail shops in Karachi, Pakistan

Abstract

This study was conducted to examine the frequency of contamination in retail meat available in Karachi, Pakistan.
Raw meat samples (250) and surface swabs (90) from meat processing equipment and the surrounding environment were analyzed for microbiological contamination.
Out of 340 samples, 84% were found to be contaminated with bacterial species, including Klebsiella, Enterobacter, Staphylococcus aureus and Bacillus subtilis. A total of 550 (66%) of the bacterial isolates were potential pathogens. Of these, 342 and 208 isolates were from meat and environmental samples respectively. Food-borne pathogens isolated from meat samples included Escherichia coli O157:H7, Listeria, Salmonella Enteritidis and Shigella species whereas environmental samples yielded Staphylococcus aureus and Shigella species. Four strains of Brucella species were also isolated from meat samples. Total aerobic counts ranged between 108 -1010 CFU/g or cm2. Resistance to a wide range of antibiotics was observed. Resistance rates to ampicillin, amoxicillin, novobiocin and cefaclor were from 62 to 75% in general. Thirty-three percent of Salmonella isolates were resistant to ampicillin. No quinolone resistance was observed. Biofilm formation was observed among 88 (16%) pathogenic bacteria including E. coli, Klebsiella, Enterobacter species and Staphylococcus aureus.
Food-borne pathogens found in retail shops could be sources for horizontal contamination of meat. Our data confirm the circulation of antibiotic resistant and biofilm forming pathogens in raw meat and its environment in retail shops in Pakistan, which could play a role in the spread of antimicrobial resistance amongst food-borne bacteria.

Full text

Original Article
Microbial contamination of raw meat and its environment in retail shops in
Karachi, Pakistan
Nafisa Hassan Ali1,2, Amber Farooqui1, Adnan Khan1, Ameera Yahya Khan1 and Shahana U.
Kazmi1
1Immunology and Infectious Diseases Research Laboratory, Department of Microbiology, University of Karachi, Karachi,
Pakistan
2Department of Pathology, Jinnah Medical and Dental College, Karachi, Pakistan
Abstract
Background: This study was conducted to examine the frequency of contamination in retail meat available in Karachi, Pakistan.
Methodology: Raw meat samples (250) and surface swabs (90) from meat processing equipment and the surrounding environment were
analyzed for microbiological contamination.
Results: Out of 340 samples, 84% were found to be contaminated with bacterial species, including Klebsiella, Enterobacter, Staphylococcus
aureus and Bacillus subtilis. A total of 550 (66%) of the bacterial isolates were potential pathogens. Of these, 342 and 208 isolates were from
meat and environmental samples respectively. Food-borne pathogens isolated from meat samples included Escherichia coli O157:H7,
Listeria, Salmonella Enteritidis and Shigella species whereas environmental samples yielded Staphylococcus aureus and Shigella species.
Four strains of Brucella species were also isolated from meat samples. Total aerobic counts ranged between 108 –1010 CFU/g or cm2.
Resistance to a wide range of antibiotics was observed. Resistance rates to ampicillin, amoxicillin, novobiocin and cefaclor were from 62 to
75% in general. Thirty-three percent of Salmonella isolates were resistant to ampicillin. No quinolone resistance was observed. Biofilm
formation was observed among 88 (16%) pathogenic bacteria including E. coli, Klebsiella, Enterobacter species and Staphylococcus aureus.
Conclusions: Food-borne pathogens found in retail shops could be sources for horizontal contamination of meat. Our data confirm the
circulation of antibiotic resistant and biofilm forming pathogens in raw meat and its environment in retail shops in Pakistan, which could play
a role in the spread of antimicrobial resistance amongst food-borne bacteria.
Key words: meat contamination, biofilm, antibiotic resistance
J Infect Dev Ctries 2010; 4(6):382-388.
(Received 21 October 2009 – Accepted 6 April 2010)
Copyright © 2010 Hassan Ali et al. This is an open-access article distributed under the Creative Commons Attribution License, which permits unrestricted use,
distribution, and reproduction in any medium, provided the original work is properly cited.
Introduction
Food-borne pathogens are the leading cause of
illness and death in developing countries costing
billions of dollars in medical care and medical and
social costs [1]. Changes in eating habits, mass
catering, complex and lengthy food supply
procedures with increased international movement
and poor hygiene practices are major contributing
factors [2]. Contaminated raw meat is one of the
main sources of food-borne illnesses [3,4]. The risk
of the transmission of zoonotic infections is also
associated with contaminated meat. International
food management agencies, especially the World
Health Organization (WHO), the Food and
Agriculture Organization and the International
Hazard Analysis Critical Control Point (HACCP)
Alliance have already provided guidelines to member
countries about safe handling procedures such as
HACCP and Good Manufacturing Practices (GMPs).
Karachi is a large city with a population of more
than 15 million. Due to overcrowding, poverty,
inadequate sanitary conditions, and poor general
hygiene, food-borne infections are on rise in the city
[5]. Raw meat available in open-air local retail shops
without appropriate temperature control is purchased
by approximately 23% households [6]. Despite
insufficient public health laboratories and inferior
clinical diagnostic settings, a number of studies
reporting outbreaks of infections somehow related
with poor hygiene and consumption of contaminated
food have been performed. In most cases, data are
loosely based on laboratory isolates which do not
reflect the actual ratio of food-borne infections;
however, a few community-based reports provide
evidence of several outbreaks caused by Salmonella,

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383
Shigella, E. coli and Listeria in Pakistan [7-9].
Moreover, antibiotic resistance levels are also
elevated among food-borne pathogens such as
Salmonella and Shigella [10,11]. It is not inevitable
to prove a direct role of drug resistance in bacteria
contaminating food items with increased clinical
cases of resistant infections, but the presence of such
bacteria in food items and their related environment
could play a role in the spread of antimicrobial
resistance amongst food-borne pathogens [12].
Therefore, to develop an effective strategy for
reducing resistance burden in the community, such
studies could provide useful information.
This study was conducted to investigate the
microbial quality of raw meat available in common
retail shops of Karachi and to determine the hygiene
status of various environmental factors associated
with meat shops and slaughter houses.
Material and methods
Samples
Thirty individual retail outlets located in Main
Saddar Market, a district south of Karachi, Pakistan,
were randomly selected for the study. A total of 340
meat and surface samples were collected. Out of the
340 samples, 250 were retail meat samples including
meat (n = 145), lungs (n = 30), spleen (n = 30), and
mucosal surfaces of intestinal tissue free from fecal
material (n = 45). Samples were collected within 12
hours post-slaughter and during early afternoons, in
order to minimize the microbial changes due to
environmental temperatures and post-slaughter
timings. Approximately eight samples were collected
from each outlet. Ninety environmental samples were
collected comprising surface swabs taken from 15-
20cm2 of the surface of meat-cutting equipment such
as knives, wooden boards, weigh scales and meat
mincers and from the surrounding environment with
a surface area of 30cm2 as shown in Table 1. From
two to five surface swabs were collected from each
outlet. Collection was dependent on the size of the
premises as well as on the cooperation of the shop
owners. Butchers working in these outlets lack
knowledge regarding the importance of disinfecting
and sanitizing; consequently, they clean their shops
once in 24 hours with detergent and water. No
sanitizer medium was used before sampling.
Environmental samples were taken using sterile
swabs in 3 ml of peptone water and transported to the
laboratory within one hour, of collection, and
processed within two hours.
Twenty-five grams of collected meat and organ
samples were weighed and transferred to sterile
flasks containing 100 ml of phosphate buffer saline
(PBS). Samples were homogenized using a meat
grinder under aseptic conditions. Environmental
swabs, kept in sterile glass tubes containing peptone
water, were inoculated on blood agar plates by direct
swabbing. To get a total viable count, samples were
further diluted serially in PBS and appropriate
dilutions were used to inoculate nutrient agar plates.
Except where indicated all culture media and
antibiotic disks were obtained from Oxoid
(Hamshire, UK).
Microbiological analyses
Diluted meat samples were inoculated on nutrient
agar by pour plate method for total viable count.
Plates were incubated at 37oC. For the isolation of
Gram-negative bacteria, samples were cultured on
Eosine Methylene Blue agar, MacConkey`s agar, and
Sorbitol MacConkey’s agar and incubated at 37oC
aerobically. For the detection of Salmonella, one
gram of each sample was also inoculated in Selenite
F broth (Difco, Michigan, USA) and incubated for 18
hours at 37oC. Tubes were further sub-cultured on
Xylose lysine deoxycholate medium and incubated
for 18 hours at 37oC. Sorbitol MacConkey’s agar was
especially used for initial screening of E. coli
O157:H7. Colourless, non-sorbitol fermenting
colonies were tested by serotyping. Sheep blood agar
(5%), Mannitol salt agar (Merck, Darmstadt,
Germany) and 6.5% NaCl Mueller Hinton agar were
inoculated and incubated at 37oC in a CO2 enriched
environment for the isolation and identification of
Gram-positive organisms.
For isolation of Brucella species, approximately
one gram of grounded meat samples were also
inoculated in 50 ml of brain heart infusion (Merck,
Darmstadt, Germany) and tripticase soy broth
supplemented with 5 µg/ml of nalidixic acid, 25
IU/ml bacitracin, 100 µg/ml cyclohexamide and 5I
U/ml of polymyxin B (Sigma, Hampshire, UK) and
incubated at 37oC under 5% CO2 enriched
atmosphere for one month. Broth cultures were sub-
cultured on a weekly basis on 5% sheep blood agar
[13].
To test for Listeria, nutrient agar plates were
incubated for additional two weeks at 37oC and
inspected for characteristic colonies. Additionally, 10
ml of trypticase soy broth supplemented with 25
µg/ml of nalidixic acid and 105 µg/ml of polymyxin
B was inoculated with one gram of meat and

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384
incubated at 37oC for two weeks. Sub-culturing was
performed every three days on 5% sheep blood agar.
Any Beta hemolytic colonies were subjected to
serotyping using Listeria O poly antisera (Becton
Dickinson, Oxford, UK).
Bacterial identification was conducted by
standard biochemical methods [13]. For Gram-
negative organisms, the identification battery
included oxidase, citrate, urea hydrolysis, sulphide
indole motility (SIM), and triple sugar iron (TSI). In
some cases, API 20E strips (bioMerieux, Inc. Polska,
Poland) were used for confirmation, whereas
identification of Gram-positive organisms was based
on Gram staining, catalase, tube coagulase, DNase
and characteristic pigment production. Serotyping
was performed for the identification of Salmonella,
Shigella and E. coli O157:H7 using specific antisera
(Becton Dickinson, Lahore, Pakistan. Antibiotic
susceptibility pattern was determined by Kirby Bauer
disc diffusion method [14] using a wide range of
commonly used antibiotics including ampicillin
(10µg), ofloxacin (5µg), cefaclor (30µg), amoxicillin
(25µg), trimethoprim (5µg), doxycycline (30µg),
cephalaxin (30µg), roxithromycin (30µg), novobiocin
(5µg), streptomycin (10µg), tetracycline (30µg),
lincomycin (10µg) and cefazolin (30µg). No control
strains were used.
Biofilm formation assay
Isolated bacteria were processed to determine
biofilm formation by crystal violet assay according to
Shanks et al. [15] with modifications. Twenty-four-
hour-old bacterial cultures with a final inocula of 1 x
106 in trypticase soya broth were dispensed into 96-
well polystyrene plates and incubated at 37oC for 24
and 72 hours. Plates were washed with PBS three
times, dried at 60oC and stained with crystal violet for
one minute. Later the wells were filled with 10%
glacial acetic acid and subjected to absorbance
measurement at 450nm. Absorbance (A450) more than
1 was considered as positive. Reference strain of
Pseudomonas aeruginosa (ATCC 27853) was used
as positive control.
Results
Meat and surface samples included in this study
showed high viable bacterial counts as shown in table
1. Gram-negative bacteria such as E. coli,
Enterobacter and Klebsiella predominantly
constituted the total viable count, whereas frequently
observed Gram-positive bacteria included Bacillus
subtilis, Micrococcus species, and Staphylococcus
species. In general, a total of 550 potential
pathogenic bacterial isolates were obtained from 340
samples collected, out of which 342 were
Samples
Sample type
No. of
samples (n)
Total
viable
count
(log of
CFU/g or
cm2)
Range of viable count (log of
CFU/g or cm2)
Maximum
Minimum
Retail Meat
Meat
145
10.2
10.5
5.2
Lungs
30
6.66
6.8
3.5
Spleen
30
6.2
6.9
2.2
Intestinal
tissue
45
8.7
9.2
8.1
Surface swabs
from meat cutting
equipments
Knives
25
10.2
10.7
7
Weighing
scales
7
9.2
9.6
8.9
Wooden
boards
20
8.5
10.1
5.2
Meat mincer
4
7.5
7.2
7.6
Surface swabs
from environment
Customer
platforms
22
5.0
3.4
6
Floors
4
8.6
7.2
9.8
Walls
4
7.0
7
7.2
12 inch long
Steel meat
anchors
4
8.2
8.5
5
Table 1. Aerobic mesophils counts on meat and environmental samples of retail shops in Karachi, Pakistan
g – gram, CFU - Colony
forming unit

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385
isolated from meat samples and 208 from surface
swabs. As shown in table 2, out of 342 bacterial
pathogens isolated from meat samples, 120 (35%)
were identified as Escherichia coli and 51 (15%) of
these E coli isolates were characterized as serotype
0157;H7, which is known to cause hemorrhagic
colitis. Other potentially pathogenic isolates were
Listeria species 14 (4%), Klebsiella 27 (8%),
Enterobacter species 51 (15%), and Staphylococcus
aureus 24 (7%). Table 2 shows the detailed
distribution of potential pathogens in meat samples
and environmental surface swabs.
Antibiotics susceptibility profile showed the
prevalence of cefazolin, lincomycin, streptomycin
and tetracycline resistance against all potentially
bacterial pathogens (Figure 1). Resistance against
ampicillin, amoxicillin, novobiocin and cefaclor was
observed 72%, 75%, 70% and 62% respectively.
Fifty percent of the isolates were resistant against
roxithromycin whereas 33% were resistant against
cephalxin. No quinolone resistant pathogen was
isolated. Methicillin and vancomycin resistance was
not observed. Table 3 illustrates the rate of antibiotic
resistance among commonly isolated bacteria.
The presence of antibiotic resistant pathogens in
retail meat and its associated environment further
stimulated interest to determine their biofilm
formation ability. A total of 88 (16%) isolates were
able to form biofilm. Biofilm formation was
predominantly observed in enteric bacteria including
E. coli (n = 35), Klebsiella species (n = 38), and
Enterobacter species (n = 25). A few Staphylococcus
aureus (n = 16) isolates were also able to form
biofilm.
Discussion
Observations showed heavy bacteriological load
carried by meat carcasses with total viable counts
ranging from 106 –1010 CFU/g. The presence of a
high number of viable bacteria, an indicator of he
expected shelf life of meat, increases the chances of
meat spoilage in a short time as described by the
Agriculture and Consumer Protection Department;
FAO
(http://www.fao.org/DOCREP/004/T0279E/T0279E0
3.htm, last accessed April 01, 2010). Similar
observations are also recorded from neighboring
countries, namely India and Bangladesh [3,16].
The presence of bacteria in meat has been widely
reported from different parts of the world [17,18].
Some groups recognized the presence of viable
bacteria, especially Gram-negative organisms from
106 to 109, as an indication of open-air meat spoilage
[19], while others argued this assertion and
considered the presence of a high number of
background organisms as a pathogen-reduction
strategy due to the organisms’ antagonistic effect
against pathogenic bacteria and thus safer for meat
quality. Therefore, it is considered that fresh meat
that contains 105–106 of background organisms are
inherently safer than those that contain less bioload;
however, this hypothesis applies only to harmless
bacteria [20]. In order to address the issue in the view
of our local scenario, the organisms were identified.
Results indicated the predominance of Gram-
Microorganisms
Number of pathogenic isolates
(n) from
Meat samples
Surface swabs
Escherichia coli
120(35)
50 (24)
Escherichia coli
O157:H7
51 (15)
ND
Listeria
14 (4)
ND
Klebsiella
27 (8)
33 (16)
Enterobacter
51 (15)
50 (24)
Staphylococcus
aureus
24 (7)
31 (15)
Salmonella
Enteritidis
24 (7)
ND
Shigella
27 (8)
4 (2)
Brucella
4 (1)
ND
Citrobacter freundii
ND
17 (8)
Kurthia
ND
11 (5)
Sporosarcina
ND
12 (6)
Total
342
208
Table 2. Frequency of potential bacterial pathogens in
samples
Figure 1. Antibiotic resistance profile of bacterial
pathogens isolated from meat and environmental samples
Numbers in parentheses represent percentages; ND – not detected

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386
negative organisms such as Salmonella, Shigella, and
Escherichia coli as reported by other groups [21].
These organisms are already involved in various
infectious disease outbreaks in Karachi [22-24]. The
presence of zoonotic bacteria such as Brucella and
Listeria indicates poor ante-mortem inspection of the
animals as well as unhygienic meat processing
[25,26].
The frequency of potential pathogens in the
surrounding environment and surfaces of retail shops
was also examined. High viable counts and the
presence of potential pathogens on meat-processing
equipment, as well as on the walls and floors of retail
shops, represent their environmental hygiene status.
However, it is interesting to note that consumer
platforms or counters of the shops were cleaner than
the floors and walls with an average of 105 CFU per
cm2, which might be due to mopping of this area
several times in a day. The presence of bacterial
pathogens in meat-processing equipment and
associated surfaces may contribute to the
contamination of meat. Previously, it has been
demonstrated that mincing meat with dirty equipment
significantly increases the level of contamination in
minced meats as compared to that in whole carcasses;
furthermore, the process of mincing has the potential
to introduce pathogens such as Listeria
monocytogenes [27]. On the other hand, food-borne
pathogens which are able to disseminate from
contaminated meat to such surfaces [28] can spread
infections in the community.
It is already known that bacteria form biofilm on
hydrated surfaces [29]. Biofilm forming bacteria are
usually resistant to a wide range of antibiotics
[30,31]. To find the prevalence of drug resistance
bacteria, assays for susceptibility profiles and
biofilm formation were performed. Resistance of
bacterial isolates to a battery of available antibiotics
and the biofilm formation ability of these isolates was
commonly observed. The problem may be attributed
to a number of possible sources, including the natural
resistance of species to certain antibiotics [31],
possible transfer of antibiotic resistance among
species, and the use of sub-therapeutic doses of
antibiotics in animal feeds to improve animal
productivity, which could also select for resistant
strains [11]. However, no control strains were used
for antibiotic susceptibility profiles, which can be
considered as limitation of the study to reach valid
conclusion.
This study presents the contamination status of
retail meat and its surrounding environment as well
as demonstrates the role of raw food as a reservoir of
antibiotic resistance bacteria that can be transferred to
humans, thereby constituting a health problem. The
application of hygiene practices along the food chain
and prudent use of antibiotics in animal husbandry
are therefore essential to control further emergence of
antibiotic resistance.
According to an FAO survey conducted in 1996,
meat output in Pakistan is increasing day by day, in
response to growing domestic demand (Meat and
meat products, FAO,
http://www.fao.org/docrep/004/w1690e/w1690e11.ht
m Last accessed April 02, 2010). Therefore it is
important to ensure the practice of WHO basic
hygiene principles, which cover food safety
procedures from the farm of origin, to ante-mortem
and post-mortem inspection, to handling until the
food is consumed. The scientific community should
join regulatory authorities to spread awareness about
basic hygiene principles. It is especially important to
Antibiotics
E. coli (n = 170)
E. coli O157:H7
(n = 51)
Klebsiella
(n = 60)
Enterobacter
(n = 101)
Salmonella
(n = 24)
n
%
n
%
n
%
n
%
n
%
Amplicillin
122
71
35
69
60
100
76
75
8
33
Amoxicillin
124
73
32
62
58
97
76
75
8
33
Cefaclor
102
60
26
51
50
83
55
55
5
21
Ofloxacin
0
0
0
0
0
0
0
0
0
0
Trimethoprim
25
15
10
20
10
17
20
20
4
17
Doxycycline
51
30
15
29
15
25
36
36
6
25
Cephalaxin
60
35
17
33
18
30
35
35
5
21
Roxithromycin
55
32
26
51
28
47
39
39
6
25
Table 3. Distribution of antibiotic resistance among commonly isolated Gram-negative bacteria from meat and environmental
samples

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provide training to meat handlers regarding food
safety.
Acknowledgement
We would like to acknowledge our colleagues Sania Siddiq
and Sabiha Shaheen for their help. This work was supported by a
grant from the Dean, Faculty of Science, University of Karachi,
Pakistan.
Conflict of Interest: No conflict of interest is declared.
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Corresponding author
Amber Farooqui
Room 214 Immunology and Infectious Diseases Research
Laboratory
Department of Microbiology
University of Karachi
Karachi-75270, Pakistan
Phone: +9221-9261389, Fax: +9221-9261077
Email: amberfarooqui@hotmail.com
Conflict of Interests: No conflict of interests is declared.