Hindawi
Journal of Food Quality
Volume 2021, Article ID 6666683, 7 pages
https://doi.org/10.1155/2021/6666683
Research Article
Bacteriological Analysis of Raw Beef Retailed in Selected Open
Markets in Accra, Ghana
Michael Olu-Taiwo, Prince Obeng, and Akua Obeng Forson
Department of Medical Laboratory Science, School of Biomedical and Allied Health Sciences, College of Health Sciences,
University of Ghana, Legon, Accra, Ghana
Correspondence should be addressed to Akua Obeng Forson; obeng.akua@yahoo.com
Received 22 October 2020; Revised 5 February 2021; Accepted 4 May 2021; Published 13 May 2021
Academic Editor: Efstathios Giaouris
Copyright © 2021 Michael Olu-Taiwo et al. +is 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.
Beef is an important and popular source of protein and nutrients. Constant monitoring and evaluation of the microbiological
contamination is pertinent for its safety and quality. +is study aimed to assess the bacteriological profiles and the bacterial loads
in beef, as well as investigate food safety practices among beef retailers in selected open markets in Accra, Ghana.+is was a cross-
sectional study with beef samples randomly purchased from six selected open markets in Accra metropolis. Beef samples were
examined for total aerobic count (TAC) and total coliform count (TCC). Bacterial identification was performed by standard
bacteriological methods and a well-structured questionnaire was administered to assess food safety and hygienic practices of beef
retailers. Overall, mean TACs ranged between 2.2×103 and 1.3×104 CFU/g, while mean TCCs ranged between 1.9×102 and
7.4×102 CFU/g. Beef samples were mostly contaminated with Staphylococcus spp. (34%), Klebsiella oxytoca (17%), Enterobacter
spp. (15%), and Proteus vulgaris (3%).+is study showed varying levels of bacterial contamination of retailed beef sold in different
Accra markets. According to the Health Protection Agency guidelines for assessing microbiological safety of ready-to-eat foods,
our mean TACs were satisfactory, while mean TCCs were within borderline quality. +e results of this study revealed that the
majority of beef vended in open markets in Accra is contaminated with coliform and pathogenic bacteria. +erefore, more
training in safe food handling and good hygiene practices is required for beef retailers. Conclusively, effective monitoring of the
bacteriological profiles and bacterial loads of meat and meat products in abattoirs and points of sale should be established, since
such a continuous monitoring system could help prevent potential health problems for consumers and provide information on
possible sources of meat borne intoxication and infection.
1. Introduction contamination at different stages of processing, from per-
sonnel and during transportation [4, 5]. +e incidence of
Beef (meat) is a nutritive-rich food that contributes vital beef contamination and related illnesses worldwide has led
proteins, vitamins, and minerals to higher bioavailability to an increase in public health concern related to meat safety
than other food sources [1, 2]. In most developed countries, in both developed and developing countries [6]. In 2015, a
beef constitutes a significant part of the normal diet and report by the World Health Organization (WHO) docu-
contributes more than 15% energy, 40% protein, and 20% mented that 600 million foodborne illnesses were respon-
fat. +e demand for meat in developing countries has sible for 420,000 deaths in 2010 [7]. Furthermore, in 2016,
continuously grown as the production and consumption the Centers for Disease Control and Prevention [8] reported
pattern of meat increases with the availability of income [3]. that a total of 839 cases of foodborne disease outbreaks
However, meat has been found to be a prime vehicle for the cumulated in 14,972 illnesses, 794 hospitalizations, and 17
dissemination of foodborne pathogens to humans.+e water deaths with 18 food products. In Pakistan, the microbial load
content activity of fresh meat and its neutral pH play a vital of rawmeat at abattoirs and retail outlets in different areas of
role in the growth of microbes. Beef may be susceptible to Lahore had been reported as a mean aerobic count of 7.15,
2 Journal of Food Quality
6.92, and 6.62 log CFU/cm2 and 5.35, 5.42, and 4.84 log
CFU/cm2 for beef, sheep, and goat meat at abattoirs and
retail outlets, respectively, with a prevalence of 45%, 51%,
and 18% for Escherichia coli, Staphylococcus aureus, and
Salmonella spp., respectively [9]. In Egypt, a study moni-
tored the bacterial contamination during different stages of
beef carcass preparation at an abattoir and found surface
counts to exceed 106 CFU/cm2 [10]. In India, a study de-
termined the microbiological quality of meat collected from
municipal slaughterhouses and retail meat shops revealed
29.7% of the samples had exceeded the legislative limit of
104 CFU/g, with varying prevalence for Escherichia coli
(10%), Staphylococcus aureus (8.3%), and Salmonella spp.
(5%) [11]. In Ghana, a study determined the microbiological
quality of fresh meat from retail outlets in the Northern
Region of Ghana and revealed mean total aerobic counts of
5.74 106 CFU/cm2, 7.58 106 CFU/cm2, and Figure 1: +e typical state of a beef retail joint.× ×
8.85×106 CFU/cm2 for morning, afternoon, and late af-
ternoon samples, respectively [12]. However, there is a lack hygienic handling of used materials such as knives and
of periodic monitoring of raw meats and limited informa- water.
tion on the bacteriological nature of meat and meat products
in open markets. +is study aimed to assess the bacterio-
logical profiles and loads of raw beef sold in open markets in 2.4. Bacteriological Analysis of Samples. Approximately 10 g
the Accra metropolis and to investigate food safety practices of raw beef sample was added to 90ml of 0.1% buffered
among beef retailers in order to provide additional infor- peptone water (Oxoid, UK) to prepare homogenate sus-
mation to inform policies to protect public health. pension in a stomacher bag (Seward, UK), followed by
tenfold serial dilutions (10−2 to 10−4) as described by
2. Materials and Methods Clarence et al. [14]. An aliquot of 0.1 ml from each serial
2.1. Study Area. +e study was conducted in the Greater dilution was inoculated onto plate count agar (Oxoid,
Accra Region which is the smallest among the 16 admin- UK), blood agar (Oxoid, UK), and MacConkey agar plates
istrative regions in Ghana. It occupies a total land surface of (Oxoid, UK), employing the spread plate method for total
3,245 km2 or 1.4% of the total land area of Ghana. However, aerobic count (TAC) and total coliform count (TCC).
in terms of population, it is the second only to the Ashanti Inoculation was done in triplicate and the plates were°
Region, with an estimated urban population of 2.5 million, incubated at 37 C for 24–48 hours. Enumeration of col-
accounting for 15.4% of Ghana’s total population [13]. Accra onies took place on plate count agar (TAC) and Mac-
metropolitan markets used for this study included Makola, Conkey agar (TCC). Furthermore, dilutions that resulted
Kaneshie, Agbogbloshie, Malata, Maamobi, and Nima in 30–300 colonies were considered countable and were
markets. included in the calculations. For bacteria identification
purpose, 3-4 well-isolated colonies were obtained from
primary cultures by subculturing and checking for purity
2.2. Study Design and Sample Collection. +is was a de- onto MacConkey agar (Oxoid, UK) and blood agar
scriptive cross-sectional study of retailed beef in some open (Oxoid, UK). +e identification of pure culture colonies
markets in the Accra metropolis (Figure 1 (A)). One hun- was based on colonial morphology, Gram staining, and
dred (100) beef samples were randomly purchased from each biochemical reactions of triple sugar iron (TSI), oxidase,
of the six selected openmarkets within the Accra metropolis, coagulase, citrate utilization, urease, and indole tests [15].
Makola (10), Kaneshie (15), Agbogbloshie (20), Malata (25), API 20E identification system (bioMerieux SA, Marcy-
Maamobi (10), and Nima (20) markets. Purchased beef l’Etoile, France) was also used to confirm the Gram-
samples were aseptically collected in sterile zip loc bags negative isolates.
(Kolysen, China), sealed, and transported in an ice chest
within 2 hours to the University of Ghana School of Bio-
medical and Allied Health Sciences Microbiology Labora-
tory for bacteriological analysis. 2.5. Statistical Analysis. Bacterial counts were calculated as
colony forming units per gram (CFU/g) and then converted
into log10 values. Descriptive statistics were computed
2.3. Survey Questionnaire. Additionally, a well-structured using the Microsoft Excel data analysis Fischer’s exact chi-
questionnaire was used to obtain data relevant to food square and one-way ANOVA was analyzed using Graph-
safety awareness from retailers. +e main areas of assess- Pad Prism software, version 6, to find any statistical dif-
ment were processing, storage, selling conditions, personal ferences. Statistical significance was set at a P value of <
and environmental hygiene, and waste disposal as well as 0.05.
Journal of Food Quality 3
3. Results may influence retailers’ acceptability of modern and more
effective ways of safety practices as well as their adherence to
3.1. Bacteriological Counts. Overall, mean TACs of sampled strict hygienic and standard slaughtering practices. Bhan-
beef ranged between 2.19×103 and 1.26×104 CFU/g. dare et al. [18] have highlighted that most abattoir and retail
Makola market had the highest mean TAC of beef workers in developing nations are mostly untrained and
1.26×104 CFU/g, while Nima market had the least mean ignorant of hygienic standards that may alleviate bacterial
TAC of 2.19×103 CFU/g (Table 1). Mean TCCs ranged contamination of beef products.
between 1.9×102 and 7.4×102 CFU/g. Maamobi market In the present study, 70% of beef retailers were licensed,
recorded the highest mean TCC of 7.4×102 CFU/g, while whereas 25% did not possess any formal proof of evidence
Agbogbloshie market recorded the lowest mean TCC of (e.g., professional license) or other legal binding state
1.9×102 CFU/g. +ere was a statistically significant differ- documents for doing business. Contrary to this study
ence between the mean TCCs of Maamobi and Agbog- findings, Mcarthur-floyd et al. [19] in Madina, Accra,
bloshie (P< 0.05) (Table 1). evaluated the practice of food safety among fast-food op-
erators and reported the possession of health license by all
3.2. Prevalence of Bacteria Isolated from Various Market fast-food operators surveyed. Furthermore, their findings
Locations. Overall, a total of 110 bacterial isolates were revealed that the food inspection agencies are more stringent
recovered from sampled raw beef. +e following bacteria on ready-to-eat food sellers as compared to retailers of raw
were isolated: Acinetobacter spp. (1.8%), Citrobacter spp. and uncooked food commodities such as beef retailers.
(1%), Citrobacter diversus (8.2%), Enterobacter spp. (15.5%), Moreover, in our study, 87% of beef retailers admitted re-
Klebsiella spp. (13.6%), Klebsiella oxytoca (17.3%), Proteus frigerating beef products as a form of storage; however, 10%
vulgaris (2.7%), Staphylococcus aureus (6.4%), and Staphy- used freezers to store their meats. Most of the beef retailers
lococcus spp. (33.6%). admitted employing traditional or other nonconforming
+e majority of bacteria identified were recovered from means such as salting and usage of antibiotics in order to
Agbogbloshie market (23.6%; 26), followed by Kaneshie preserve meat.With regard to the usage of water for cleaning
(20%; 22), Nima (20%; 22), and Malata (20%; 22) markets. purposes, 25% of beef retailers made use of well water for
+e least number of bacteria was isolated from Makola washing of meat, whereas this practice may be considered
(8.2%) and Maamobi markets (8.2%), respectively (Table 2). worrisome in terms of cross-transmission of meat withpathogenic bacteria. A study conducted by Ngwa and
Chrysanthus [20] on the usage of well water revealed that
3.3. Demographics and Food Safety Awareness of Beef this type of water is highly contaminated with bacteria of
Retailers. Overall demographics, educational status, and fecal origin such as Klebsiella spp. (95%) and Escherichia coli
food safety awareness of beef retailers are summarized in (52%), as well as pathogenic bacteria like Salmonella typhi
Table 3. With respect to what causes diseases, 80% were (32.5%). Additionally, salting as a means of preservation for
aware that microorganisms are responsible for diseases, meat is not only inadequate but also could predispose
while 18% said they were not aware of what causes diseases. consumers to health risks such as high blood pressure and
In terms of inspection, sampling, and control by health other cardiovascular diseases [21]. +e combined retailing of
authorities, 85% of the respondents claimed to have regular beef along with other meats like chevron, chicken, and
experience in the matters, while 8% rarely confront that mutton may facilitate cross-contamination with microor-
issue. With regard to handwashing practices, 96% said they ganisms, due to the fact that contamination of meats may
washed their hands after using the urinal and toilet, while 4% occur through different meat sources [22]. In this study,
responded that such measures were not necessary. some retailers were not alarmed by the presence of increased
bacterial loads in meat, since they believed that cooking
4. Discussion would eradicate the organisms present. However, Prescott
and Klein [23] have reported that most strains of Staphy-
In this study, 60% of beef retailers were male and 40% were lococcus aureus implicated in staphylococcal enteritis are
female, and while 65% of the retailers were within the age responsible for the synthesis of extracellular toxins, which
range of 16–35 years, 35% were above 35 years. +ese are actually heat-resistant proteins that remain pathogenic
findings are in agreement with a previous study by Adzitey when consumed even in cooked foods [23].
et al. [16], where it was reported that butchering and retailing +e general indicators of the microbiological food
of beef were mostly practiced by the youth and middle-aged quality are TAC under favorable conditions that may en-
men, since the beef retailing business may be physically hance the multiplication of microorganisms [24]. In this
exhaustive. With regard to the education level of the beef study, an overall, mean TAC of beef in the surveyed markets
retailers, primary education accounted for 50%, followed by in Accra ranged between 2.19×103 and 1.26×104 CFU/g
secondary (35%), and tertiary (15%) education, respectively. (3.34–4.1 log CFU/g). +ese findings are comparable to
+ese findings are in agreement with a previous study by another Ghanaian study by Soyiri et al. [25] which revealed a
Adzitey et al. [17] conducted in the Northern Region of TAC range of 1.9×102–2.3×104 CFU/g in retailed beef. In
Ghana, which reported that 62% of respondents possessed contrast, a higher mean TAC of 2.5×105–2.25×108 CFU/g
an elementary form of education. +e standard of education and 2.7×104–2.0×108 CFU/g was reported by Jahan and
is pertinent to the awareness of beef safety practices, since it Siddique [26] in Bangladesh and Erdem et al. [27] in Turkey,
4 Journal of Food Quality
Table 1: Bacterial counts of beef from various markets.
Locations N Mean TACCFU/g Mean Log10 Mean TCCCFU/g Mean Log10
Mokola 10 1.26×104 4.1 363 2.56
Kanashie 15 4.79×103 3.68 316 2.5
Agbogloshie 20 3.09×103 3.49 191 2.28∗
Malata 25 3.0×103 3.47 468 2.67
Maamobi 10 4.9×103 3.69 741 2.87∗
Nima 20 2.19×103 3.34 372 2.57
Total 100
∗P< 0.05.
Table 2: Occurrence of bacterial isolates from various markets.
Markets No. of samples taken List of bacteria recovered No. of isolates Total %
Klebsiella spp. 1
Klebsiella oxytoca 5
Makola 10 Proteus vulgaris 1 9 (8.2)
Staphylococcus aureus 1
Staphylococcus spp. 1
Citrobacter diversus 1
Enterobacter spp. 2
Klebsiella spp. 1
Kaneshie 15 Klebsiella oxytoca 9 22 (20)
Proteus vulgaris 2
Staphylococcus aureus 4
Staphylococcus spp. 3
Citrobacter diversus 1
Enterobacter spp. 5
Agbogbloshie 20 Klebsiella spp. 3Klebsiella oxytoca 2 26 (23.6)
Staphylococcus aureus 1
Staphylococcus spp. 14
Citrobacter diversus 3
Enterobacter spp. 1
Malata 25 Klebsiella spp. 7Klebsiella oxytoca 2 22 (20)
Staphylococcus aureus 1
Staphylococcus spp. 8
Acinetobacter spp. 1
Maamobi 10 Citrobacter diversus 2 9 (8.2)
Staphylococcus spp. 6
Acinetobacter spp. 1
Citrobacter spp. 1
Citrobacter diversus 3
Nima 20 Enterobacter spp. 8 22 (20)
Klebsiella spp. 3
Klebsiella oxytoca 1
Staphylococcus spp. 5
respectively. +e International Commission on Microbio- According to Health Protection Agency guidelines for
logical Specification for Foods (ICMSF) has proposed that assessing the microbiological safety of ready-to-eat foods
ready-to-eat foods with TAC between 0 and 103 CFU/g are [30], our mean TAC was satisfactory, while the mean TCC
considered acceptable, within 104–105 CFU/g are considered findings were within borderline quality and signals that the
tolerable, and ≥106 CFU/g are considered unacceptable [28]. hygiene of practices of meat handling and processing along
+erefore, the level of contamination in this study could be the meat production chain must be urgently improved.
considered tolerable based on the recommended standards. +erefore, considering the rather limited number of samples
Our mean TCC of beef surveyed ranged between 1.9×102 analyzed from selected locations and the varying environ-
and 7.4×102 CFU/g. In a similar study by Koffi-Nevr et al. mental conditions for some retail joints, there is a certain
[29], a TCC of 1.6×102–4.0×102 CFU/g was reported. degree of possibility that the bacterial loads could escalate to
Journal of Food Quality 5
Table 3: Demographics and food safety awareness of beef retailers.
Demographics and food safety awareness Percentages
Sex Male 60%Female 40%
Below 16 0%
Age 16–35 65%
Above 35 35%
Primary 35%
Educational status Secondary 50%
Tertiary 15%
Months 25%
Duration of being in business Years 75%
Don’t remember 0%
Present 70%
Health license Absent 25%
Don’t know 3%
Refrigerator 87%
Temporary method for storage of beef Freezer 10%
None 3%
1 week 79%
Maximum duration of storage 1 month 20%
More than month 0
Washing of beef before vending Yes 65%No 35%
Water 90%
What type of water is used for washing Water and soap 0%
Antiseptic 0%
Tap water 75%
Water source for meat washing Well water 25%
Rainwater 0%
Yes 97%
Is food safety important Not important 0%
No response 0%
Food safety course 65%
Source of food safety information Media 8%
None 20%
Have you had any training on food safety Yes 78%No 20%
Months ago 5%
If yes, when? Years ago 75%
Don’t remember 20%
unsatisfactory levels if food safety parameters and hygienic Salmonella spp. (42.5%), Pseudomonas spp. (62.5%), and
status are not constantly monitored. Klebsiella spp. (80%). +e occurrence of bacteria in this
+e predominant bacteria isolated in this study were study may have originated from the usage of contaminated
Staphylococcus spp. (34%), Klebsiella spp. (17%), Klebsiella well water used for washing the beef before retailing. In
oxytoca (17%), and Enterobacter spp. (15%). +is is in addition, bacteria may have gained access from the soil, since
contrast to a previous study carried out on street-vended in some abattoir settings postslaughter processing is per-
polyethylene-packaged pawpaw and watermelon in Accra formed on the bare floor [27]. Bacterial isolates of the genus
which reported predominant bacteria isolated were Enter- Klebsiella spp. and Enterobacter spp. are of clinical signifi-
obacter spp. (33%), Citrobacter spp. (20%), and Klebsiella cance and may act as opportunistic pathogens that could
spp. (15.9%) [31]. On the other hand, no Escherichia coli was cause infections of the lower respiratory and urinary tract
isolated in both studies. Similarly, Jahan and Siddique [26] in system [33]. +e occurrence of coagulase-positive Staphy-
Bangladesh reported the isolation of Staphylococcus spp. lococcus aureus may be attributed to insufficient hygiene
(26.7%), Klebsiella spp. (20%), Enterobacter spp. (10%), and practices and cross-contamination by handling meat and
Salmonella spp. (13.3%) in fresh beef. In contrast to this money with the same unwashed hands [34]. Staphylococcus
study findings, however, no Salmonella spp. was isolated. In aureus is known to cause food poisoning, which is often
another study by Chuku et al. [32] in Nigeria, researchers characterized by a sudden start of nausea, vomiting, stomach
reported the isolation of Escherichia coli (83.6%), Staphy- cramps, and diarrhea. Endotoxins that are produced when
lococcus aureus (96.3%), Staphylococcus epidermidis (88.8%), Staphylococcus aureus loads exceed 105 CFU/g are the
6 Journal of Food Quality
primary cause of food poisoning [35, 36]. Globally, Staph- Acknowledgments
ylococcus aureus is one of the common causes of foodborne
disease and staphylococcal intoxication could be attributed +e authors would like to express their gratitude to all the
to improper handling of foods (meat) [37]. A previous study beef retailers who volunteered to take part in this study.
by Essayagh et al. [38] have reported an outbreak of food
poisoning in Morocco at a family dinner, which resulted in 9 References
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