Bacteriological Quality of Beef Offered for Retail Sale in Cote divoire
Seydou O. Coulibaly
This study was designed to monitor the bacteriological quality of beef meat produced and offered for retail sale on the different markets of Abidjan after slaughtering beefs in the main slaughter-house of Abidjan (Côte dIvoire). The bacterial load was assessed on samples collected at a regular 3 h interval from 6: am to 6: pm according to classical methods for the examination of foods. Mean counts (log10 cfu g-1) of total aerobic microorganisms, faecal coliforms, Staphylococcus aureus, Pseudomonas, were 4.93, 1.83, 1.53 and 1.29 at 6: am and at 8.1, 4.73, 2.43 and 2.79 at 6: pm, respectively. The pH ranged from 5.09 to 6.90 and the temperature from 37.29 to 39.59°C. Anaerobic sulphite reducers were detected only at 3: pm and 6: pm with count ranging from 0.76 to 0.83 log10 cfu g-1. Salmonella was detected in 7 to 27% of the samples analyzed. All the counts exceeded the established values in the microbiology criteria for beef meat. Based on the quality criteria established for beef meat, the percentage of samples of a satisfactory quality decreased within the same day to reach 0% in the evening. The percentage of an acceptable quality decreased from 47% at 6: am to 0% at 12:00 noon while that of an unacceptable quality increased from 33 to 100% at 6: pm. All the samples were contaminated at the end the selling time (6: pm). Therefore, the product was unsafe for human consumption. The presence of these organisms is a warning signal for a possible occurrence of food intoxication.
Received: February 24, 2011;
Accepted: May 25, 2011;
Published: June 18, 2011
Developing countries face with high incidences of food poisoning outbreaks,
with obvious economic consequences. While food borne diseases remain an important
public health problem worldwide, one of the most significant food safety hazards
is associated with foods from animals (Kivi et al.,
2007; Maripandi and Al-Salamah, 2010). Meat is considered
as the most important source of proteins consumed by humans. However, meat is
the most perishable of all staple foods since it contains sufficient nutrient
needed to support the growth of microorganisms (Huda et
al., 2010). For highly perishable foodstuffs such as fresh red meat,
the threat of food poisoning is particularly high (Nel et
al., 2004; Yousuf et al., 2008). Thus,
if food is not immediately utilized or preserved after harvesting, it spoils.
Côte d'Ivoire is a wet sub-Saharan African country where bovine cattle
breeding are almost absent. So the country imports livestock up to 80% of its
needs from Mali and Burkina Faso. Although beef meat is popular in Côte
dIvoire, it accounts for 37% of the meat consumed (Anonymous,
2005) because of the increasing price of meat products.
In Côte dIvoire, fresh meats are sold everyday at a retail level
to the public on open markets especially for low-income people who cant
afford a refrigerator for preservation. After slaughtering, beef carcasses are
not stored in chillrooms. So they must be sold within the same day. It is generally
agreed that the internal tissues of healthy slaughtered animals are free of
bacteria at the time of slaughtering. However, when the meat gets to the retail
market, it may contain varying numbers and types of microorganisms (Nollet
and Boylston, 2007). In addition, in Côte dIvoire, food such
as fish or fresh meat is always kept exposed while awaiting buyers, making it
naturally vulnerable to infection with different types of microorganisms. Therefore,
improper handling and improper hygiene may lead to the contamination of fresh
meats and eventually affect the health of the consumers (Koussemon
et al., 2008).
In Côte dIvoire, even though people were used to well cook food
and ate home most of the time, now-a-days, the alimentary trend has changed.
Many people eat out buying ready to eat foods sold by the street sides. It should
be noted that these foods are undercooked most of the time. In the world, one
of the most important food safety hazards is associated with undercooked meat
and poultry (Dyckman and Lansburgh, 2002). Street vending
of foods is a common characteristic of countries with high unemployment rates,
low salaries and poor social security programme. In West Africa, especially
in Côte dIvoire, many popular street-fast-processed and vended foods
such as chicken and beef meat are not always well cooked and are eaten without
further processing or cooking. Therefore, contaminated foods, from fresh red
meat infected with microorganisms, can lead to consumer health problems. Ologhobo
et al. (2010) observed that microbial counts of chicken and beef
suya (street sides roasted meat) were at levels that pose health problems to
consumers. The same authors reported earlier on pathogens like Salmonella,
Staphylococcus and enthero-pathogenic Escherichia coli in beef
There are relatively few surveys and a lack of information on the bacteriological
status of beef carcasses offered for retail sale and the level of hygiene of
the slaughterhouses in Côte dIvoire. Since the beef carcasses are
not preserved after slaughtering but sold within the same day at ambient temperature,
it seems important to investigate some bacteria such as E. coli and S.
aureus which are indicators of excessive human handling (Clarence
et al., 2009). Pseudomonas, a proteolytic contaminating food
bacterium which may be used to predict the level of spoilage of the beef carcasses
while several foodborne outbreaks linked to Salmonella were attributed
to meat and poultry (Dechet et al., 2006; Thomas
et al., 2006). The presence of Salmonella infections such
as typhoid fever continues to be a major public health concern in many countries
such as Côte dIvoire. Therefore, the aim of this study was to assess
the evolution of such bacteria over the time and within the same day of slaughtering.
The bacteria investigated were total aerobic count, anaerobic sulphite reducers,
Staphylococcus aureus, Pseudomonads, faecal coliforms and Salmonella.
MATERIALS AND METHODS
Material and sampling: Beef carcasses were obtained from the main slaughterhouse
in Abidjan, located in the commune of Port-Bouet, Abidjan District, Côte
dIvoire from january to june 2009. Beef carcasses were sampled at the
end of the slaughtering because they were not stored in chillrooms but exposed
at ambient temperature (32±4°C). The samples were collected with
3 butchers chosen randomly in the slaughterhouse. Per sampling day, samples
of about 300 g were aseptically collected in a clean polyethylene bag from the
same portion (the thigh) of the same carcass from each butcher using the excision
method as indicated by Gill and Jones (2000). The thigh
was sampled from all the vendors on Monday mornings at 3 h intervals between
6: am (end of slaughtering) and 6: pm (end of selling). The average time interval
between sampling from one butcher to the next one was ten minutes. A total of
300 samples were collected from 60 beef carcasses. Each sample was placed into
a sterile plastic bag, labelled and stored in an ice box waiting to be shipped
to the laboratory.
Temperature and pH determinations: The temperature and pH of the meat samples were monitored in situ to the abattoir using a portable thermometer. The measures were determined less than 1 h post-mortem and monitored at 3 h intervals for 12 h from 6: am to 6: pm. The temperature and pH were obtained at the time of sampling by inserting a thermometer and a probe electrode into the muscle.
Microbiological assays: Once in the laboratory, no more than 2 h after
sampling, each sample was cut into smaller pieces and ground in a stomacher
into a homogeneous mixture. Twenty five grams of the mixture were suspended
in 225 mL of 0.1% sterile buffer peptone water (Oxoid CM 509) in a plastic bag
and mixed together again for 30 sec at normal speed. The homogenates were used
for all the microbiological analyses. The 1 mL of the homogenate was serially
diluted in an aseptic condition and used for the enumeration of microorganisms.
Total aerobic counts were performed using Plate Count Agar (Oxoid CM 463); faecal
coliforms and Staphylococcus spp counts were carried out on violet Red
bile lactose agar (Oxoid CM 107), incubated at 44°C for 24 h and Baird Parker
Agar (Oxoid CM 275) at 37°C for 24-48 h, respectively. Typical black colonies
with zones around and atypical black colonies were considered as Staphylococci
spp. Staphylococcus aureus was then identified using coagulase test,
DNase test, Gram reaction and catalase activity. For the isolation of anaerobs
that are capable of reducing sulphide, Trypsin Soja Neomycin (TSN, Merck 1.11972)
was inoculated and incubated at 37°C for 24-48 h. We investigated Pseudomonas
spp. on Cetrimide Agar (Biorad, France) at 30°C for 24-48 h. Oxidase (+)
colonies were taken into consideration. Salmonella spp. were isolated
using the classical technique with a pre-enrichment on buffered peptone water
(Oxoid CM 509), enrichment into Rappaport Vassiliadis Broth (Merck 1. 07700),
isolation on Salmonella- Shigella Agar (Merck 1.07667) and identification with
the API 20 E (Biomérieux, France). The presence or absence of Salmonella
was taken into consideration. The mean number of colonies counted for all count
types (except Salmonella) was expressed as log10 colony forming
units per gram (cfu g-1) of sample. All the tests were carried out
in duplicate. The expressions acceptable, marginally acceptable, unacceptable
were used to determine quality of the samples according to the microbiological
criteria for fresh beef meat (Clarence et al., 2009).
Statistical analysis: The data collected underwent an Analysis of Variance (ANOVA) using STATISCA 99. All values were expressed as the mean of three measurements. The data collected were subjected to one way Analysis of Variance (ANOVA). With respect to the bacteriological level, temperature and pH investigation for each to sampling time, mean values were compared for the different sampling times. Duncan test was used in order to determine which means were significantly different from which others (p = 0.05).
Temperatures and pH of samples: The mean temperature and pH values at
various times post mortem are presented in Fig. 1. The temperature
ranges from 37.29 to 39.59°C. The pH values range from 5.09 to 6.90 with
a mean value of 5.7.
||pH and temperatures of beef carcasses at different sampling
times. Bars with same letter are not significantly different
|| Bacterial mean counts of beef carcasses analysed at different
|TAC: Total aerobic count, FC: Faecal coliforms, ASR: Anaerobic
sulphide-reducers, +: Present in less than 10% of samples, ++: Present in
20% of samples, +++: Present in 27% of samples. Means with the same letter
in the same column are not significantly different at 5%
There was no significant difference (p>0.05) between mean temperatures
at 6: am and 9: am and between 12: 00 and 3: pm. However, there was a significant
difference (p<0.05) between mean temperatures at 3: pm and 6: pm. concerning
the pH, no significant differences (p>0.05) was observed from 9: am to 6:
pm. But there was one (p<0.05) between 6: am and 9: am. It should be emphasized
that the lowest pH value was recorded at the highest temperature (39.59°C).
Bacterial loads of samples: The distribution pattern of the bacteria
counts are shown in Table 1. The mean of total aerobic count
on the fresh meat ranged between 4.93-8.1 log10 cfu g-1,
faecal coliforms count between 1.83-4.73 log10 cfu g-1,
S. aureus between 1.53-2.43 log10 cfu g-1 while
Pseudomonads count ranged between 1.29-2.79 log10 cfu g-1.
The bacterial counts increased with time for all the samples analyzed. Mean
counts (log10 cfu g-1) of total aerobic bacteria, faecal
coliforms, S. aureus, Pseudomonas were at 6: am 4.93, 1.83, 1.53,
1.29 and at 6: pm 8.1, 4.73, 2.43, 2.79, respectively. The anaerobic sulphide
reducers were not detected during the first periods of sampling from 6: am to
12:00. Their counts started at 3: pm with values ranging from 0.76 to 0.83 log10
cfu g-1 at the end of the selling time. Significant differences (p<0.05)
were observed between samples for total aerobic counts, faecal coliforms and
S. aureus from 6:am to 6:pm. However, no significant difference (p>0.05)
was observed between samples for Pseudomonas and the anaerobic sulphide
reducers for all the sampling times. Differences in counts up to 2 log units
were found at the same time period when compared to different carcasses. Salmonella
was detected in 7 to 27% of the samples analyzed.
||Percentage of the microbiological quality of the samples at
different sampling times (AQ: Acceptable quality, MAQ: Marginally Acceptable
quality, UQ: Unacceptable quality)
The bacteriological quality of all the beef samples analysed is represented in Fig. 2. The percentage of acceptable quality decreased from 47% at 6: am to 0% at 12:00 while that of the unacceptable quality increased from 33 to 100% at 6: pm. At 9: am, only 3% of the samples were acceptable for human consumption. All the samples were contaminated at the end the selling time (6: pm) and no sample was even marginally acceptable for human consumption.
The different temperature values recorded in this study were in accordance
with those reported by Mackey and Roberts (1993) who
indicated that once the slaughtering is complete, the internal temperature of
the carcasses generally ranges between 30 and 39°C. The temperature of the
muscle tissue in this study falls slowly probably because the beef carcasses
were exposed to ambient temperatures above 30°C and possibly to some radiant
heating. In this study, the lowest pH was recorded at the highest temperature.
This result agreed with that of Bowker et al. (2010)
who stipulated that a rapid decrease of pH values at higher temperature may
burst the lysosomal membrane in which some cathepsins could hydrolyze specific
myofibrillar proteins. Also, the combination of low pH and high temperature
could provoke an earlier release of Ca2+ from the sarcoplasmic reticulum,
thus activating calcium-dependent protease-I which retains 28% of its maximum
activity at post-mortem conditions of pH 5.5 to 5.8. The mean pH value of 5.7
found in this work falls in these pH conditions. The lowest pH value at the
highest temperature suggested an increasing production of lactic acid via anaerobic
glycolysis during marketing at elevated temperature. Huff-Lonergan
and Lonergan (2005) reported that high postmortem temperatures enhanced
the degradation of muscle proteins. The highest mean pH values obtained at 6:
am in this work probably indicate differences in pH of the groups of muscles
in the portions cut from carcasses at different times. Ndou
et al. (2011) reported that physical activity of the animals for
hours before slaughter, reduces glycogen concentration and plasma glucose levels
below critical values and eventually leading to increased meat pH above critical
range of 5.5 to 6.0. This argument could explain the pH values in this work
which range from 5.09 to 6.90.
The mean temperatures of beef carcasses obtained over the time suggest that
the meat was exposed to bacteria proliferation. The high level of microbial
flora on the meat from this study could be generally attributed to the filthy
environment, poor personal hygiene of the butchers and retailers. There could
be possible cross contamination between adjacent raw meat through unclean hands
of the handlers and/or flies. The increasing numbers of bacteria recovered from
samples over time could be due to growth and/or increasing numbers of bacteria
being deposited on the carcass along with dust. Also, the hands and knives,
gloves, aprons, cutting table surfaces used could be implicated as media for
cross contamination of the meat and spread spoiling organisms such as Pseudomonas
and pathogens present on carcasses onto freshly exposed tissues and meat from
other carcasses. Likewise, careless sneezing and coughing among butchers can
lead to a contamination of the products. In addition, handling the carcasses
and the money with the same unwashed hands could also be a good source of contamination.
This unhygienic handling of the meats can affect the ultimate quality of the
fresh product (Biswas et al., 2011; Selvan
et al., 2007; Cohen et al., 2006) and
indicates that the lack of hygiene could be the major source of meat contamination
at the main slaughter-house of Abidjan, Côte dIvoire. Salihu
et al. (2010) indicated that the hygienic conditions are poor when
foods are produced in non-industrial establishments, mainly because of the lack
of required equipment for adequate processing.
The high load of bacteria on the samples analyzed could also be due to the
long period of time the carcasses are displayed at the retail market and sold
at high ambient temperature (32±4°C) on stalls without a chilling
step. Contamination is uneven probably because of accidental contact with contaminated
materials. The present findings were in accordance with the results of previous
studies of Ukut et al. (2010). Rao
et al. (2009) reported that most meats have a high water content
corresponding to the water activity of approximately 0.99 which is suitable
for a microbial growth.
Salmonella was isolated in 27% of the meat samples examined at the end
of the marketing period, making these samples unfit for human consumption. Present
finding agreed with those of Nisbet and Ziprin (2001)
who indicated that the conditions of slaughter houses tend to allow the spread
of Salmonella among carcasses with ranges upward from 21%. Jackson
and Mcgowan (2001) stated that meat is considered spoiled when it is unfit
for human consumption. At the end of the selling time (6: pm), 100% of beef
carcasses sampled were of unacceptable quality as a result of faecal coliforms,
Staphylococcus aureus or Salmonella, suggesting that it is better
to buy the beef meat earlier in the morning. Results in this work were in accordance
with those of Gormley et al. (2010) indicating
that contamination with bacterial pathogens occurred earlier in the production
chain. All the counts exceeded the established values in the microbiology criteria
for beef meat. Storing the meat for sale in refrigerators (4-6°C) could
preserve it and help avoid the drying of carcass surfaces and high microbial
proliferation. Methods and developing technologies (superchilling, natural biopreservatives
etc.,) for preserving fresh meat, proposed and investigated by Zhou
et al. (2010) could also be applied to fresh meat products for high
quality, safety, fresh appearance and an extended shelf life.
The results of this study showed the poor bacteriological quality of retail beef carcasses offered for sale in Côte dIvoire and indicated that the meats sold to the public are grossly contaminated with pathogenic bacteria (Salmonella, S. aureus, anaerobic sulphite reducersY) and viable source of various diseases. Some of these diseases could spread and reach epidemic level which could lead to serious public health problems. It seems therefore necessary to make the following recommendations from the findings of this study: 1) Meat handlers and sellers should be educated on the adverse effects of the lack of proper personal and environmental hygiene and sanitation; 2) Good manufacturing practices should be strictly adhered to by butchers and those selling the meat. the equipment must be washed properly before use; 3) Fresh meats should be well cooked before consumption.
Breeding cattle, sheep and goats. Cote d'Ivoire, Economic Mission in Abidjan.
Bowker, B.C., J.S., Eastridge, E.W. Paroczay, J.A. Callahan and M.B. Solomon, 2010.
Aging/tenderization Mechanisms. In: Handbook of Meat Processing, Toldra, F. (Ed.)., Willey-Blackwell, Iowa, USA., pp: 87-104
Clarence, S.Y., C.N. Obinna and N.C. Shalom, 2009.
Assessment of bacteriological quality of ready to eat food (Meat pie) in Benin City metropolis, Nigeria. Afr. J. Microbiol. Res., 3: 390-395.Direct Link |
Cohen, N., H. Ennaji, M. Hassar and H. Karib, 2006.
The bacterial quality of red meat and offal in Casablanca (Morocco). Mol. Nutr. Food Res., 50: 557-562.PubMed |
Dechet, A.M., E. Scallan, K. Gensheimer, R. Hoekstra and J. Gunderman-King et al
Outbreak of multidrug-resistant Salmonella enterica
serotype Typhimurium definitive type 104 infection linked to commercial ground beef, Northeastern United States, 2003-2004. Clin. Infect. Dis., 42: 747-752.CrossRef | PubMed | Direct Link |
Dyckman, L.J. and J.E. Lansburgh, 2002.
Meat and Poultry: Better USDA Oversight and Enforcement of Safety Rules Needed to Reduce Risk of Food-Borne Illness. In: Food Safety is Anyone Watching, Smyth, V.L. (Ed.). Nova Science Publishers Inc., New York, USA., pp: 101-135
Gill, C.O. and T. Jones, 2000.
Microbiological sampling of carcasses by excision or swabbing. J. Food Prot., 63: 167-173.Direct Link |
Gormley, F.J., C.L. Little, K.A. Grant, E. De Pinna and J. McLauchlin, 2010.
The microbiological safety of ready-to-eat specialty meats from markets and specialty food shops: A UK wide study with a focus on Salmonella
and Listeria monocytogenes
. Food Microbiol., 27: 243-249.CrossRef |
Huda, N., Y.H. Shen, Y.L. Huey, R. Ahmad and A. Mardiah, 2010.
Evaluation of physico-chemical properties of Malaysian commercial beef meatballs. Am. J. Food Technol., 5: 13-21.CrossRef | Direct Link |
Huff-Lonergan, E. and S.M. Lonergan, 2005.
Mechanisms of water-holding capacity of meat: The role of postmortem biochemical and structural changes. Meat Sci., 71: 194-204.CrossRef | Direct Link |
Jackson, D. and C.H. Mcgowan, 2001.
Diet management effects on carcass attributes and meat quality of young goats. Small Ruminant Res., 28: 93-98.
Kivi, M., A. Hofhuis, D.W. Notermans, W.J. Wannet and M.E. Heck et al
A beef-associated outbreak of Salmonella
Typhimurium DT104 in the Netherlands with implications for national and international policy. Epidemiol. Infect., 135: 890-899.CrossRef | PubMed | Direct Link |
Koussemon, M., R. Koffi-Nevry, K. Tano, M. Traore and A. Kamenan, 2008.
Assessing the microbiological quality and conditions of sales of Cyprinus carpio
sp. and Cybium tritor
: Three fish species mostly consumed in Cote D'Ivoire. J. Fish. Int., 3: 1-6.Direct Link |
Mackey, B.M. and T.A. Roberts, 1993.
Improving slaughtering hygiene using HACCP and monitoring. Fleischwirtsch Int., 2: 40-45.
Maripandi, A. and A.A. Al-Salamah, 2010.
Multiple-antibiotic resistance and plasmid profiles of Salmonella enteritidis
isolated from retail chicken meats. Am. J. Food Technol., 5: 260-268.CrossRef | Direct Link |
Ndou, S.P., V. Muchenje and M. Chimonyo, 2011.
Animal welfare in multipurpose cattle production systems and its implications on beef quality. Afr. J. Biotechnol., 10: 1049-1064.Direct Link |
Nollet, L.M.L. and T. Boylston, 2007.
Beef Quality and Tainting. In: Handbook of Meat, Poultry and Seafood Quality, Wiley-Blackwell (Ed.). Technology and Engineering, Amazon, France, pp: 719
Nel, S., J.F.R. Lues, E.M. Buys and P. Venter, 2004.
Bacterial populations associated with meat from the deboning room of a high throughput red meat abattoir. Meat Sci., 66: 667-674.CrossRef | Direct Link |
Nisbet, D.A. and R.L. Ziprin, 2001. Salmonellosis
in Animals. In: Food-Borne Disease Handbook, 2nd Edn., Revised and Expanded Vol. 1. Bacterial Pathogens, Hui, Y., M. Pierson and J. Gorham (Eds.). Marcel Dekker, Inc., New York, USA., pp: 265-284
Ologhobo, A.D., A.B. Omojola, S.T. Ofongo, S. Moiforay and M. Jibir, 2010.
Safety of street vended meat products-chicken and beef suya. Afr. J. Biotechnol., 9: 4091-4095.Direct Link |
Rao, V.A., G. Thulasi and S.W. Ruban, 2009.
Meat quality characteristics of non-descript buffalo as affected by age and sex. World Applied Sci. J., 6: 1058-1065.Direct Link |
Salihu, M.D., A.U. Junaidu, A.A. Magaji, R.M. Aliyu and Y. Yakubu, 2010.
Bacteriological quality of traditionally prepared fried ground beef (Dambun nama
) in Sokoto, Nigeria. Adv. J. Food Sci. Technol., 2: 145-147.
Selvan, P., R.N. Babu, S. Sureshkumar and V. Venkataramanujam, 2007.
Microbial quality of retail meat products available in Chennai city. Am. J. Food Technol., 2: 55-59.CrossRef | Direct Link |
Biswas, A.K., N. Kondaiah, A.S.R. Anjaneyulu and P.K. Mandal, 2011.
Causes, concerns, consequences and control of microbial contaminants in meat-A review. Int. J. Meat Sci., 1: 27-35.CrossRef | Direct Link |
Thomas, A., C.H.O. Lallo and N. Badrie, 2006.
Microbiological evaluation of broiler carcasses, wash and rinse water from pluck shops (cottage poultry processors) in the county Nariva/Mayaro, Trinidad, Trinidad and Tobago, West Indies. Tropicultura, 24: 135-142.Direct Link |
Ukut, I.O.E., I.O. Okonko, I.S. Ikpoh, A.O. Nkang and A.O. Udeze et al
Assessment of bacteriological quality of fresh meats sold in calabar metropolis, Nigeria. Electron. J. Environ. Agric. Food Chem., 9: 89-100.Direct Link |
Yousuf, A.H.M., M.K. Ahmed, S. Yeasmin, N. Ahsan, M.M. Rahman and M.M. Islam, 2008.
Prevalence of microbial load in shrimp, Penaeus monodon
and prawn, Macrobrachium rosenbergii
from Bangladesh. World J. Agric. Sci., 4: 852-855.
Zhou, G.H., X.L. Xu and Y. Liu, 2010.
Preservation technologies for fresh meat-A review. Meat Sci., 86: 119-128.CrossRef | Direct Link |