Odwar et al.

BMC Research Notes 2014, 7:627

http://www.biomedcentral.com/1756-0500/7/627

SHORT REPORT Open Access

A cross-sectional study on the microbiological

quality and safety of raw chicken meats sold in
Nairobi, Kenya
Joyce Arua Odwar1, Gideon Kikuvi1, James Ngumo Kariuki2 and Samuel Kariuki3*

Abstract
Background: Chicken is a rich source of meat protein and is increasingly being consumed in urban areas in Kenya.
However, under poor hygienic environment, raw chicken meat presents an ideal substrate supporting the growth
of pathogenic Escherichia coli and Coliform bacteria indicating the potential presence of other pathogenic bacteria; this
may constitute a major source of food-borne illnesses in humans. This study sought to assess the microbiological
quality and safety of raw chicken meat sold in Nairobi, Kenya by determining the E. coli/coliform contamination levels
as well as the antimicrobial resistance patterns and pathogenicity of E. coli isolated.
Findings: We conducted a Cross-sectional study to collect two hundred raw chicken samples that were randomly
purchased between the periods of August 2011-February 2012. Enumeration of bacteria was done using 3 M Petri film
E. coli/Coliform count plates, isolation and identification of E. coli through standard cultural and biochemical testing,
antimicrobial susceptibilities interpreted according to criteria set by the Clinical and Laboratory Standards Institute
(2012) while Polymerase chain reaction assays were used to determine presence of virulence genes in isolated E. coli.
Data was analyzed using SPSS version 17.0. Contamination rates were 97% and 78% respectively for Coliform bacteria
and E. coli. Seventy six percent of samples fell under the unacceptable microbial count limit (>100 cfu/ml) and
significant differences in the E. coli/coliform counts (p < 0.001) were observed among the chicken retail outlets
with samples from supermarkets having the lowest level of contamination compared to the rest of the retail outlets.
Seventy five percent of the isolates were resistant to at least one of the 12 antibiotics tested with resistance to tetracycline
being the highest at 60.3%. In addition 40.4% E. coli isolates were positive for the ten virulence genes tested.
Conclusion: Raw retail chicken meats in Nairobi are not only highly contaminated, but also with potentially
pathogenic and multi-drug resistant strains of E. coli. It will be important for public health authorities and retail
chicken processing outlets to collaborate in ensuring adherence to set out principles of hygienic processing and
handling of chicken meats in order to reduce potential risks of infection.
Keywords: Raw retail chicken meat, E. coli/coliforms, Microbial counts

Findings cost billions of dollars in medical care and sometimes even

Background result to death [4]. Several epidemiological reports have
Ensuring safe food supply has been one of the major implicated foods from animal origin as major vehicles
challenges and concerns for producers, consumers and associated with illnesses caused by food borne pathogens
public health officials in both developing and developed [5-7]. Coliform bacteria, especially fecal coliforms, are
countries. This is because foods excessively contaminated good microbial indicators of the potential presence of dis-
with pathogenic and spoilage micro-organism are undesir- ease causing bacteria and also show the general sanitary
able and can cause food borne illnesses [1-3]. Such illnesses quality of the food. Food contamination by Escherichia
coli is closely associated with fecal contamination. This is
* Correspondence: [email protected]
3
because E. coli are the most prevalent commensal enteric
Centre for Microbiology Research, Kenya Medical Research Institute, P.O Box
43640–00100, Nairobi, Kenya
bacteria in animals and humans and are also important
Full list of author information is available at the end of the article

© 2014 Odwar et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative
Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and
reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain
Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article,
unless otherwise stated.
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zoonotic agents that can be implicated in animal and In a cross-sectional study, chicken samples were ran-
human infectious diseases [8]. domly purchased from August 2011 to February 2012
Raw or undercooked chicken meat is particularly from different retail outlets spread over 28 locations in
prone to contamination. The microbiological quality of Nairobi. In order to take into account compounding
chicken meat as purchased by consumers depends mostly factors of socio-economic status within Nairobi, the
on; the slaughter process, sanitation during processing retail outlets where samples were purchased were classi-
and packaging, maintenance of adequate cold chain storage fied into supermarkets, shops from high end areas (low
from the processing to the retail level and to the consumer densely populated, up-market residential suburbs), shops
and finally sanitation during handling at the retail end from middle end areas (middle densely populated areas
[9-12]. Chicken meat can also act as a reservoir of drug further classified into high middle and low middle income
resistant bacteria. Antimicrobial resistance among E. coli areas) and shops from low end areas (densely populated
in food animals such as chicken is of increasing concern slums and informal settings). Classification of locations
due to the potential for transfer of these resistant patho- into these groups was done based on a study on residen-
gens to the human population [13-15]. tial segregation in Nairobi [20]. A total of two hundred
In urban areas such as Nairobi, marketing of chicken chicken samples (n = 39, supermarkets; n = 39 high end
products is generally undertaken in retail outlets such as area retail outlets; n = 84, high middle end area retail out-
supermarkets, local butcheries located in different geo- lets; n = 20, low middle end area retail outlets and n = 18,
socio-economic status and even from street vendors in low end area retail outlets) were purchased. Both freshly
some low income settings. Public health research in slaughtered as well as samples that have been in storage in
countries such as the United States of America focus- freezers were included in the study. Packaged chicken
ing on food qualities demonstrated that stores in low samples were transported in cool boxes to the laboratory
socio-economic status populations, because of a higher for bacterial isolation within 1 hour from time of col-
prevalence of food safety violations, were shown to be lection. Samples were processed at the Kenya Medical
consistently exposed to food that is of lower microbial Research Institute, Centre for Microbiology Research
quality. Because of this access pattern, such populations laboratories, Kenyatta hospital compound. Ethical approval
are placed at increased risk of food-borne illnesses [16,17]. to perform this study was obtained from the Ethics Review
In Kenya, there is a paucity of data on coliform contamin- Committee at Kenya Medical Research Institute, Reference
ation and antimicrobial resistant E. coli in raw retail SSC No. 2036.
chicken supplied to retail outlets in the city. Studies re-
lated to antimicrobial resistant E. coli have been done on Bacteriological analysis
isolates from farm animals and chicken carcass samples Enumeration of E. coli and coliform bacteria from the
from slaughter [18] but not from raw retail chicken which chicken samples was performed as described in the
is made available to consumers. Furthermore, no studies Association of Analytical Communities International,
are available on the contamination levels in chicken meat official methods of analysis using 3 M petrifilm E. coli/
available to populations living in different socio-economic Coliform count plates [21] with slight modification.
status yet, these data are essential for performing risk The samples, which included the skin of the chicken
assessment and risk management for food safety. This along with the meat itself, were aseptically removed
study reports on the microbiological quality and safety from the package and 100 gram piece of chicken was
of chicken meat available to populations who purchase weighed and placed in 100 ml sterile distilled water.
from different retail outlets (supermarkets, retail outlets One ml of the rinse water from the sample was placed
in high income areas, retail outlets in middle income onto the center of the bottom film and covered carefully
areas and retail outlets in low income areas) in the city avoiding entrapment of air bubbles and the plates from all
of Nairobi. samples incubated for 24 ± 2 hrs at 35°C. Colony counts
for each petrifilm were done the following day and the mi-
Methods crobial count results converted to the base 10 logarithm
Study area and sampling of the number of colony forming units per ml (cfu/ml)
The study was conducted in Nairobi County. Nairobi is rinse water obtained from the samples. Typical E. coli
the administrative and commercial capital in Kenya and colonies growing on the petrifilm were then selected
home to thousands of businesses including the retail and sub-cultured in MacConkey agar to obtain pure
chicken business.. There is a huge disparity in income colonies. After a series of biochemical tests for confirma-
levels and population densities in Nairobi. The people tive identification [22], positive E. coli isolates were stored
living in the western suburbs are generally the more at −80°C in trypticase soy broth for further antimicrobial
affluent while the lower and middle-income populations susceptibility tests and PCR to determine the presence of
dominate the eastern suburbs [19]. virulence genes.
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Antimicrobial susceptibility testing outlets, ANOVA was used after converting the counts to
Using the Kirby-Bauer disc diffusion method [23], E. coli base 10 logarithms. The chi-square test was used to assess
were tested for their susceptibility to 12 commonly any statistical significant association between anti-
used antimicrobials on disks containing; Ampicillin microbial resistances in the E. coli isolated with regard
(AMP 10 μg), Amoxycillin-clavulanic acid (AMC, 30 μg), to retail outlet classification from where the raw chicken
Tetracycline (TE 30 μg), sulphamethoxazole-trimethoprin was purchased.
(SXT 30 μg), Ciprofloxacin (CIP 5 μg), Ceftriaxone (CRO
30 μg), Ceftazidime (CAZ 30 μg), Kanamycin (K 30 μg), Results
Streptomycin (S 10 μg), Gentamicin (CN 10 μg), Nalidixic Contamination rate and microbial count in raw retail
acid (NA 30 μg) and Chloramphenicol (C 30 μg). The chicken
concentrations of the antimicrobial disks were selected Contamination rate of chicken samples by total coliform
based on the internationally recognized standards and bacteria was found to be 97% while contamination by E.
guidelines on antimicrobial routine testing and reporting coli was 78%. The average E. coli and coliform counts
on enterobacteriaceae provided by the Clinical and La- for all samples in general were observed to be above the
boratory Standard Institute. E. coli strain 25922 was used acceptable range for E. coli counts as set by the Hazard
to control for bacterial growth and potency of antibiotic Analysis and Critical Control Point system (HACCP),
disks. Inoculated agar plates were incubated at 37°C for developed by Food and Agriculture Organization (FAO)
24 h. The susceptibility zones were also measured and and adopted by the Codex Alimentarius Commission
interpreted according to criteria set by the Clinical and (3.911 and 5.0261Log10cfu/ml respectively). According
Laboratory Standards Institute [24]. to this system, the acceptable food safety range is
100 cfu/ml or less (2.000 Log10cfu/ml or less), the mar-
Bacterial DNA extraction and detection of virulence genes ginal or intermediate range is over 100 cfu/ml but not
in E. coli above 1000 cfu/ml (over 2.000 but not above 3.000
DNA from the isolated E. coli as well as from 5 control Log10cfu/ml) and the unacceptable range is above
strains was extracted following the procedures described 1000 cfu/ml (above 3.000 Log10cfu/ml) [27]. Only 80
by Ehrt and Schnappinger [25], with slight modifications. (40%) out of a total 200 retail chicken samples that were
A loop full of overnight bacterial culture was suspended purchased fell under the acceptable range for E. coli
in 1 ml of sterile distilled water and then boiled for counts. 76% of samples fell under the unacceptable
10 minutes at 95°C. The cell mixture was centrifuged for range for total coliforms. As shown in Tables 1 and 2 su-
5 minutes at 14,000 rpm and supernatant was used as permarkets had the highest percentage of samples within
the DNA template for PCR amplification. Ten PCR acceptable food safety ranges while average counts of sam-
primers were used to detect the target genes enumerat- ples from the rest of the retail outlets were within mar-
ing toxins in pathogenic E. coli [26]. A multiplex PCR ginal or unacceptable counts of above 2.000 Log10cfu/ml.
system was optimized by the progressive incorporation There was a statistical significant difference in the E. coli
of primers corresponding to the different genes and sev- count (F (4,175) =16.676; MSE = 106.576; p < 0.001)
eral combinations of melting temperatures, primer con- and coliform counts (F (4,179) =18.37; MSE = 105.097;
centrations and DNA template concentration. PuReTaq p < 0.001) among the outlets with supermarkets having
ready to go PCR beads (GE Health care) were used for the lowest E. coli and coliform count compared to the
PCR. The total reaction volume in each PCR tube was rest. Graphical evidence of the differences of E. coli
25 μl containing 3 μl template DNA, 2 μl primer (0.2 μl and coliform counts observed in the different retail
of each primer) and 20 μ sterile PCR water. PCR was outlet classifications are also shown in Figures 1 and 2.
done under the following conditions; initial denaturation
at 94°C for 5 minutes. This was followed by 35 cycles of Prevalence of antimicrobial resistant E. coli isolated from
denaturation at 94°C for 1 minute, annealing at 56°C for raw retail chicken
30 seconds and extension at 72°C for 1 minute. The final Seventy five percent (117 out 156) of the E. coli isolated
step was amplification at 72°C for 10 minutes. Ampli- exhibited resistance to at least one of the 12 antibiotics
cons were then subjected to agarose gel electrophoresis tested. As seen in Table 3, prevalence of antimicrobial
and viewed under UV light. resistance was highest for tetracycline followed by
sulphamethoxazole-trimethoprin, ampicillin and strepto-
Statistical analysis mycin. Only 24.5% of the isolates were fully sensitive to all
Statistical analysis including means, medians and standard antibiotics while 42.9% were resistant to 3 or more antibi-
deviations, was conducted by means of SPSS version 17.0 otics especially to the above mentioned antimicrobials.
software. To determine differences in microbial counts in There was no significant difference in the prevalence of
chicken samples purchased from among the various retail antimicrobial resistance among the 5 classifications of
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Table 1 Descriptive statistics of microbiological count of raw chicken meats from 5 different classifications of retail
outlets
Total count log10 CFU/ml of carcass rinse
Bacteria Summary statistics Supermarkets H.I.A butcheries H.M.I butcheries L.M.I butcheries L.I.A butcheries
E.coli Average log10 0.9376 2.6510 5.0007 4.8084 4.9882
Median 0.9031 1.7243 6.0000 5.9031 6.0792
SD 0.6794 2.3638 2.8155 2.5910 3.1096
Minimum 0.0000 0.0000 0.0000 1.0410 0.0000
Maximum 2.1460 8.0000 8.0790 8.0000 8.0000
Coliforms Average log10 1.7239 5.0769 6.1855 5.2953 6.0111
Median 1.5315 6.0000 7.5374 6.0000 7.0731
SD 1.3324 2.9304 2.3052 2.5475 2.6770
Minimum 0.6990 0.9030 0.3420 1.1760 0.4770
Maximum 8.0000 8.0790 8.1610 8.0000 8.1760
H.I.A butcheries-High income area butcheries, H.M.I butcheries-High-middle income area butcheries.
L.M.I- Low-middle income area butcheries, L.I.A- Low income area butcheries.

retail outlets (χ2n-1 = 4.178; d.f = 4; p = 0.382). However, and 90% in two states in Australia [31-34]. Similarly,
samples from supermarkets had the highest prevalence studies in Hanoi, Vietnam, Morocco and some states in
(84.6%) while samples from outlets in low income areas America have shown that the percentage of retail chicken
had the lowest prevalence of antimicrobial resistance samples which fall under the unacceptable food safety
(62.5%). range were also high and that perishable produce items,
including poultry, available in markets in low-socio eco-
Prevalence of E. coli isolates harboring virulence markers nomic status census tracts had higher microbial indicator
Of the E. coli isolated from raw retail chicken meat, counts compared to markets in high-socio economic
40.4% carried at least one of 10 virulence genes tested status due to a higher prevalence of food safety violations
and specific for 5 known diarrheagenic E. coli. Of the E. [30,35-37,16,17]. The results observed in this study might
coli positive for virulence genes in this study, ETEC was be due to factors common in Nairobi such as home
the most common pathogenic E. coli (61%) while the slaughter of chicken by small scale poultry producers
least common was EAggEC (5%) (Table 4). instead of slaughter at private or municipal government
approved chicken slaughter houses thus increasing the
Conclusion potential risks for contamination due to bio-security flaws
The E. coli contamination rate observed in this study [13]. All samples from supermarkets and a majority of
was almost similar to that observed in studies conducted samples from high income butcheries were products of
in other developing countries. For instance, contamin- government approved private chicken slaughter houses.
ation rates of 98% were observed in the north east part Majority of carcasses in Nairobi tend to be lumped
of India, 100% in Cameroon and 100% in Vietnam together in one large container or sack as they are being
[28-30]. Similar high recovery rates have been observed transported in ambient temperature thus exposing them
in studies from developed countries with contamination to the open air as well as allowing transfer of contaminants
rates as high as 100% in Japan, 89% Minnesota, U.S.A, from one carcass to another and subsequent microbial

Table 2 Assessment of Microbial count results of raw chicken meat from the different retail markets
Assessment of microbial counts Log10cfu/ml
% acceptable samples % marginal samples % unacceptable samples
Retail outlet E.coli Coliforms E.coli Coliforms E.coli Coliforms
Supermarket 97% 84% 3% 13% 0% 3%
H.I.A butcheries 69% 26% 10% 15% 21% 59%
H.M.I butcheries 29% 7% 12% 14% 60% 79%
L.M.I butcheries 25% 10% 10% 20% 65% 70%
L.I.A butcheries 16% 33% 6% 6% 78% 61%
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Table 3 Antimicrobial resistance profiles among E. coli

isolated in retail chicken meat (n = 156)
Antibiotic Frequency of resistant isolates %
AMC 4 2.6
SXT 77 49.4
TE 94 60.3
AMP 53 34
CIP 7 4.5
CAZ 0 0
K 8 5.1
S 47 30.1
CRO 18 11.5
Figure 1 Distribution of E. coli count among the 5 retail outlet
classifications. Counts were evenly distributed., the size of the CN 1 0.6
boxes for high- middle income, low-middle income and low income NA 23 14.7
areas indicate that the middle 50% E. coli counts are spread out for
C 21 13.5
these groups while for high class butcheries and supermarkets the
box sizes indicate that the middle 50% of the counts are
clumped together.
study in Accra, Ghana found that even though hygienic
conditions in supermarkets were generally better than
multiplication. Studies in Iran and Switzerland showed that those in local markets and farms, there was no significant
there were significant differences in contamination rates difference between the microbial counts for these retail
between individually packed and unpacked chicken meat outlets and they all had low microbial counts [43]. The au-
samples [38,39]. Use of freezers and cooling temperatures thors attributed this observation to the deliberate efforts
for storage and display in some outlets from high middle by the food sector in improving the hygienic procedures
income and low income areas could have resulted to few in the processing of poultry over the years.
samples falling under the acceptable food safety range in Similar prevalence of antibiotic resistance in E. coli
these outlets as seen from the outliers in Figure 1 [40,41]. isolated from retail chicken have been observed in other
In most retail outlets, the degree of physical contact studies ranging from 40.6% in Japan, 52% in Iceland,
between different kinds of meat on display such as beef, 84.6% in Minneapolis, U.S.A, 83.8% in Vietnam and even
fish and mutton may have led to cross contamination of 100% isolates in Senegal being resistant to one or more
different meats. Also, use of bare hands in handling meat, antibiotics [31,44-47]. The high prevalence of resistance
utensils and money at the same time as observed may in poultry meat isolates is alarming given the evidence of
have increased chances of microbial contamination [42]. possible transmission of antibiotic resistant food borne
In contrast to the findings in this study, a similar recent bacteria to consumers and food handlers [48]. Similar
multi-drug resistance phenotypes of E. coli isolated from
retail chicken have been reported in studies conducted
in Japan, Vietnam, Saudi Arabia and Slovakia [30,31,49,50].
The common resistance phenotypes observed are of
great clinical significance since these antimicrobials
are considered to be among the frontline therapeutic
drugs for treatment of most bacterial infections in

Table 4 Classification of pathogenic E. coli identified from

retail chicken meat
Classification of pathogenic E. coli Frequency of isolates %
EPEC 13 20.6
ETEC 38 60.3
Figure 2 Distribution of Coliform count among the 5 retail EIEC 4 6.3
outlet classifications. Apart from supermarkets, the other 4 retail
outlet classifications have bulk of the count concentrated on the EaggEC 3 4.8
high end of the scale. STEC 5 7.9
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humans in Kenya. Past studies assessing antimicrobial known animal reservoirs for these pathogens hence any
consumption in food producing animals in Kenya showed primary source of contamination appears to be infected
that tetracyclines, sulphonamides and trimethoprins, humans [63,67]. Another reason for this observation in
nitrofurans, aminoglycosides, beta lactams and the this study is that ETEC had several virulent gene markers
quinolones were the most commonly used drugs in compared to the rest and thus could be easily detected
food producing animals with tetracyclines and sulpho- more than the others. These results are important as they
namides/trimethoprin topping the list in popularity indicate that apart from being highly contaminated with
and accounting for nearly 78% of the use [51]. A corre- coliforms which could lead to quick spoilage, raw retail
sponding study in Tanzania showed similar results sup- chicken in Nairobi, Kenya is a potential source of food
porting these findings [52]. Such use has been shown borne illnesses as it carries pathogenic E. coli. This has
to result in the development of resistant bacteria which important implications and present unique challenges for
can then reach heavily exposed individuals such as interventions for microbial contamination of retail chicken
slaughter house workers, food handlers and farmers meats in urban settings.
who feed the animals with the antimicrobials [53].
Competing interests
These resistant bacteria can then easily contaminate The authors declare that they have no competing interest.
the carcasses of food animals along the production line
to the retail outlets. In countries such as Uganda and Authors’ contributions
Iceland, studies have shown that broiler chicken pro- JA was the main author, who participated in conception of the study and
study design, literature search, acquisition of data, statistical analysis and
duction has been associated with a high prevalence of drafting of the manuscript. SK was involved in supervising, designing and
antimicrobial resistance in isolates from these chickens coordinating the study, interpreting the data and critical revision and
due to consumption of antimicrobials [54,55]. In this drafting of the manuscript. GK participated in supervision, study design and
development of the manuscript. JNK greatly contributed in statistical analysis
study, all samples from supermarkets, which had more and data interpretation. All authors read and approved the final manuscript.
resistant isolates, came from improved breeds of
chicken/broilers while 80% of samples from low in- Acknowledgments
The authors would like to acknowledge personnel of KEMRI, Centre of
come areas were from local/indigenous chicken breeds. Microbiology Research, Enterics laboratory for their technical assistance and
A common practice for broiler chicken producers in co-operation and the Director, KEMRI for permission to publish. This work
urban areas in Kenya is to add antibiotics into the was funded by a joint WHO/FAO pilot projects grant.
commercial feeds or drinking water for chicken thus Author details
exposing them more to undue antimicrobial consump- 1
Institute of Tropical Medicine and Infectious Diseases, Jomo Kenyatta
tion [56]. This practice may modify the intestinal flora University of Agriculture and Technology, P.O Box 62000–00200, Nairobi,
Kenya. 2Centre for Public Health Research, Kenya Medical Research Institute,
and create a selective pressure in favor of resistant P.O Box 20752–00202, Nairobi, Kenya. 3Centre for Microbiology Research,
bacteria [57]. On the other hand, indigenous chicken Kenya Medical Research Institute, P.O Box 43640–00100, Nairobi, Kenya.
production in most African countries including Kenya
Received: 1 February 2014 Accepted: 6 September 2014
is traditionally based on free range breeding systems Published: 10 September 2014
allowing birds to grow without any external influence.
They are estimated to reach a mature, marketable age References
by 8 months [42,58]. 1. Lindqvist R, Anderson Y, De Jong B, Norberg P: A summary of reported
food borne disease incidents in Sweden, 1992 to 1997. J Food Protect
Studies done in Burkina Faso, Korea and Lebanon also 2000, 63:1315–1320.
showed presence of E. coli contaminants harboring viru- 2. Su HP, Chu SI, Tsai JL, Lee CL, Pan TM: Bacterial food borne illness
lence genes in fresh poultry meat (with prevalence of outbreaks in Northern Taiwan, 1995 to 2001. J Infect Chem 2005,
11:146–151.
43%, 14% and 14% respectively) and that that ETEC, 3. Lynch M, Painter J, Woodruff R, Braden C: Surveillance of food borne
EPEC and STEC were the most common diarrheagenic disease outbreaks in United States, 1998 to 2002. Morbidity Mortality Wkly
E. coli detected [59-61]. This could be because ETEC, Rep Surveil Summaries/CDC 2006, 55:1–34.
4. Fratamico PM, Bhunia AK, Smith JL: Food borne pathogens. In Microbiology
EPEC and STEC are much frequently implicated in and Molecular biology. Wymondham, Norfolk: Caster academic press;
various food and water borne diseases and they are 2005:273.
known contaminants of meat and meat products [62,63]. 5. Pertersen KE, James WO: Agents, vehicles and causal inference in
bacterial food borne disease outbreaks, 1986 to 1995. J Am Vet Med
Studies, for instance in Canada, Spain and Minnesota Assoc 1998, 212:1874–1881.
U.S.A, have also shown that live chicken and other 6. Todd A: Epidemiology of food borne diseases. World Health Stat 1997,
food animals are known reservoirs of these pathogenic 50:1–2.
7. Tauxe RV: Emerging food borne diseases: an evolving public health
E. coli and therefore contamination could actually be challenge. Emerg Infect Dis 1997, 3:425–434.
from the animal during evisceration or even from 8. Costa D, Poeta P, Saenz Y, Coelho AC, Matos M, Vinue´ L: Prevalence of
water used during their processing [64-66]. On the antimicrobial resistance and resistance genes in faecal Escherichia coli
isolates recovered from healthy pets. Vet Microbiol 2008, 127:97–105.
other hand EIEC and EaggEC are not implicated much 9. Belluck P: Federal inspectors seek source of Escherichia coli
in food and water borne illnesses and there are no contamination. In New York Times. 1997:1.
Odwar et al. BMC Research Notes 2014, 7:627 Page 7 of 8
http://www.biomedcentral.com/1756-0500/7/627

10. Borche E, Arinder P: Bacteriological safety issues in beef and ready to eat 34. Pointon A, Sexton M, Dowsett P, Saputra T, Kiermeier A, Lorimer M: A
meat products as well as control measures. Meat Sci 2002, 62(3):381–390. baseline survey of the microbiological quality of chicken portions
11. Andrea W: Mobile slaughter houses will help small farmers. In News and carcasses at retail in two Australian States, 2005 to 2006. J Food
observer. 2010:3. Protect 2008, 71(6):1123–1134.
12. Selvan PR, Narendra B, Sureshkumar S, Venkatamanujam V: Microbial 35. Amara A, Ziani Z, Bouzoubaa K: Antibiotic resistance of Escherichia coli
quality of retail meat products available in Chennai city. Am J Food strains isolated in Morocco from chickens with coccilobacillosis. Vet
Technol 2007, 2(1):55–59. Microbiol 1995, 43:325–330.
13. O’Brien TF: Emergence, spread, and environmental effect of antimicrobial 36. Koro ME, Anandan S, Quinlan JJ: Microbial quality of food available to
resistance: how use of an antimicrobial anywhere can increase resistance populations of differing socio economic status. Am J Prev Med: Elsevier Inc
to any antimicrobial anywhere else. J Clin Infect Dis 2002, 34(3):78–84. 2010, 20(10):30.
14. Angulo FJ, Nargund VN, Chiller TC: Evidence of an association between 37. Chaiba A, Rhazifilali F, Chahlaoui A, Soulaymani Bencheikh R, Zerhouni M:
use of anti-microbial agents in food animals and anti-microbial resistance Microbiological quality of poultry meat on the Meknes market
among bacteria isolated from humans and the human health (Morocco). Inter J Foodsaf 2010, 9:67–71.
consequences of such resistance. J Vet Med 2004, 51:374–379. 38. Vaskas TA, Dahesht EA, Seifi S, Rahmani M, Motaghifar A, Safanavaee R:
15. Molbak K: Spread of resistant bacteria and resistance genes from animals Study and comparison of the bacterial contamination outbreak of
to humans – the public health consequences. J Vet Med 2004, chicken meat consumed in some cities of Mazandaran province, Iran. Afr
51:364–369. J Microbiol Res 2012, 6(33):6286–6290.
16. Algert SJ, Agrawal A, Lewis DS: Disparities in access to fresh produce in 39. Regula G, Ursula L, Roger S, Danuser J: Risk factors for antibiotic resistance
low income neighborhoods in Los Angeles. Am J Prev Med 2006, in campylobacter species isolated from raw retail poultry in Switzerland.
30:365–370. BioMed Central: Publ Health 2003, 3:39.
17. Moore LV, Diez-Roux AV: Associations of neighborhood characteristics 40. Jakabi M, Gelli DS, Ristiri CA, De Paula AMR, Sakuma H, Lopez GIS: Presence
with the location and type of food store. Am J Publ Health 2006, of Salmonella species and Escherichia coli O157:H7 in raw meat in Sao
96:325–331. Paolo city, Brazil and evaluation of low temperature (refrigeration and
18. Kikuvi GM, Ole-Mapenay IM, Mitema ES, Ombui JN: Antimicrobial freezing) in resistance of these bacteria. In Determination of human
resistance in Escherichia coli isolates from faeces and carcass samples of pathogen profiles in food by quality assured microbial assays. Paper presented
slaughter cattle, swine and chickens in Kenya. Israel J Vet Med 2006, at the proceedings of a final research coordination meeting held in Mexico
61(3–4):82–88. city, Mexico. Edited by Loaharanu P, Rubio T. 2002:35–42.
19. Afullo A, Odhiambo F: The primary solid waste storage gaps experienced 41. Popkin BM: Technology, transport, globalization and the nutrition
by Nairobi households. Ethiop J Environ Manag 2009, 2:3. transition food poultry. J Food Poult 2006, 10:1016.
20. K’Akumu OA, Olima WHA: The dynamics and implications of residential 42. Nyaga P: Good bio-security practices in small scale commercial and
segregation in Nairobi. Habitat Int J 2007, 31:87–99. scavenging production systems in Kenya. http://www.fao.org/docrep/013/
21. AOAC: Official methods 966.24 for enumeration of Escherichia coli and al838e/al838e00.pdf.
Coliform bacteria in raw meats. 2006. http://www.3M.com/microbiology. 43. Adu-Gyamfi A, Torgby-Tetteh W, Appiah V: Microbiological quality of
22. MacFaddin JF: Biochemical Tests for Identification of Medical Bacteria. chicken sold in Accra and determination of D10-value of E. coli. J Food
Philadelphia: Lippincott Williams and Wilkins; 2000. 3:363–36. Nutri Sci 2012, 3:693–698.
23. Bauer AW, Kirby WMM, Sherris JC, Turk M: Antibiotic susceptibility testing 44. Thorsteinsdottir TR, Haraldsson G, Fridriksdottir V, Kristinsson KG, Gunnarsson
by a standardized single disk method. Am J Clin Path 1966, 45:493–496. E: Prevalence and genetic relatedness of antimicrobial resistant
24. Clinical and Laboratory Standards Institute, CLSI: Performance Standards Escherichia coli isolated from food animals, food and humans in Iceland.
for Antimicrobial Susceptibility Testing. Twenty-second Informational Zooneses Publ Health 2010, 57:189–196.
Supplement. M100-S22. Clinical and Laboratory Standards Institute. 45. Van TTH, George M, Istivan T, Tran L, Cole PJ: Antibiotic resistance in
Wayne, PA: CLSI; 2012. Document M100-S22. food-borne bacteria contaminants in Vietnam. App Environ Microbiol 2007,
25. Ehrt S, Schnappinger D: Isolation of plasmids from E. coli by alkaline lysis: 73(12):7906–7911.
Methods in molecular biology. Springer Protocols 2003, 235:75–78. 46. Johnson JR, Kuskowski MA, Smith K, O’Bryan TT, Tatini S: Antimicrobial
26. Fujioka M, Kasai K, Miura T, Sato T, Otomo Y: Rapid diagnostic method for resistant and extra intestinal pathogenic Escherichia coli in retail foods.
the detection of diarrheagenic Escherichia coli by multiplex PCR. Jpn J J Infect Dis 2005, 191:1040–1049.
Infect Dis 2009, 62:476–480. 47. Fofana A, Bada AR, Seydi M, Akakpo AJ: Antibiotic resistance of Escherichia Coli
27. Food Safety and Inspection Service: Guidelines for Escherichia coli testing strains isolated from raw meat in Senegal. Dakar Med 2006, 51(3):145–150.
for process control verification in poultry slaughter establishment: 48. Bester LA, Essack SY: Antibiotic resistance via the food chain: Fact or
HACCP guidelines and policies. 1996. http://www.fsis.usda.gov/wps/portal/ fiction? S Afri J Sci 2010, 106(9/10):1–5.
fsis/topics/regulatorycompliance/compliance-guides-index#Ecoli. 49. Al-Ghamdi SA, El-Morsy F, Al-Mustafa ZH, Al-Ramadhan M, Hanif M: Antibiotic
28. Saikia P, Joshi SR: Retail market poultry meats of North-East India: a resistance of Escherichia coli isolated from poultry workers, patients and
microbiological survey for pathogenic contaminants. Res J Microbiol 2010, chicken in the eastern province of Saudi Arabia. J Trop Med Intern Health
5(1):36–43. 1999, 4(4):278–283.
29. Nzouankeu A, Ngandjia A, Ejenguele G, Njine T, Wouafo MH: Multiple 50. Ruzauskas M, Šiugždinienė R, Šeputienė V, Sužiedėlienė V, Virgailis M,
contaminations of chickens with Campylobacter, Escherichia coli and Daugelavičius S: The situation of antimicrobial resistance of enteric
Salmonella in Yaoundé, Cameroon. J Infect Dev Ctries 2010, 4(9):583–586. bacteria isolated from animal origin to quinolones and fluoroquinolones.
30. Thangh Huong CT, Hai Duong NT, Thu Hien NT: Contamination of some Veterinarijairzootechnika 2010, 50:73–80.
bacteria isolated from chicken meat in retail markets in Hanoi and 51. Mitema ES, Kikuvi GM, Wegener HC, Stohr K: An assessment of
examination of the antibiotic resistance ability of Salmonella and E. coli antimicrobial consumption in food producing animals in Kenya. J Vet
strains isolated. J Sci Dev 2009, 7(2):181–186. Pharm 2001, 24(6):385–390.
31. Ashraf MA, Hirofumi S, Tadashi S: Isolation and molecular characterization 52. Nonga HE, Mariki M, Karmurbo ED, Mdegela RH: Assessment of
of multidrug resistant strains of Escherichia coli and Salmonella from antimicrobial usage and antimicrobial residues in broiler chickens in
retail chicken meat in Japan. J Food Sci 2009, 74:7. Morogoro municipality, Tanzania. Pakistan J Nutr 2009, 8(3):203–207.
32. Johnson JR, Murray AC, Gajewski A, Sullivan M, Snippes P, Kuswoski MA, 53. Hammerum AM, Heuer OE: Human health hazards from antimicrobial
Smith KE: Isolation and molecular characterization of Nalidixic acid resistant Escherichia coli of animal origin. J Clinic Infect Dis 2009, 48:916–921.
resistant extra intestinal pathogen Escherichia coli from retail chicken 54. Majalija S, Oweka F, Wito GS, Lubowa M, Vudriko P, Nakamaya FM: Antibiotic
products. Antimicrob Agents Chemother 2003, 7:2161–2168. susceptibility profiles of faecal Escherichia coli isolates from dip-litter broiler
33. Zhao S, Blickenstaff K, Bodeis-Jones S, Gaines SA, Tong E, McDermott PF: chickens in Northern and Central Uganda. J Vet Res 2010, 3(4):75–80.
Comparison of the prevalence and antimicrobial resistances of Escherichia 55. Thorsteinsdottir TR, Haraldsson G, Fridriksdottir V, Kristinsson KG, Gunnarsson
coli isolates from different retail meats in the United States, 2002 to E: Broiler chickens as source of human Fluoroquinolone resistant
2008. J Food Microbiol 2012, 78:23. Escherichia coli, Iceland. J Emerg Infect Dis 2010, 16(1):133–135.
Odwar et al. BMC Research Notes 2014, 7:627 Page 8 of 8
http://www.biomedcentral.com/1756-0500/7/627

56. Kariuki S, Onsare R, Mwituria J, Ngetich R, Nafula C, Karimi K, Karimi P,

Njeruh F, Irungu P, Mitema E: Improving food safety in meat value chains
in Kenya. General interest paper: FAO/WHO project report. Food Protect
Trend 2013, 5:172–179.
57. Diarra MS, Silversides FG, Diarrassouba F, Pritchard J, Masson L, Brousseau R:
Impact of feed supplementation with antimicrobial agents on growth
performance of broiler chickens, Clostridium pefringens and Enterococcus
counts and antibiotic resistance phenotypes and distribution of
antimicrobial resistance determinants in Escherichia coli isolates. App
Environ Microbiol 2007, 73(20):6566–6576.
58. Upton M: The role of livestock in economic development and poverty
reduction. http://www.fao.org/ag/againfo/programmes/en/pplpi/docarc/
wp10.pdf.
59. Kagambega A, Martikainen O, Lienemann T, Siitonen A, Traore AS, Barro N,
Haukka K: Diarrheagenic Escherichia coli detected by 16-plex PCR in raw
meat and beef intestines sold at local markets in Ouagadougou, Burkina
Faso. Intern J Food Microbiol 2012, 153(1–2):154–158.
60. Lee GY, Jang HI, Hwang ZG, Rhee MS: Prevalence and classification of
pathogenic Escherichia coli isolated from fresh beef, poultry and pork in
Korea. Internat J Food Microbiol 2009, 134(3):196–200.
61. El-Rami FE, Rahal EA, Sleiman FT, Abdolnoor AM: Identification of virulence
genes among antibacterial resistant Escherichia coli isolated from
poultry. Adv Stud Biol 2012, 4(8):385–396.
62. CDC: Escherichia coli: General information. http://www.cdc.gov/ecoli/general/.
63. Feng P, Stephen DW Jinneman K: Diarrheagenic Escherichia coli:
Bacteriological analytical manual. http://www.fda.gov/food/
foodscienceresearch/laboratorymethods/ucm070080.htm.
64. Bergeron CR, Prussing C, Boerlin P, Daignault D, Dutil L, Reid-Smith R:
Chicken as reservoir for extra-intestinal pathogenic Escherichia coli in
humans, Canada. J Emerg Infect Dis 2012, 18:3.
65. Cortés P, Blanc V, Mora A, Dahbi G, Blanco JE, Blanco M: Isolation and
characterization of potentially pathogenic antimicrobial-resistant
Escherichia coli strains from chicken and pig farms in Spain. Appl Environ
Microbiol 2010, 76:2799–2805.
66. Johnson JR, Sannes MR, Croy C, Johnston B, Clabots C, Kuskowski MA:
Antimicrobial drug–resistant Escherichia coli from humans and poultry
products, Minnesota and Wisconsin, 2002–2004. Emerg Infect Dis 2007,
13:838–846.
67. Smith H, Willshaw G, Cheasty T: E. coli as a cause of out breaks of
diarrhoeal disease in the U.K. Microbiol Today 2004, 31:117–118.

doi:10.1186/1756-0500-7-627
Cite this article as: Odwar et al.: A cross-sectional study on the
microbiological quality and safety of raw chicken meats sold in Nairobi,
Kenya. BMC Research Notes 2014 7:627.

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