AMERICAN JOURNAL OF FOOD AND NUTRITION

Print: ISSN 2157-0167, Online: ISSN 2157-1317, doi:10.5251/ajfn.2013.3.3.167.175

© 2013, ScienceHuβ, http://www.scihub.org/AJFN

Occurrence of Escherichia coli and Salmonella spp. in street-vended

foods and general hygienic and trading practices in Nakawa Division,
Uganda
D. Mugampoza., 1, 2, G.W.B. Byarugaba2., A. Nyonyintono2 and P. Nakitto3
1
Division of Food Sciences, School of Biosciences, University of Nottingham, Sutton
Bonington Campus, LE12 5RD, Loughborough, Leicestershire, United Kingdom.
2
Department of Food Processing Technology, Kyambogo University, P.O. Box 1, Kampala,
Uganda.
3
School of Nutritional Sciences, Institute of Biochemistry, Food Science and Nutrition,
Hebrew University of Jerusalem, P.O. Box 12, Rehovot, 76100, Israel.
ABSTRACT

Food borne diseases such as Salmonellosis and entero-haemorrhagic Escherichia coli (EHEC)
have been associated with consumption of street-vended foods in many African countries.
Although health problems associated with consumption of street-vended foods do exist in
Uganda, up to this day, there is limited scientific data on the microbiological quality and safety of
street-vended foods in various regions of the country. The aim of this study was to establish the
occurrence of common food-poisoning pathogens including E. coli and Salmonella spp. in
selected street-vended foods sold in Nakawa and Naguru Parishes located in peri-urban Kampala
city. Samples analyzed in the present study were based on four food categories which comprised
of mainly high risk foods and those prone to adulteration by dubious street food vendors. In
particular, food samples including fish stew, meat stew, fried eggs, salads, and unbottled drinking
water were taken for microbial analysis from the study area. Standard microbiological methods
were used for isolation, enumeration, and identification of bacteria. The SPSS software was used
for the analyses and the significance level was set at p<0.05. Binary stepwise logistic regression
analysis was used to investigate factors that may influence exposure of street-vended foods to
pathogens. In the results, E. coli levels were found to be 100% and 60% in Nakawa and Naguru
Parishes respectively. Microbial enumeration of Salmonella spp. was negative for all samples
tested. Vendors who did not meet adequate personal hygiene standards, adjusted odds ratio,
AdjOR: 0.96, CI: 0.85-0.99 and those who stored food at inappropriate temperatures, AdjOR:
0.88, CI: 0.47-0.97 were more likely to have their food exposed to pathogen spreading vectors.
The presented results indicate that street foods vended in Nakawa and Naguru Parishes are a
source of contamination as elucidated by presence of E. coli. Street food vending may be
improved by supporting the identified at-risk groups.

Key words: street foods, E. coli, Salmonella, food safety, food vending.

INTRODUCTION order to suit the local tastes and preferences, others

are commonly manufactured by local food processing
The term 'street food' refers to a wide variety of foods
industries, while some may be imported (Mensah et
and beverages prepared and/or sold by vendors and
al., 2002). In Uganda, like many other developing
hawkers especially in streets around trading centers
countries, street foods provide income and livelihood
and other public places for immediate consumption or
for many communities particularly the low-income
consumption at a later time without further processing
persons. Currently, street food vending in Uganda is
or preparation (von Holy and Makhoane, 2006).
probably the single largest employer in the informal
Whereas most street foods are prepared on a daily
sector providing affordable and convenient meals,
basis using a variety of locally available ingredients in
drinks and snacks to the majority of people especially
 Am. J. Food. Nutr, 2013, 3(3): 167-175

on journeys, those working in urban centres and a and levels of the different types of food-borne
high proportion of low-income earners in their pathogens that may be present in the various foods
residential areas. The majority of people depending sold. The study reports the occurrence and levels of
on street-vended foods are often more interested in E. coli and Salmonella spp. in some street-vended
their convenience than safety, quality and hygiene foods sold in selected Parishes of Nakawa Division
(Kumar et al., 2006; Badrie, 2012). and highlights the major factors predisposing the
foods to contamination by these organisms during
Microbiological contamination of street foods has
local production operations, handling and storage.
become a major public health concern (WHO, 2002).
The majority of street food vendors are uninformed of MATERIALS AND METHODS
good hygiene practices (GHP) (Mensah et al., 2002),
Description of the study area: Nakawa Division is
which poses increased risk of contamination for most
located in Kampala district and is comprised of six
of the food products involved (Bhaskar et al., 2004;
Parishes namely; Banda, Naguru, Mutungo, Ntinda,
Tambekar et al., 2009). Epidemiological links
Nakawa and Luzira. The study was conducted in
between street foods such as ready-to-eat (RTE), viz:
Nakawa and Naguru which were the most densely
salad vegetables, sprouts, rice and fish, and disease
populated Parishes with a large number of low-
emergence have been previously reported in India,
income persons largely involved in street food
South Wales, Egypt and the Dominican Republic
vending operations. The two Parishes have several
(Umoh and Odoba, 1999; Kumar et al., 2006). In
types of food items vended through informal markets
most parts of the world, food-borne disease
on streets and mainly target students and other low-
incidences are more commonly associated with
income persons. In most cases, the majority of food
Salmonella serotype enteritidis (SE), Vibrio cholera,
vendors are tax evaders operating in evenings after
Escherichia coli serotype 0157:H7, Listeria
the office hours of tax collecting authorities. The food
monocytogenes and food-borne trematodes (Mensah
items covered under the study were classified into
et al., 2002; Wawa et al., 2009; Tambekar et al.,
four categories on the basis of preparation method
2011; Annan-Prah et al., 2011). The emergence of
and/or main ingredient(s) as shown in Table 1.
the above mentioned disease outbreaks is mainly
linked to globalization of food supply that introduces Table 1. Categories of the various street foods
pathogens into new geographical areas, exposure of used in the study
travelers, refugees and immigrants to unfamiliar food-
borne hazards, mutations in microorganisms, Category specific food items cooking
changes in the human population and changes in method
peoples’ life styles (WHO, 2002; CDC, 2008), all of Traditionally fish, fish in frying,
which are also prevalent in Uganda. prepared local groundnut sauce, stewing
The presence in food of E. coli and other dishes chicken, beef
boiling
Enterobacteriacae such as Enterococcus faecalis is
indicative of faecal contamination (Gelsomino et al.,
2002) and suggests poor hygiene during preparation, Fast prepared fried egg, boiled egg dip-frying
handling and storage, lack of reheating and improper snacks sandwiched in fried
vending temperatures (Umoh and Odoba, 1999; irish potato
Tambekar et al., 2011). Although some studies have
reported the presence of E. coli 057:H7, Listeria spp.
and other microorganisms in some processed dairy Vegetable- fresh salads, mainly uncooked
products sold in some parts of Uganda (Wawa et al., based sliced tomatoes and
2009; Mugampoza et al., 2011), limited studies have cabbage
been conducted to assess the prevalence and levels
of E. coli and Salmonella spp. and the factors
Drinks un-bottled drinking unboiled
predisposing street-vended foods to microbial
water from various
contamination. This poses potential hazards to the
sources
rapidly growing market of these foods especially in
the peri-urban parts of the country such as Nakawa
Division. Moreover, there is insufficient surveillance
mechanisms in Uganda to establish the occurrence

168

Establishing the factors influencing microbial
contamination of street foods: Street food vendors
in the major streets and markets of Naguru and
Nakawa Parishes (n = 96) were the main subjects of
the study. Prior to data collection, information about
the purpose of the study was given to the targeted
street food vendors in the study area by the
researchers. The aspect of confidentiality of data and
respect for food vendors’ privacy was observed at all
times. Direct observation and a validated semi-
structured questionnaire were used to collect the
socio-demographic information of selected street
vendors as well as other qualitative data. The
qualitative data included methods of food
preparation, handling and storage as well as
adequacy of sanitary requirements in regard to
hazard analysis and critical control points (HACCP)
and personal habits of food handlers.
Sampling: Approximately 500g samples of food
items in each category (Table 1) were systematically
purchased from different street vendors operating in
the study area using stratified random sampling,
whereby each Parish constituted a stratum. The
samples were aseptically transferred into separate
sterile stomacher bags, labeled and delivered to the
Uganda National Bureau of Standards (UNBS)
microbiology laboratory in chilled plastic boxes for
analysis within 24hrs of collection. Initially, total
aerobic counts were enumerated on 30 random
samples in order to determine the foods with the
highest risk of microbial contamination.
Detection and enumeration of E. coli: The
presumptive E. coli (EC) were enumerated using the
most probable number (MPN) technique as described
in the bacteriological analytical manual (BAM) (Feng
et al., 2002). Twenty five gram samples were added
to 225ml peptone water and homogenized for 2
minutes, 230rpm in stomacher bags used to suspend
microbial cells, obtaining the initial dilution of 10 -1.
Further 10-fold dilutions up to 10-9 were prepared in
peptone water. The samples (1ml) from each dilution
series were transferred in triplicates into 16mm
Durham tubes containing 9ml of lauryl tryptose broth
(LTB) and gently rotated to suspend any adhering
matter into the liquid. All tubes were incubated at
35oC for 24-48h and observed for turbidity and gas
production which was indicative of the positive result.
All tubes with positive results were sub-cultured in
16mm Durham tubes of EC broth by transferring 1ml
inoculants into 9ml broth. The tubes were further
incubated at 45oC for 48h and observed for turbidity
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Am. J. Food. Nutr, 2013, 3(3): 167-175
and gas production. The MPN was calculated based
on results of EC tubes.
Confirmatory test for E. coli: Samples (0.1ml) from
EC broth tubes with positive results were surface
spread on tellurite-cefexime sorbitol MacConkey agar
(TC-SMAC) and further incubated at 37oC for 24h.
The plates were examined for 1-2mm neutral/grey
colonies with smoky centers. Presumptive colonies
that were characteristic of E. coli were streaked onto
tryptic soy agar (TSA) with 0.6 % yeast extract and
incubated at 37oC for 24h. Pure colonies were sub-
cultured in peptone water, incubated at 37oC for 24h
and tested for indole production by adding 5 drops of
,
xylene and Kovac s reagent. A red colour was
indicative of E. coli.
Detection of Salmonella spp: Salmonella spp. were
detected using the bacteriological analytical manual
(BAM) method (Feng et al., 2002). Samples (25g)
were aseptically added to 225ml sterile lactose broth
(LB) and homogenized in stomacher bags for 2
minutes, 230rpm to suspend microbial cells. The
mixture was incubated at 35oC for 24±2hrs to allow
enrichment. Then, 1ml portions were transferred into
10ml selenite cystine broth (SCB) in 16x150mm
tubes and further incubated at 35oC for 24±2hrs to
allow selective enrichment for Salmonella spp. The
tubes were vortexed briefly and cultures streaked on
bismuth sulphite agar (BSA), hektoen enteric agar
(HEA) and xylose lysine desoxycholate (XLD) agar
and further incubated at 35oC for 24±2hrs. The plates
were examined for typical Salmonella colonies as
follows: brown, grey or black without metallic sheen
(BSA); blue or blue-green with or without black
centres (HEA); pink colonies with or without black
centers (XLD). Two typical colonies from each of the
selective media were inoculated into triple sugar iron
(TSI) and lysine iron (LI) agar slants by stabbing
about 4mm deep followed by streaking using an
inoculation loop. The agar slants were incubated at
35oC for 24±2hrs with loose caps. TSI tubes were
observed for red slants (alkaline) and yellow butt
(acid) with or without blackening whereas LI slants
were observed for purple coloration of the butt
(alkaline). Presumptive Salmonellae from TSI and LI
agar slants were inoculated into 10ml urea broth
(UB), incubated at 35oC for 24±2hrs and subjected to
methyl red (MR), indole and Voges Proskauer (VP)
tests for confirmatory identification of Salmonella spp.
The VP test was conducted by transferring 1ml of UB
culture into MR-VP medium and incubating at 35oC
for 24±2hrs. Naphthol solution (0.6ml) and 40%
potassium hydroxide were added and after shaking, a
 Am. J. Food. Nutr, 2013, 3(3): 167-175

few crystals of creatine added, the mixture was confidence intervals were calculated for each factor
allowed to stand for 2hrs and observed for Eosin pink and reported. A 95% confidence interval (CI) and a
colouration which was indicative of VP positive significance level of p<0.05 were used for any
reaction. MR test was conducted by incubating the analyzed variable in the present study.
MR-VP medium for additional 48±2hrs at 35oC after
RESULTS
the VP test. Then 5 drops of MR solution were added
and observed for a distinct red solution which was Occurrence of E. coli and Salmonella spp: The
indicative of a positive reaction. Indole test was occurrence and levels of the bacterial pathogens
performed by inoculating positive cultures from TSI varied significantly (p<0.05) with the type of sample
agar into tryptone broth (TB) followed by incubation and sampling site (Table 1). Salmonellae were not
at 35°C for 24±2hrs. Then, 0.3ml of Kovacs’ reagent detected in all samples analyzed. E. coli was
was added to 5ml TB culture in a test tube and detected in all samples from Nakawa and Naguru
observed for deep red coloration, which was positive Parishes. In comparison, samples from Nakawa had
for Indole test. lower levels of E. coli compared to those obtained
from Naguru Parish (Table 2). Levels of E. coli in fish
Statistical analyses: Microbial counts were
(0.29±0.05 and 0.29±0.05 log10 Cfu/g) and meat stew
normalized by transformation to log 10 Cfu/ml. In order
(0.29±0.07 and 0.36±0.01 log10 Cfu/g) from both
to establish statistical significant differences of
Parishes were not significantly different (p>0.05) and
microbial loads in Nakawa and Naguru parishes,
generally lower than the acceptable standard of 2
analysis of variance (ANOVA) was applied. The
log10 Cfu/g in ready to eat foods according to
Statistical Package for Social Sciences Software v.16
previous research results established (Richards et
(SPSS Inc.; Chicago, Illinois, USA 2007) and
al., 2000). The occurrence of E. coli was higher in
Microsoft Office Excel 2007 were used for data
fried eggs, salads and un-bottled drinking water with
processing and analysis. Descriptive statistics were
mean counts ranging from 4.27±0.31 to 7.48±0.20;
generated for variables under study, particularly with
0.28±0.07 to 11.99±0.15 log10 Cfu/g; and confluent
frequency distributions for categorical data. Logistic
growth respectively. In respect to this observation,
regression was performed to predict which vendor
samples from Naguru showed relatively higher levels
characteristics were related to the aspect of exposure
of contamination than those obtained from Nakawa
of the vended food to pathogen spreading vectors.
Parish for the above mentioned foods.
The dependent outcome used in logistic regression
analysis was whether street-vended foods were Table 2. Occurrence and levels of E. coli and
exposed or non-exposed to pathogen spreading Salmonella spp. in some street-vended foods
vectors. The dependent variable was tested for from different sites in Nakawa Division
normality using normal Q-Q plots with descriptive
E. coli (log10 CFU/g) Salmonella spp.
statistics. To explore the explanatory variables (log10 CFU/g)
associated with the outcome of interest, factors that Sample
were statistically significant (p<0.05) with bivariate Nakawa Naguru Nakawa Naguru
analysis when analyzed independently were included Fish 0.29±0.05a 0.29±0.05 not not
in the multivariate logistic regression models. stew detected detected
Inferential statistics including Pearson’s correlation
were used to determine the linear relationship Meat 0.29±0.07 0.36±0.01 not not
between variables of interest and to test for co- stew detected detected
linearity between independent variables considered Fried 4.27±0.31 7.48±0.20 not not
for logistic regression. The Forward Log likelihood eggs detected detected
ratio (FLR) stepwise selection method was used in
Salads 0.28±0.07 11.99±0.15 not not
the multivariate models to evaluate the final positive detected detected
predictors and the potential risk factors for the
outcome. The values used for entry and removal of Un- confluent confluent not not
each variable from the final models were set at bottled growthb growth detected detected
default SPSS settings; 0.05 and 0.01 respectively. drinking
water
The goodness-of-fit for the final models was based
on the Hosmer and Lemeshow goodness-of-fit a
Values are means of three determinations ±
statistic test. The crude odds ratios and adjusted standard deviations. bConfluent growth (no discrete
odds ratios (AdjOR) together with their 95%

170

countable colonies due to continuous growth
covering all media on Petri dish)
Factors predisposing street foods to microbial
contamination: Direct observation studies showed
that the majority vendors in Nakawa Division (67.1%,
of 96) operated stalls located very close to the main
streets exposing the foods to dust and other physical
contaminants. About twenty percent of the vendors
had access to hand washing facilities. Washing of
hands, utensils and dishes was often done in open
space in plastic buckets. The majority brought their
water supply in plastic buckets or collected water
from a near-by-public tap source. Further, street food
vendors stated that they lacked proper lighting and
toilet facilities (toilet paper, running water). In most
cases (75%), there was no refrigeration/cooling
facility due to lack funds to purchase them or
insufficiency of modern well constructed permanent
vending units equipped with electricity supply.
Traditional foods were often kept covered in plastic
containers. Generally, the immediate surroundings
were often filled with garbage (organic litter) and no
garbage bins were provided by the city council
authorities for waste disposal. In most instances,
street foods were purchased and consumed in the
same location. In Naguru Parish, only 33.3% of
vendors had their heads covered, the majority wore
usual clothing. In all instances, ready-to-eat meals or
fast serve foods such as fried eggs were normally
Table 3. Bivariate logistic regression analysis for factors contributing to exposure of street-vended
foods to pathogens1
Variable, n=96 Category
Location of food from the street Too close
Appropriately located
Environmental sanitation in
respect to HACCP
Unsuitable
Suitable
Regular hand washing facilities
Not available
Personal hygiene of food vendor
Available
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Am. J. Food. Nutr, 2013, 3(3): 167-175
grilled for about five minutes on flat iron plates heated
by timber charcoal. Vegetables salads were usually
hand-chopped on open wooden cut-boards and
served to consumers without further heat treatment.
A number of explanatory variables were significantly
(p<0.05) associated with exposure of food to
pathogen-spreading vectors among vendors when
analyzed with bivariate and multivariate logistic
regression analyses (Tables 3 and 4). Binary analysis
revealed that factors including availability of food-
handling equipment, type of food sold (home-made or
industry manufactured), whether or not vendors were
regularly monitored by public health officials, social
behaviors & health habits of vendors such as
smoking, coughing, sneezing, etc, as well as method
of waste and refuse disposal used by the vendors
were not significantly (p>0.05) associated with
exposure of the foods to pathogen-spreading vectors.
Interestingly, binary analysis suggested that some
key factors such as location of food sold from the
street, environmental sanitation in respect to HACCP
system, education level of the food vendor and
knowledge of food laws regarding hygienic vending of
foodstuffs were all significantly (p<0.05) associated
with exposure of the street foods to pathogens (Table
3). However, most of these factors from binary
analyses were not independent significant predictors
for exposure of food to pathogens with multivariate
analysis as shown in the final model below (Table 4).
Crude OR (95% CI) p value
12.10 (3.97-36.87) <0.001
1.00
0.99 (0.95-1.00) <0.001
1.00
0.94 (0.80-0.98) <0.001
1.00
 Am. J. Food. Nutr, 2013, 3(3): 167-175

Variable, n=96 Category Crude OR (95% CI) p value

Not suitable 0.98 (0.91-0.99) <0.001
Food storage temperature
Suitable 1.00

Not appropriate 0.93 (0.79-0.98) <0.001

Education level of food
vendors Appropriate 1.00

Not attended 33.00 (6.83-159.55) <0.001

school vendor
Primary school
5.62 (1.52-20.80)

Secondary school
1.00

Knowledge of food laws No 0.85 (0.85-0.99) <0.001

regarding hygienic vending of
foodstuffs
Yes 1.00

1
Each variable was used independently with binary logistic regression analysis and mainly statistically significant
variables are presented (p<0.05), OR: Odds ratio; CI: Confidence interval; 1.00: Reference groups
Table 4. Multivariate logistic regression model for exposure of street foods sold in Nakawa Division to
food-borne pathogens using the FLR stepwise method1
Variable, n=96a Category AdjOR (95% CI) p value
Personal hygiene of food Not suitable 0.96 (0.85-0.99) <0.001
vendor

Suitable 1.00

Food storage temperature Not appropriate 0.88 (0.47-0.97) 0.005

Appropriate 1.00
1
Final model had Hosmer and Lemeshow goodness of fit statistic test as χ² =0.29, p= 0.87 and the model
constant had p value of <0.001
DISCUSSION 2002). The high E. coli counts observed in the RTE
food samples is similar to other studies (Badrie et al.,
The occurrence and levels of E. coli in fried eggs,
2002; Kumar et al., 2006) and warrants further
salads and un-bottled drinking water was higher than
investigation of the conditions of preparation. E. coli
the acceptable standard of 2 log10 Cfu/g (Feng et al.,
count is an important criterion for evaluating the
172

sanitary quality of various foods (Gelsomino et al.,
2002). Use of contaminated ingredients, aerial
contamination from dust, cross contamination from
personnel and inadequately cleaned containers are
likely sources of contamination into RTE foods and
drinks (Food Standards Agency, 2011). The
concentration of E. coli greater than 2 log10 Cfu/g in
RTE is considered to be of high risk to consumers
(Wawa et al., 2009), especially if pathogenic strains
of the organism such as verotoxigenic E. coli (VTEC)
0157H and enterotoxigenic E. coli (ETEC) are
involved (Moxley et al., 1998; Woodward et al.,
2002). Variation in E. coli counts among the different
street foods under the present study may be largely
attributed to differences in methods of preparation
and use of raw materials with different levels of
contamination with the organism (Estrada-Garcia et
al., 2004). The occurrence of E. coli in fish and meat
stews was relatively low and similar to that reported
in other countries (Suwimon et al., 2009; Abong’o
and Momba, 2009). Although E. coli is has low
thermal tolerance at temperatures above 50oC
(Delaney, 1990), stationary-phase cells of the
organism can exhibit acid, heat, salt and starvation
tolerance due to expression of the genes rpoS and
grpE (Delaney, 1990), which may partly explain our
results. This may partly explain why inadequate
thermal processing and cross contamination of RTE
cooked foods is often associated with sporadic
disease outbreaks linked to consumption of food
products contaminated with pathogenic strains of E.
coli (CDC, 2006; Manning et al., 2008). Heat shocked
cells of E. coli can remain viable under cold storage
for several days at temperatures of 0-4°C (Karine et
al., 2003; Malay, 2006). Although pasteurization kills
most pathogens in food products (Allen et al., 2004),
contamination can still occur during packaging.
However, improperly performed pasteurization and
post pasteurisation cross contamination are the most
likely explanations for the presence of E. coli in fish
and meat stews samples in this study. The
occurrence of Salmonella spp. in street foods sold in
Nakawa Division was, as expected, not frequent and
generally not detected in the study. Contamination of
street foods with Salmonella spp. has been reported
in other countries with incidences of 17% in Malaysia
(Arumugaswamy et al., 1995), 5% in Mexico
(Estrada-Garcia et al., 2004) and 6% in Addis Ababa,
Ethiopia (Muleta and Ashenafi, 2001). The reported
incidence of virulent strains of Salmonella has been
attributed to the differences in hygiene conditions
during food handling, processing and storage of the
food products. The results of this study suggest that
173
Am. J. Food. Nutr, 2013, 3(3): 167-175
sanitary handling of street foods as well as presence
of waste close to food preparation and vending
premises in Nakawa Division are major contributory
factors to contamination with E. coli.
CONCLUSION
Fried eggs, salads and un-bottled drinking water sold
in Nakawa Division present a health risk of infection
given their high levels of E. coli. There is need for
comprehensive risk assessment of E. coli from food
products under the Ugandan local food production,
processing and handling environments. The
occurrence and levels of E. coli in hot meat-based
stews was lower than 1 log Cfu/g implying adequate
heat treatment is important in control of the organism.
The presence of E. coli in fried eggs suggests post-
preparation contamination as this RTE food is usually
prepared using dry heat. There is need to identify
pathogenic strains of E. coli in various street foods
sold in Uganda. Further studies should focus on
identification of major sources of E. coli in street food
preparation, storage and vending premises. This may
be an important step in risk assessment and
controlling the incidence of these organisms in street
foods in Uganda. Overall, the study highlighted the
need for effective sensitization and education to
stakeholders on microbiological food risks, proper
instruction and supervision in food handling
procedures. Greater consumer/vendor education on
transmission of enteric food-borne diseases and food
safety risks and how safely to cook and serve foods,
and more vigilance in street food vending monitoring
by competent food inspectors is needed to ultimately
ensure food hygiene that provides food safety.
ACKNOWLEDGEMENT
This work was funded by Kyambogo University
(Uganda) while Uganda National Bureau of
Standards (UNBS) provided the technical support.
Authors are grateful to Mr. Charles Odongwun
(UNBS) for his assistance in the laboratory.
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