Bacterial and parasitic contaminants of salad vegetables sold in markets in Fako Division, Cameroon and evaluation of hygiene and handling practices of vendors
Akoachere et al. BMC Res Notes
Bacterial and parasitic contaminants of salad vegetables sold in markets in Fako Division, Cameroon and evaluation of hygiene and handling practices of vendors
Jane‑Francis Tatah Kihla Akoachere 0
Bertrand Fossi Tatsinkou 0
Joseph Mbapngong Nkengfack 0
0 Department of Microbiology and Parasitology, Faculty of Science, University of Buea , PO Box 63, Buea, South West Region , Cameroon
Objective: Increase in awareness of the health benefits of vegetables has resulted in an increase in consumption. Many vegetables are consumed raw to retain the natural taste and heat labile nutrients. The safety of raw vegetables is a great concern. We investigated the bacteriological and parasitological quality of salad vegetables sold in three major markets in Fako Division Cameroon, the hygiene and preservation practices of vendors and determined the antimicrobial sensitivity of bacterial isolates, to provide data that could be used to improve food safety and safeguard public health. Results: Bacterial contamination was high. Mean aerobic bacteria counts ranged from 2.5 × 106 to 15 × 106 cfu/g, total coliform counts from 4 to > 2400/g and fecal coliforms < 3 to 1100/g. Six bacterial species were isolated among which Staphylococcus aureus (35.4%) predominated while Serratia marcescens (8.5%) was the least. Bacteria showed high resistance to erythromycin (87.6%). Ten parasitic organisms were detected. Balantidium coli (25.6%) and Entamoeba spp. (21.7%) predominated. Contamination was highest in lettuce and lowest in green pepper. Hygiene and vegetable preservation practices of vendors were poor and could aggravate contamination. Contamination of fresh salad vegetables with pathogenic bacteria and parasites could be a food safety concern in study area.
Salad vegetables; Pathogenic bacteria; Antibiotic resistance; Intestinal parasites; Hygiene practices; Cameroon
Vegetables have health promoting characteristics [
being a source of vitamins and minerals, and
phytochemicals some of which are antioxidant, phytoestrogens and
anti-inflammatory agents. The recent increase in
awareness of the health benefits of vegetables has resulted in
increased consumption. Insufficient consumption of fruit
and vegetable contributes to poor health and increases
the risk of noncommunicable diseases .
Consumption of vegetables as part of a diet contributes to weight
] reducing the risk of obesity, a risk factor for
noncommunicable diseases. Because of their health benefits,
WHO and FAO in 2003 launched a global initiative to
promote the consumption of fruits and vegetables [
A lot of vegetables are consumed raw as salad to retain
the natural taste and heat labile nutrients. The safety of
vegetables eaten raw is a great concern as they have been
shown to harbor pathogenic bacteria [
]. Poor hygienic practices in the production
and post-harvest system contribute to contamination [
]. There are documented outbreaks of human
infections associated with the consumption of raw vegetables
]. Trade has contributed to geographic spread of these
]. Recent years have witnessed an increase
in the frequency of occurrence of these infections.
Studies in developed and developing countries have
demonstrated the potential of raw vegetables to transmit
8, 9, 21–23
]. Data on microbial quality of
vegetables in Cameroon is scarce despite the fact that it
has witnessed an increase in vegetable consumption and
cultivation, as cultivation in addition to ensuring food
security, has become an income generating activity [
]. Recent studies in Cameroon have reported the use
of contaminated water for irrigation of vegetables [
]. Thus, there is an urgent need to evaluate
microbiological safety of salad vegetables sold in Cameroon.
This study was aimed at investigating the microbiologic
quality of salad vegetables from markets in Fako,
Division Cameroon, to highlight their potential in disease
transmission and provide data that could guide policy
to improve food safety and safeguard public health. The
hygiene and preservation practices of vendors were also
Study area and study design
The study was conducted in three towns in Fako,
Cameroon: Buea, Tiko and Limbe. Buea, the capital of
Southwest region is located on the eastern slopes of Mount
Cameroon. According to data from the Cameroon
Development Corporation (CDC) annual rainfall in Buea
varies between 3000 and 3500 mm. Buea being the capital
of former West Cameroon receives tourists who visit
historic sites as well as Mount Cameroon.
Limbe is situated along the Atlantic coast of West
Africa. It is bordered in the north by Buea, east by Tiko,
west by Idenau and south by the Atlantic Ocean. Limbe
and Buea have recently experienced an expansion in hotel
and restaurant business as these towns have been hosting
many national and international events.
Tiko is located 21 km from Limbe, and has a
temperature range of 35–37 °C. Limbe and Tiko have warm
equatorial climatic conditions. Humidity is as high as 80%.
Six vegetable types were purchased weekly from
randomly selected vendors in three markets: Buea Central
Market, Tiko Market and Limbe Market, for a period of
10 weeks from October to December 2015 and analyzed
for bacteria and parasite contamination. The
antimicrobial susceptibility of bacteria isolates and the hygiene and
preservation practices of vendors were investigated.
Sample collection and processing
Thirty samples each of cucumber, carrot, lettuce, green
pepper, green cabbage and red cabbage were purchased
from randomly selected vendors. One sample of each
vegetable was collected per week per site for 10 weeks
(total of 180 samples). Each sample was placed in a sterile
polythene bag and transported to the laboratory at
temperature range 4–6 °C. Twenty-five grams of sample was
immersed in 225 ml of sterile distilled water for 15 min,
vigorously agitated and waste water used for analyses.
Enumeration of aerobic bacteria, total coliforms and fecal coliforms
Aerobic bacterial count was determined by the pour plate
method using nutrient agar (Liofilchem® s.r.l., Italy). A
10−4 dilution of waste water was prepared and 1 ml
inoculated. Plates were incubated at 37 °C for 24 h.
Undiluted wash water was used for the enumeration of
coliforms. Total and fecal coliforms were enumerated by
the multiple fermentation test [
Isolation and identification of bacteria
The following media from Liofilchem® s.r.l. (Italy) were
used: nutrient agar, MacConkey agar, Salmonella-Shigella
agar and mannitol salt agar. Agar plates were inoculated in
duplicate with 100 µl of sample by the spread plate
technique. Prior to inoculation of Salmonella–Shigella agar,
samples were pre-enriched overnight in selenite F broth
(Becton, Dickinson & Company) at 37 °C. Plates were
incubated at 37 °C for 24 h. Pure cultures were
characterized by Gram staining, motility, oxidase and catalase tests,
and growth on triple sugar iron agar (Oxoid) [
positive cocci were subjected to the coagulase test. The
identity of gram negative rods was confirmed using the
Analytical Profile Index 20E (Biomérieux SA, France) kit.
Antimicrobial susceptibility testing
The standard disc diffusion technique [
] was used.
The following antibiotic discs from Oxoid (Basingstoke,
England) were used: erythromycin (10 μg), gentamycin
(30 μg), ampicillin (10 μg), ciprofloxacin (5 μg),
chloramphenicol (30 μg) and streptomycin (10 μg). The
diameters of inhibition zones were compared with those of the
Clinical Laboratory Standards Institute (CLSI) [
Undiluted waste water was poured through sterile gauze
and left for about 10 h to sediment. The supernatant was
discarded and sediment centrifuged at 1207×g for 5 min.
A drop of the sediment as well as iodine stained smears
were examined microscopically. Identification was based
on their morphology [
Evaluation of hygiene and preservation practices of vendors
A questionnaire was administered to 60 vendors (20
from each market), randomly selected from those
samples were obtained. Data was also collected by visual
Data was entered in Epi Info version 3.5.3 and exported to
SPSS version 20. The ANOVA test was used to compare
differences in mean aerobic bacterial counts between
various types of vegetables. The Bonferroni corrected
post hoc t test (significance at P ≤ 0.0083) was used to
compare the means of aerobic bacterial counts, total
coliform counts and fecal coliform population of vegetables
from various sites. The Chi square test was used to
examine differences in the occurrence of bacterial isolates and
parasites. Values were considered significant at P ≤ 0.05.
Aerobic bacterial, total coliform and fecal coliform load of samples
Aerobic bacteria counts were high, ranging from
2.5 × 106 to 15 × 106 cfu/g. Lettuce had the highest mean
count (9.5 × 106 cfu/g) while green pepper had the lowest
(5.2 × 106 cfu/g) (Fig. 1). ANOVA test showed a
significant difference in counts between vegetables (P = 0.00).
The overall mean total coliform count was highest in
lettuce (1171.6 ± 117.16/g). In Tiko, mean counts were
significantly higher in green cabbage (P < 0.0083) while in
Limbe and Buea, counts were significantly higher in
lettuce (Table 1).
Fecal coliforms were detected in all samples.
Carrots and lettuce had highest count (248.9 ± 397.72 and
165.03 ± 270.95/g respectively). There were no
significant differences in counts between vegetables (P ˃ 0.0083)
Six bacteria species were isolated. Staphylococcus aureus
(83.9%) was the predominant organism while Serratia
marcescens (20%) was the least (Fig. 2). All six species
were detected in all vegetable types. S. aureus was most
frequently isolated from leafy vegetables while other
bacteria were more frequently isolated from carrots.
Antimicrobial susceptibility of isolates
Ciprofloxacin (95.1%) was the most active drug.
Resistance to erythromycin (75.6%) was highest. With the
exception of 96 isolates of Staphylococcus aureus
susceptible to erythromycin, all other bacteria were resistant
(Additional file 1). One Shigella isolate was resistant to all
Fig. 1 Mean aerobic bacterial counts (× 106 CFU/g) of samples from study sites. Mean aerobic bacterial load of samples was generally high.
Highest counts occurred in leafy vegetables green cabbage (GC), red cabbage (RC) and lettuce (LE) compared to non‑leafy cucumber (CU), green
pepper (GP) and carrots (CA). Number of each sample analyzed (n) = 30. ANOVA test gave a significant difference (P = 0.00) in counts between
999.7 ± 1046.15
613.8 ± 914.84
1171.6 ± 117.16
365.7 ± 616.24
722 ± 1081.44
170.73 ± 264.34
Fig. 2 Distribution of bacteria isolates in samples. Six species of bacteria, mostly enteric organisms were detected in vegetables. S. aureus, the
only non‑ enteric organism was the most frequently isolated. All six species were present in all types of vegetables. Only C. freundii (X2 = 16.118,
P = 0.007) showed significant differences in the occurrence in various types of vegetables
Contamination with parasites
Ten parasitic protozoans and helminths were detected.
Balantidium coli (32.4%) was most frequently detected
(Additional file 2). With the exception of Trichuris
trichiura, all parasites were detected in Buea (Additional
file 3). The highest level of contamination occurred in
lettuce (25.4%) and the least in green pepper (8.5%)
(Additional file 4). Balantidium coli and Entamoeba spp.
were detected in all vegetable types.
Evaluation of hygiene and preservation practices of vendors
More females (76.5%) participated in the survey. The
majority of participants (41.7%) had no formal
education, and did not cultivate the crops (85%). Hand washing
with soap was practiced by 23.3%. Only 16.7% had
formal training on hygiene and food preservation
(Additional file 5). Washing of vegetables was practiced by
35.0% amongst which 38.1% used stream water. None of
the vendors transported vegetables to the market or sold
them under controlled temperature conditions.
Vegetables were placed on dirty bags during sale. Unsold
vegetables were kept in the market (55.0%) or left in the
backyard of their houses (45.0%).
Samples had high aerobic bacterial counts. Uzeh et al.
] reported high levels of bacteria in raw vegetables.
Bacterial counts were in the order: Lettuce > red
cabbage > green cabbage > cucumber > carrot > green
pepper. Foods are regarded as harmful when the
bacterial load is high even if the bacteria are not known to be
]. Coliforms were detected in all samples.
Mean counts showed a pattern similar to that observed
for bacterial load. Lettuce leaves have a large surface area
suitable for water, soil and air contact, and fecal
droppings from birds making it more susceptible to
contamination than the other vegetables. Green pepper is raised
above the ground reducing contamination by soil
bacteria. Its surface is smooth and surface area small
limiting colonization. Highest fecal coliform counts were
observed in carrots similar to the report of Weldezgina
and Muleta [
]. Carrots being a root crop could have
received contamination from the soil, irrigation water,
animal wastes used as fertilizer, water used for
washing and from handlers. Its pits and crevices retain dirt
containing organisms which may not be easily removed
by slight washing. Recent studies in Cameroon [
] report that these vegetables are irrigated with
fecally polluted water. Six bacteria species were isolated
with Staphylococcus aureus predominating. Apart from
Staphylococcus aureus, all isolates are enteric organisms
indicating fecal contamination. Similar bacteria have
been isolated elsewhere [
10, 37, 38
]. Isolates were most
sensitive to Ciprofloxacin and resistant to erythromycin.
One isolate of Shigella was resistant to all six antibiotics
tested. Antibiotic-resistant bacteria or resistance
determinants are known to spread to humans via the food
]. Thus raw vegetables could be a source of
multi-drug resistant pathogenic bacteria.
Ten species of intestinal parasites were detected.
Surveys in other parts of the world have also shown that raw
vegetables could be agents for transmission of these
]. Balantidium coli predominated similar to the
report of Simon-Oke et al. [
]. Contrary to our findings,
Alade et al. [
] reported a higher prevalence of Ascaris
lumbricoides, while Olyaei and Hajivandi [
Toxocara leonine. Similar to Olyaei and Hajivandi [
we observed a low prevalence of Fasciola spp. and
Trichuris trichiura. Leafy vegetables and carrots were more
contaminated. Their uneven surfaces facilitate
microbial attachment. Similar to Abougraina et al. [
Mohamed et al. [
], the highest level of parasite
contamination was in lettuce and least in vegetables with smooth
Our study showed a higher level of contamination
(61.6%) with intestinal parasites than 13.5% in Khartoum
], 36% in Ghana [
], and 58% in Tripoli [
However, a higher rate of contamination (75.9%) was reported
in Kenya [
]. The detection of enteric bacteria and
parasites in samples implies that they could be contaminated
with enteric viruses. The majority of the participants do
not practice good hygiene thus increasing the chances of
contamination. Transportation to the market was under
unhygienic and uncontrolled temperature conditions and
this favour the growth of microorganisms [
]. Our study
shows that there is an urgent need to sensitize vendors
on good hygiene and preservation of vegetables, and the
public on proper washing and sanitization of vegetables
prior to consumption.
We did not investigate for the presence of other
foodborne pathogens such as Listeria monocytogenes, E. coli
O157:H7 as well as enteric viruses. We did not include
a control strain in susceptibility testing. Also, the
minimum inhibitory concentration (MIC) of potent
antibiotics was not investigated.
Additional file 1. Antimicrobial susceptibility of bacteria isolates. Bacteria
isolated were tested against six antibiotics of different classes. Cipro‑
floxacin was the most active drug while resistance to erythromycin was
Additional file 2. Occurrence of Parasites in samples. Ten species of para‑
sites at various developmental stages were detected. Balantidium coli was
the most frequently detected while Trichuris trichuria was the least.
Additional file 3. Distribution of parasites in study sites. Not all ten
species were detected in each study site. Ascaris lumbricoides, hookworm,
Strongyloides stercoralis, Balantidium coli and Entamoeba species were
detected in all study sites.
Additional file 4. Distribution of parasites in vegetables. All parasites
were not detected in all types of vegetables. Only B. coli and Entamoeba
species were found in all types of vegetables.
Additional file 5. Characteristics of vendors and hygiene and preserva‑
tion practices. Hygiene and preservation practices of vendors was poor
and this could aggravate contamination.
WHO: World Health Organisation; FAO: Food and Agricultural Organisation;
CDC: Cameroon Development Cooperation; APHA: American Public Health
Association; CFU: colony forming units; MPN: most probable number.
J‑FKTA designed and coordinated the study, analyzed data and drafted the
manuscript; BFT designed the study and reviewed the manuscript; JMK col‑
lected and analyzed data. All authors read and approved the final manuscript.
We are grateful to Mr. Ojong Samuel of the Clinical Diagnostic Laboratory of
the University of Buea, Cameroon for his assistance in parasite identification.
We greatly appreciate the vendors of salad vegetables for sacrificing their
business time to participate in this study.
The authors declare that they have no competing interests.
Availability of data and materials
All data generated or analyzed during this study are included in this published
article [and its additional files].
Consent for publication
Ethics approval and consent to participate
Ethical clearance for this study was obtained from the Institutional Review
Board Faculty of Health Sciences, University of Buea. All participants were
informed about the objectives of the study and their participation was
voluntary. Participants signed an informed consent form to indicate their
willingness to participate in the study. When necessary, questions were
asked in Pidgin English (a local language) and the researcher completed the
We received no funding for this study. The study was financed by authors.
Springer Nature remains neutral with regard to jurisdictional claims in pub‑
lished maps and institutional affiliations.
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