A Survey of Bacterial Contaminants in Leaty Vegetables
A Survey of Bacterial Contaminants in Leaty Vegetables
A Survey of Bacterial Contaminants in Leaty Vegetables
Email address:
avural@dicle.edu.tr (A. Vural)
Abstract: Two hundred sixty one samples, collected from supermarkets in Istanbul, Turkey. All samples were analysed for
aerobic mesophilic bacterial counts (AMC), aerobic psychrotrophic bacterial counts (APC), enumeration of yeasts and moulds
(YM), coliforms, Escherichia coli and detection of Escherichia coli O157:H7, Salmonella spp., Listeria monocytogenes,
thermotolerant Campylobacter spp. AMC ranged from 2.95 to 3.75 log10 CFU/g. APC ranged from 0 to 3.55 log10 CFU/g. The
highest counts of coliforms were found in carrot, spinach, green leaf lettuce, cos lettuce and iceberg lettuce. The highest counts
of YM were found in tomato, spinach, green leaf lettuce, cos lettuce and iceberg lettuce. Green leaf lettuces, cos lettuces,
iceberg lettuces, spinach and carrot were highly contaminated with aerobic mesophilic (3.6 log10 CFU/g), psychrotrophic
microorganisms (3.4 log10 CFU/g), and showed a high incidence of E.coli (41.77% of samples). Of the samples analysed, 10
(3.83%) were Salmonella spp. positive and 17 (6.51%) were thermotolerant Campylobacter spp. positive. None of the samples
was positive for Escherichia coli O157:H7 and Listeria monocytogenes. Fresh vegetables and fruits, sold in Istanbul, Turkey,
are needed to control foodborne pathogens especially Salmonellosis and Campylobacteriosis.
Keywords: Food Safety, Fresh Fruit, Microbiological Quality, Raw Vegetable
parasitic and viral pathogens capable of causing human 2.3. Aerobic Mesophilic Plate Count and Aerobic
illness and a number of reports refer to raw vegetables and Psychrotrophic Plate Count
fruits harbouring potential foodborne pathogens [3, 13, 16,
22-25]. Laboratory analyses to enumarate of aerobic mesophilic
The Centers for Disease Control and Prevention has plate count and psychrotrophic plate count were performed in
reported an increase of fresh produce related foodborne accordance with the ISO 4833-1:2003 standard [30] and ISO
disease outbreaks between 1995 and 2005 around the world 17410:2001 [31], respectively.
[26]. 2.4. Enumeration of Yeasts and Moulds
Istanbul which has a geographic and geopolitics
importance due to representing a transit corridor between Laboratory analyses to enumarate of yeasts and moulds
Europa and Asia is a rapidly developing market cause of high were performed in accordance with the ISO 7954:1987
population growth rate and continuous migration from standard [32].
various regions of Turkey and the neighboring countries.
This high density of the population is regarded as a 2.5. Enumeration of Coliforms and Escherichia coli
comprehensive supply of foods. Especially, the rapid growth Samples were prepared as described above. Homogenate
of supermarkets chains in Turkey over the past ten years and or the rinse fluid was prepared using BPW. For each selected
also the subsequent development of quality requirements like dilution, 0.1 ml of sample was spread-plated onto brilliance E.
volume, regularity, quality homogeneity, range of varieties, coli/coliform agar (Oxoid, Cambridge, UK). The plates were
packaging have given rise to new market opportunities for incubated at 37 °C for 24 h, following which, the number of
local agriculture [27]. pink (coliform) and purple (presumptive E. coli) colonies
The present survey was intended to supply some was counted [33]. Identification of E. coli was carried out
assessment on the microbiological quality of marketed fresh with IMVIC tests [34].
vegetables and fruits in Istanbul, Turkey [28].
2.6. Isolation of E. coli O157:H7
2. Materials and Methods Samples were prepared as described above. Homogenate
2.1. Collection of Samples or the rinse fluid was prepared using BPW. Laboratory
analyses to detect of E. coli O157:H7 were performed in
Two hundred sixty one fresh vegetables and fruits samples accordance with the ISO 16654:2001 standard [35)].
were analyzed between the period May 2012 and January
2013. The samples analyzed included: 161 samples of whole 2.7. Isolation of Salmonella Spp.
fresh vegetables, 100 samples of fresh fruits. Samples of all Samples were prepared as described above. Laboratory
of the fresh produce sold in Istanbul were randomly analyses to detect of Salmonella spp. were performed in
purchased from different major supermarkets and local chain accordance with the ISO 6579:2002 standard [36].
markets, in their original, individual packages. Production
data of the samples are shown in table 1. 2.8. Isolation of Listeria monocytogenes
2.2. Preparation for Microbial Analysis Samples were prepared as described above. Laboratory
analyses to detect of L. monocytogenes were performed in
All samples were analysed as soon as possible after accordance with the ISO 11290 method [37].
purchase. Before samples were taken out of their original
packaging, the possible contact surfaces were carefully 2.9. Isolation and Confirmation of Thermotolerant
sterilised using polyurethane sponges to prevent cross- Campylobacter spp.
contamination. Damaged samples were discarded before
analysis. For lettuce, spinach and purslane approximately 25 Laboratory analyses to detect thermotolerant
g of each sample were placed in a sterile stomacher bag and Campylobacter spp. were performed in accordance with the
homogenized using a stomacher (Interscience - BagMixer ISO 10272-1:2006 standard (qualitative analysis) [38]. To
400 P, France) with 225 ml of sterile 0.1% buffered peptone confirm suspect isolates polymerase chain reaction (PCR)
water (BPW) (Oxoid, Cambridge, UK) for 2 min. For all methods [39] and a commercially available real-time PCR kit
other commodities, i.e. cucumber, tomato, green bean, squash, (Taq Man Campylobacter spp. Kit, AB Applied Biosystems)
carrot, plum and peach each sample (whole) was aseptically were applied. For quality control, the C. jejuni ATCC 33560
transferred into a stomacher bag filled with equal weight of reference strain was used.
BPW. Each whole sample was then agitated and rubbed by 2.10. Confirmation of Presumptive Colonies
hand in the stomacher bag for 2 min to suspend surface
microbes [23, 29]. Appropriate 1:10 dilutions of the resultant API® (bioMerieux, Marcy-l’Etoile, France) was used for
homogenate or the rinse fluid were prepared using BPW. the confirmation of presumptive colonies. The biochemical
tests were carried out according to the manufacturer’s
instructions.
154 Serkan Kemal Buyukunal et al.: Microbiological Quality of Fresh Vegetables and Fruits
Collected from Supermarkets in Istanbul, Turkey
Type of samples n Coliform count (log10 CFU/g) E.coli count E.coli presence (log10 CFU/g)
range median range median number of positive samples(%)
Green leaf lettuce 15 3.25-3.45 3.3 0-2.65 2.5 12 (80)
Iceberg lettuce 15 3.25-3.45 3.35 0-2.55 2.25 7 (46.67)
Cos lettuce 16 3.2-.3.4 3.3 0-2.6 2.35 9 (56.25)
Spinach 19 2.95-3.45 3.2 0-2.5 0 4 (21.05)
Purslane 14 2.95-3.05 3 0 0 0
Cucumber 10 2.7-2.85 2.8 0 0 0
Tomato 11 2.9-3.1 2.95 0 0 0
Green bean 11 2.3-2.8 2.7 0 0 0
Kidney bean 11 2.5-2.8 2.55 0 0 0
Squash 10 2.5-2.8 2.7 0 0 0
Eggplant 10 2.5-2.8 2.55 0 0 0
Pepper 11 2.5-2.8 2.7 0 0 0
Carrot 14 3.25-3.45 3.25 0-2.3 0 1 (7.14)
Plum 12 0-2.3 0 0 0 0
Apricot 12 0-2.3 0 0 0 0
Peach 12 0-2.3 0 0 0 0
Apple 12 2.5-2.9 2.7 0 0 0
Pear 14 2.6-2.9 2.65 0 0 0
Grape 14 0-2.3 0 0 0 0
Strawberry 18 0-2.3 0 0 0 0
Total 261 0-3.45 2.75 0-2.65 0 33 (12.64)
Table 4. The incidence of Escherichia coli O157:H7, Salmonella spp., Listeria monocytogenes and thermotolerant Campylobacter spp. in the samples
analysed.
But in our country, number and content of the study is not Tournas (4) noted that YM counts ranged between 3.1-5.95
satisfactory. Our study was planned for this reason. The AMC log10 CFU/g in lettuce, <2-5.3 log10 CFU/g in carrots, 2-3.8
for the whole vegetables and fresh fruits examined was log10 CFU/g in cucumbers, 4-4.1 log10 CFU/g in iceberg
around 3.35 log10 CFU/g, with a range of 2.95-3.75 log10 lettuce, 3.4-3.6 log10 CFU/g in spinach, 2-6.2 log10 CFU/g in
CFU/g and 3.30 log10 CFU/g, with a range of 2.95-3.50 log10 different kind of tomatoes (cherry, grape, Roma). Tournas [4]
CFU/g, respectively. Pianetti et al. [40] reported that aerobic and Tournas and Katsoudas [42] declared the some health
colony count does not relate to food poisoning and infections, problems related with the presence of yeasts and moulds in
generally. However, it acts as an indicator for food quality vegetables and fruits. Some of these may produce
and shelf life. mycotoxins and others are known to cause allergic reactions.
According to the HACCP-TQM technical guidelines, raw Aycicek et al. [10] found coliform counts up to 6.9 log10
foods containing <104 CFU/g (<4 log10 CFU/g), 104-5x106 CFU/g, E.coli counts up 3.8 log10 CFU/g. Microbial loads of
CFU/g (4-6.7 log10 CFU/g), 5x106-5x107 CFU/g (6.7-7.7 outer leaves of lettuce, cos lettuce and icerberg lettuce,
log10 CFU/g) and >5x107 CFU/g (>7.7 log10 CFU/g) parsley and dill samples detected the same levels. E.coli
(number of spoilage microorganisms aerobic plate count at positive sample percentages of raw eaten vegetable was
70°F (21.1°C) are rated as “good”, “average”, “poor” and among 10% (iceberg lettuce and carrot)-70% (parsley). Seow
“spoiled food”, respectively (41). In our study, the quality of et al. [23] noted that highest level of coliforms was found in
261 samples was regarded as “good”. bean sprouts and fresh-cut salads. Viswanathan and Kaur [14]
Aycicek et al. [10] reported some raw eaten vegetables found coliform counts ranged between 6-9 log10 CFU/g in
(lettuce, cos lettuce, iceberg lettuce, parsley, dill, carrot) total raw salad vegetables, 4-7 log10 CFU/g in fruits and 8-11 log10
aerobic counts between 0 and 7.4 log10 CFU/g. Abadias et al. CFU/g in sprouts, respectively. Also, it was reported that
[1] found the AMC ranged from 4.3 to 8.9 log10 CFU/g in prevalances of E.coli 50% of lettuces and 10% of carrots in
fresh-cut vegetables, from 2.0 to 7.1 log10 CFU/g in fresh-cut their study. Abadias et al. [1] noted that E.coli was not
fruits, from 7.1 to 9.2 log10 CFU/g in sprouts and from 2.7 to detected in fresh-cut fruit, but was present in 7.1% whole
8 log10 CFU/g in whole vegetables. APC counts were similar vegetable samples and 11.4% fresh-cut vegetable samples.
to those of mesophilic microorganism, with carrot (7.9 log10 Our findings about E.coli prevalences showed similarity with
CFU/g) and spinach (7.4 log10 CFU/g) being the vegetables these results. Especially, lettuces varieties, spinach, purslane,
with the highest mean counts. Badosa et al. [17] reported carrot etc. are risky products. Applying agricultural
fruits had AMC ranging from 1 to 8 log10 CFU/g, most of techniques should be reviewed for hygienic conditions.
them ranging between 3 and 4 log10 CFU/g. Oliveira et al. HACCP-TQM technical guidelines give threshold and
[15] noted thatthe AMC ranged from <3 to 7 log10 CFU/g in quality levels for food-borne illness hazards according to the
conventional and from 5 to >7 log10 CFU/g in organic lettuce. volunteer feeding test of healthy people groups. For, E.coli,
Psychrotrophic microorganism is very similar to those of the estimated illness dose is 6-10 log10 CFU/g and suggested
mesophilic microorganisms, with ranges between 3 to >7 level of E.coli for purchasing 1 log10 CFU/g (41). In our study,
log10 CFU/g in organic lettuce and between <3 to 7 log10 purchasing limit for E.coli was exceeded 19.76% of
CFU/g in conventional lettuce. Seow et al. (23) reported that vegetable samples (33 of the 167). On the other hand, none
AMC of fresh vegetables and fruits counts ranged from 1.6 to of the fruit sampleswere exceeded this level.
9.1 log10 CFU/g with the lowest counts recorded for orange A lot of studies were undertaken about food-borne disease
and highest counts recorded for bean sprouts. Fresh-cut related to consumption of fresh fruit and vegetable showed
salads had the highest mean APC of 4.9 log10 CFU/g. In that the number of the outbreaks has increasing day by day.
another study done by Viswanathan and Kaur [14], it was Each year millions of cases occur that most of this E.coli
reported that AMC for raw salad vegetables, fruits and 0157:H7, Salmonella spp., Listeria monocytogenes,
sprouts were in the range between 5-10 log10 CFU/g, 6-8 Campylobacter spp. etc. Infections cause mild ilness, severe
log10 CFU/g and 9-12 log10 CFU/g, respectively. These infections and serious complications-including death [43].
findings were higher than our study. These differences may Abadias et al. [1] noted that none of the fresh, minimally-
be originated from regions, geographical and climatical processed fruit and vegetables, and sprouts samples was
conditions, irrigation techniques and post-harvest processes. positive for E.coli O157:H7 and thermotolerant
Regarding the YM range of fresh produces, our findings is Campylobacter. Of the samples analyzed 1.3% was
similar to other author’s studies. Generally, lettuces, tomatoes Salmonella spp. and 0.7% were L.monocytogenes positive.
and carrots contamination is higher than the other Seow et al. [23] reported that E.coli O157:H7 and
commodities for YM. Abadias et al. [1] found that the ranges Salmonella spp. was not detected in the analyzed of total 125
for YM in fresh-cut vegetables, fresh-cut fruit, sprouts and fresh fruits and vegetables samples. Al-Hindawi and Rished
whole vegetables were 2.0-7.8, 1.7-4.9, 2.8-7.6 and 2.2- 6.1 [44] reported that 7% of 43 vegetables samples were detected
log10 CFU/g, respectively. Grated carrot was the highest mean positive for Salmonella spp. Ercolani [45] noted that 68.3%
counts for YM (6.1 log10 CFU/g). Oliveira et al. [15] reported rate of Salmonella in lettuces. Garcia-Villanova Ruiz et al.
that 51.4% of the organic lettuce, 52.8% conventional lettuce [46] reported that analyzed of 80 lettuce samples, 6.3% were
was found in the range between 4 and 5 log10 CFU/g, positive and 5.2% of analyzed 28 spinach samples were
respectively. The YM mean was 4.7 and 4.2 log10 CFU/g. positive for Salmonella spp. Garcia-Villanova Ruiz et al. [47]
Journal of Food and Nutrition Sciences 2015; 3(4): 152-159 157
at the another study reported that analyzed 46 of 849 production. Farmers should be informed about the sources of
vegetables samples were detected positive Salmonella spp. microbial contamination and should be trained in hygienic
Jerngklinchan and Saitanu [48] reported 8.7% rate of production. It is emphasized that whole fresh vegetables and
Salmonella in bean sprouts. Viswanathan and Kaur [14] fresh fruits should be protected from contamination by
tested of 72 vegetables and 33.3% of the samples were human, animal and other wastes which may constitute a
Salmonella spp. positive; tested of 24 fruits and 37.5% of the hazard to health of the consumer through fresh produces. The
samples were Salmonella spp. detected positive. use of poor microbiological quality of irrigation water should
In the present study E.coli O157:H7 was not detected. be avoided. On the other hand, post-harvest washing of fresh
E.coli O157:H7 presents sporadically at very low levels vegetables and fruits with organic antimicrobial agent and
together with very high levels of competitor organisms that’s use of edible coatings containing antimicrobial is an
why it is very difficult to detect. Salmonella spp. important method for pathogen reduction.Transport vehicles
contamination in lettuces, spinach and carrots may cause by and warehouse should be designed specifically for the
the use of contaminated irrigation water and untreated bovine transport and storage of fruits and vegetables. Also, strict
or ovine originated manure. temperature control from harvesting to consumption by
Arumugaswamy et al. [49] reported of the analyzed 22 farmer, handler, transporter, warehouseman etc. and
lettuce, 5 cucumber, 7 bean sprouts sample, 22.7%, 80%, consumers is highly important.
85% were positive for L.monocytogenes, respectively. Breer
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