2023.08.04.18
Files > Volume 8 > Vol 8 no 4 2023

Assessment
of the microbiological quality and heavy metal risk in vegetable species
marketed in outdoor fairs

1 Universidad
Politécnica Salesiana, Carrera de Ingeniería en Biotecnología de los Recursos
Naturales, Sede Quito, Campus El Girón, Grupo de Investigación y Desarrollo en
Ciencias Aplicadas a los Recursos Biológicos, Av. 12 de octubre N2422 y Wilson,
Quito, 170109, Ecuador; [email protected].
2 Universidad
Politécnica Salesiana, Carrera de Ingeniería en Biotecnología de los Recursos
Naturales, Grupo de Investigación en Biotecnología Aplicada a los Recursos Naturales,
Av. 12 de octubre N2422 y Wilson, Quito, 170109, Ecuador;
[email protected], [email protected].
* Correspondence: e[email protected]; Tel.:+593(995129321)
(Quito, Ecuador)
Available from. http://dx.doi.org/10.21931/RB/2023.08.04.18
ABSTRACT
The
objective of this study was to evaluate the possible health risks associated
with the content of heavy metals and microorganisms in the consumption of
watercress, lettuce, lemon balm and taraxaco. The products were purchased in
several markets in the city of Quito. In this study, the products marketed in
the north and center of the town showed better size characteristics, while the
soluble solids, pH and ash showed no definite behavior. In addition, due to the
volcanic origin of the Ecuadorian soils in which the samples under study were
grown, it could influence the lead content that varied between 0.02 ppm
(taraxacum, lemon balm and lettuce) up to 2.60 ppm (watercress). This value
exceeded the maximum limit allowed by the CODEX, becoming a health risk. In
addition, the microbial quality of the different species under study showed
high contamination with mesophilic aerobic microorganisms and parasites. These
results provide valuable information that could finance food safety decisions
by the government to protect health and improve the quality of life of the
people of Quito.
Keywords:
food
safety, mesophilic aerobic, parasites, lead, Cadmium
INTRODUCTION
Vegetables
are critical dietary components because they provide essential nutrients, such
as vitamins, minerals and fibers, and many health benefits. Food safety has
been affected since most vegetables absorb contaminants in the soil and
accumulate in different foliar tissues or cell walls
1. The risk of microbiological contamination on leafy greens is concerning.
In the United States (US) in 2009,
leafy greens were identified at the top of the 10 riskiest foods regulated by
the Food and Drug Administration (FDA) 2, with 22% of foodborne illnesses associated with
leafy greens consumption 3, and involved with significant economic losses.
Fresh vegetables
and fruits can be contaminated with pathogenic bacteria and heavy metals.
During pre-harvest, contact with contaminated irrigation water, soil, fecal
matter of wild animals, and communication with asymptomatic human carriers can
contaminate the products. At the postharvest level, the products are
contaminated by contact with contaminated water, other asymptomatic human
carriers, or the production process and distribution environment 4.
To explain how microorganisms of
concern are transmitted across the food chain, we studied risk factors
contributing to microbial contamination of vegetables eaten raw in markets.
Edible and medicinal plant species can be obtained at fairs or wholesale markets,
selling products shown not to have microbiological and bromatological controls.
In general, in products that are consumed fresh, it has been found that there
is the possibility of more significant contamination of microorganisms that
could cause certain diseases in humans 5.
The food pattern in Ecuador is linked
to individual economic access, religion, and ancestral and current culture. 6, means of surveys indicate that a person in Ecuador consumes around 183
g/day between fruits and vegetables. Nevertheless, the population in these last
years has been linked to their nutritional pattern in health care; this is why,
according to the FAO, in 2016, there were 28307 tons of vegetables, a figure
that has been increasing since several years ago, indicating that the
consumption of vegetables has spread and therefore the market offering.
Watercress (Nasturtium officinale R. Br.) is one of
the most consumed vegetables in Ecuador. It has been used since ancient times
as traditional medicine to calm respiratory problems and skin diseases.
According to 7,
a watercress is a plant belonging to the cruciferous family that can grow
spontaneously near almost all water courses; it will always require an
acceptable flood level in fresh water. The watercress contains sodium,
potassium, calcium, iron, sulfur, fiber, pro-vitamin A and vitamin C 8.
On the other hand, it has been determined that the leaves and stems of the
watercress may contain small slugs that, in turn, host parasites such as
Fasciola hepatica.
The lettuce (Lactuca sativa L.) is another more
frequently consumed vegetable. This provides a high content of carotenoids,
vitamin C, minerals, fiber, and water. It also provides an alkaline reaction to
the human body, accompanied by a high cellulose content and good-quality
proteins 9.
The most common diseases in cabbage lettuce are derived from inadequate
handling in the postharvest and poor control of the optimum temperature in all
the production processes. According to 10,
among the microorganisms that may be present are bacteria (Coliforms, Pseudomonas spp. and Erwinia, Escherichia coli), parasites (Entamoeba histolytica, Giardia spp.), viruses (Norwalk,
hepatitis A) and fungi (Botrytis, Fusarium) that form products that cause
diseases in the human being.
Lemon balm (Melissa officinalis L.) and taraxaco (Taraxacum officinale F.H. Wigg.) grow
exposed to highly interacting microorganisms that are in symbiosis or cause
physiological alterations. The genera that are most interacting with these
species are Agrobacterium spp.,
Clavibacter spp., Erwinia spp., Pseudomonas spp., Xanthomonas spp.,
Streptomyces spp., Xylella spp., and those that infect them through
cross-contamination are: Clostridium botulinum, Staphylococcus aureus, Bacillus
cereus and the family Enterobacteriaceae. Lemon balm and taraxaco are
cultivated in the Ecuadorian inter-Andean region, which has the presence of
heavy metals of a geographical nature. In addition, the recurrent agricultural
activity increases the presence of metals due to using fertilizers, pesticides,
manure, slurry and sewage sludge 11.
All the plant species
already mentioned are part of a food and medicinal culture available to
everyone. For this reason, the objective of this study was to evaluate the
possible health risks associated with the content of heavy metals and
microorganisms in the consumption of watercress, lettuce, lemon balm and
taraxaco in the markets of the Metropolitan District of Quito to raise
awareness of the quality and safety of these products that form a basis in
Ecuadorian food.
MATERIALS
AND METHODS
Reagents and Standards
Reagents
of analytical grade as nitric acid (PumChem CID: 944), sulfuric acid (PumChem
CID: 1118), sodium hydroxide (PumChem CID: 14798) and sodium chloride were
obtained from Panreac (Barcelona, Spain). Cadmium, lead standards, cadmium
standard and violet crystal were purchased from Merck (Labomersa S. A.,
Ecuador). Peptone was obtained from BD. (Biosciences, United States).
Plant Materials
The
watercress (Nasturtium officinale R.
Br.), lettuce (Lactuca sativa L.), lemon balm (Melissa
officinalis L.) and taraxaco (Taraxacum
officinale (L.) Weber ex F.H. Wigg) were purchased from an average of
thirty markets of the zonal distributions of the Metropolitan District of Quito
(Figure 1). The leaves were considered a sample unit, and a whole head of
lettuce was regarded as one sample. Approximately 1 Kg of each species was
purchased randomly from four retail sites within each market. The amount of
samples was selected as described by the INEN-1750
12. After
sampling, all samples were placed in sterile zipped bags and immediately stored
in cooling boxes with ice packs. The refrigerated samples were taken to the
Life Sciences laboratories of the Salesiana Polytechnic University
(Girón-Quito). The transit time was 1 to 3 hours. The market samples were
analyzed within 24 hours or immediately upon reaching the laboratory.

Figure 1. Location
of markets in the Metropolitan District of Quito-Ecuador. S An, San Antonio; Pom, Pomasqui; Cal, Calderón; Cara,
Carapungo; Cot, Cotocollao; Ken, La Kennedy; Ame, La América; S Cl, Santa
Clara; Iña, Iñaquito; Cen, Centro; Qui, Quinche; L Gr, Llano Grande; Com,
Comité del Pueblo; Pue, Puembo; Yar, Yaruquí; Cum, Cumbayá; Tum, Tumbaco; S Ro,
San Roque; Mag, La Magdalena; S Ba, San Bartolo; Sol, Solanda; Chi, Chiriacu;
May, Mayorista; Ecu, La Ecuatoriana; El Ca, El Canal; Ci Ib, Ciudadela Ibarra;
Gua, Guamaní; Con, Conocoto; Ala, Alangasí; Ama, Amaguaña
Measurements Performed on Foods
The
bromatological analyses performed on the fresh watercress (Nasturtium officinale R. Br.), lettuce (Lactuca sativa L.), lemon balm (Melissa
officinalis L.) and taraxacum (Taraxacum
officinale (L.) Weber ex F.H. Wigg) were size (equatorial and longitudinal
diameter in cm,
weight in g, humidity in %, ash in %, soluble solids in °Brix, titrable acidity
in % and pH. The soluble solids were quantified as described by INEN-ISO-2172 13, with a Hand-Refractometer RHC-200ATC (Huake, China), while a S40
SevenMulti pHmeter (Mettler Toledo, Belgium) was used to measure out the pH.
Titulable acidity and relative density were determined as described by INEN-ISO-750 14 and INEN-391 15. A
humidifier HB4 3-S Halogen (Mettler Toledo, Belgium) was used to measure the
humidity and dry material, while the ash was measured as described by 16.
Heavy Metal Analysis
Sample preparation
The
samples were dried at 70 ºC for 24 hours in a KBF 240 air recirculation oven
(Binder, Germany). The dried samples were ground in a primary IKA 11 mill,
stored in a glass bottle and hermetically sealed. The sample was treated as
described by AOAC-999.10 17, with modifications. Approximately 250 mg of the pulverized sample was
mixed in a Teflon digester with 1.5 mL of concentrated nitric acid and 1.5 mL
of sulfuric acid. The mixture was digested in a Speedwave HB43-S Digestion
(Berghof, Germany) for 40 min according to the specifications of the equipment
manual. The digested mixture was graduated in 25 mL with deionized water.
Atomic absorption
The
calibration curve was built on the same day with concentrations of lead and
cadmium standards separately from 0.5, 1.0, 2.0 and 4.0 ppm.
Quantification was performed on a SpectrAA-55 Atomic Absorption
Spectrophotometer (Varian-Agilent Technologies, United States), as described by
AOAC-999.10 17. The
lead was quantified at 217.0 nm and the Cadmium at 228.8 nm. All the digested
mixture was read three times, and the concentration was expressed in mg/kg dry
weight (DW).
Microbiological and Parasitological
Analysis
The most
widely accepted and used techniques are those recommended by WHO for a total
count of microorganisms in plant materials. According to the methodology of the
WHO, 10 g of fresh sample was suspended in 90 mL of sodium chloride-peptone
buffer at a pH of 7.0. A fresh sample was plated in duplicate to count total aerobic
bacteria and incubated at 30-35 ºC for 48 h 18.
For the
parasitological analysis, dilutions 10-1 were made with the plant
extract and sterile water, centrifuged at 3000 rpm for 5 min, and the pellet
formed was removed and placed in an Eppendorf tube. After this, a slide with
0.2 µL of sample and 0.2 µL of violet crystal was placed in an optical
microscope, and the presence of parasites or cysts was observed.
Statistical analysis
Statistical
differences were determined by analysis of variance (simple ANOVA). The mean
separation was made via a Tukeyʼs test with 0.01 significant differences, and
correlations by Pearson with a 99 % confidence level were employed to estimate
the possible significance of the samples. Moreover, Principal Components
Analysis (PCA) was applied to select the variables most influencing the
differences between samples. The INFOSTAT 2009 software was used for
statistical analyses.
RESULTS
In Tables 1 to 4 found
Physicochemical properties, microbiological results, and heavy metals.

Table 1. Average value (FW) of parameters
related to the commercial quality of taraxacum (T. officinale) a

Table 2. Average value (FW) of parameters
related to the commercial quality of lemon balm (M. officinale) a

Table 3. Average value (FW) of parameters
related to the commercial quality of watercress (N. officinale) a

Table. Average value (FW) of parameters related to the commercial quality of lettuce (L. sativa) a 4
DISCUSSION
Estimation
of food quality
Size
The selected markets
correspond to 55.5 % of the total in the Metropolitan District of Quito. The
markets that presented the highest values of equatorial and longitudinal
diameter were Santa Clara and Llano Grande for lemon balm, San Roque for
taraxaco and Llano Grande for lettuce and watercress (Table 1 to 4). Thus, in
most cases, the markets located to the north of the city showed enormous sizes;
this may be because these markets are provided with products from the Pichincha
province, while the markets of the center and south are supplied with products
from the Cotopaxi province, marking the difference in said products. The
average longitudinal diameter of lemon balm was 5.3 cm, less than reported by 19,
which showed values of longitudinal diameter of 9 cm and equatorial diameter of
7 cm. On the other hand, the statistical differences shown by the analyzed
samples of lemon balm indicate that at least one market has different diameters
than the others, agreeing with that reported by other authors that suggest that
it is sold in the markets regardless of the size of the leaf, causing maximum
use of the therapeutic properties presented by the species the other hand, the
longitudinal diameter (13.43 cm) and the equatorial diameter (4.97 cm) of the
watercress showed values similar to those reported by other authors who
indicated a length of 15 to 20 cm.
Weight
The markets that
presented the highest weights of the samples under study were San Roque for
taraxaco, San Bartolo for lemon balm, Llano Grande for watercress and San
Antonio de Pichincha for lettuce (Table 1 to 4). On the other hand, the markets
that presented the highest dry matter values were Cumbayá for taraxaco,
Carcelén for lemon balm, El Calzado for watercress and Alangasí for lettuce.
About the previous data, the weight values showed a relationship with the data
obtained from dry matter. Thus, the markets located to the south of the city
presented higher values of humidity and low weights; this again could be due to
the place of origin of the samples since most of the products that reach the
wholesale market located south of the city can be from the province of
Cotopaxi.
The distribution of dry
matter was lemon balm (14.3 %), taraxacum (12.8 %), watercress (7.2 %) and
lettuce (5.8 %). The dry matter values of the watercress were similar to those
reported by other authors, which showed 94.6 % humidity 20,21.
The markets with the
highest ash values were Tumbaco Centro for Taraxaco, La Ecuatoriana and Solanda
for lemon balm, San Antonio de Pichincha for watercress and San Roque for
lettuce. Thus, in most cases for taraxaco and lemon balm, the ash values
exceeded that established by the Ecuadorian Technical Norm of ash of 2 % 22.
This was also observed in the simple of cress obtained from San Antonio de
Pichincha, who reported values of 2.08 %. The ash values of lemon balm,
taraxaco and watercress showed significant differences in the place of sales,
while the lettuce did not present differences.
Soluble solid (SS.)
The markets that
presented higher values of SS were the Comité del Pueblo and San Bartolo for
watercress, Carapungo and San Antonio de Pichincha for lettuce (Table 1 to 4).
In addition, the average values for SS classified from highest to lowest for
the samples under study were watercress (3.78 ºBrix), lettuce (3.41 ºBrix),
taraxaco and lemon balm (2.20 ºBrix). All samples analyzed except taraxaco and
lemon balm did not show significant differences when considering all the
markets under study.
On the other hand, the
markets that presented the highest pH values were La Ecuatoriana for taraxaco,
Iñaquito for lemon balm, and America for watercress and lettuce. In addition,
the average values from highest to lowest for pH were lemon balm (6.83), watercress
(6.68), lettuce (6.56), taraxaco (6.40). These values are similar to those
reported by other authors 7.
Concerning the statistical analysis of the pH, considering all the markets in
the study, these showed significant differences, except the lettuce, which did
not differ.
Heavy metal analysis
Lead
The markets with the
highest values of Pb were San Bartolo for taraxaco, Alangasí for lemon balm,
Cumbayá for watercress and several markets in the case of lettuce (Table 1 to
4). These data indicate that no specific region accumulates heavy metals; this
may be due to the fact that the soils of the Sierra region are volcanic and
have high amounts of heavy metals.
The taraxaco, lemon and
lettuce balm showed average values of 0.02 ppm in most cases and 1.90 ppm for
watercress. Thus, at least one market showed statistical differences concerning
the values reported for the remaining markets under study. The concentrations
of Pb for lemon balm, taraxaco and lettuce are within the limits accepted by
the Ecuadorian Technical Standard that reports maximum values of 0.5 ppm 22 and 0.3 ppm established by CODEX and the
European Union Regulations for heavy metals 23.
However, the values of watercress exceed the maximum limits, becoming a health
risk since lead can replace calcium accumulating in bone tissues, as suggested
by other authors 24.
Although taraxaco is
considered a bioindicator of environmental contamination, as suggested by other
authors 25,
it has a low concentration compared to the rest of the samples under study.
Cadmium
Lemon balm and taraxaco
showed a Cd value of 0.01 ppm for the studied markets. Therefore, all the needs
under study did not show significant differences in the values reported. In the
case of watercress and lettuce, these showed concentrations of 0.05 and 0.02
ppm, respectively, in most of the different markets under study, and these
values corresponded to the maximum concentration. Cadmium, in general, should
be absent in plant tissues; however, its presence may be related to the type of
soil in which it is grown, which corresponds to the inter-Andean region whose
areas show the presence of heavy metals of a geographical nature from the
Cordillera of the Andes, as suggested by other authors 26.
On the other hand, according to the limits established by the FAO (4.2 ppm),
the CODEX and the European Union Regulation for heavy metals 23 with reference limits of 0.2 ppm, the results
obtained for the samples under study did not exceed the permissible limit.
PCA analysis for food
quality
Applied to our data set,
PCA revealed that the first principal components explain 29.6 % of lettuce,
33.1 % of lemon balm, 37.06 % of watercress, and 44.0 % of taraxaco of total
variance. A plot of the scores of the first factor (PC1) versus the second
principal component (PC2), i.e., the projection of the samples along the
directions identified by the first two PCs, is reported in Figure 2. PC1 was
mainly linked to lead in most of the samples under study, all with positive
loading values in this component.

Figure
2. Scores plot of the watercress (N. officinale) (A), lemon balm (M.
officinalis) (B), lettuce (L. sativa)
(C) and taraxaco (T. officinale) (D)
using the two first principal components obtained by PCA of weight, dry
material, ash, lead, Cadmium, pH, soluble solids and titulable acidity.
Microbiological quality
Mesophilic
Aerobic Microorganisms
The average of
mesophilic aerobic microorganisms in all samples exceeded the values of 4 log10
CFU/g (1x104 CFU/g (Table 1 to 4). The results of lettuce were
similar to the study of 2,
who reported ranged from a geometric mean of 3.50 to 8.39 log CFU/g in lettuce,
parsley and radish; 27
found values of >6 log CFU/g in environmentally friendly romaine lettuce,
and 28
presented ranges between 5 to >7 log10 CFU/g for organic vegetables and 3 to
>7 log10 CFU/g for conventional vegetables, including ʽLooseleafʼ,
ʽButterheadʼ, ʽRomaineʼ and ʽRed looseleafʼ lettuce.
The high load of
microorganisms could be due to the contamination between the transports of
vegetables from the farm to the market. This possible contamination was also reported
by 29
who observed that the counts of indicator microorganisms increased from farm to
market, for example, mean Enterobacteriaceae and Listeria spp. Counts were on average higher by 0.9 log CFU/g and by
0.5 log CFU/g respectively at market compared to farm, indicating that between
farm and market, vegetables are either contaminated or that there are
conditions that allow the growth of microorganisms.
On the other hand, the
pH values for taraxaco, lemon balm, watercress and lettuce were 6.4, 6.8, 6.7
and 6.5, respectively. The pH values found could explain the high microbial
quantity in the different species, as indicated 30,
who points out that the bacteria count may be low when pH is low (presence of
acidic substances). However, at neutral or higher pH (5 to 8.5), the level of
contamination of the herbal preparations may be higher.
Parasites
The present study
evaluated the presence or absence of eggs and cysts of parasites in the
different species. Thus, the watercress and lettuce showed the highest
identification of parasites eggs or cysts, followed by lemon balm and taraxaco
(Table 1 to 4). Some authors suggest that the watercress structure favors the
level of contamination due to the multiple and separated leaves, which allows a
greater adherence of parasites 31.
In addition, this type of plant is developed in highly humid soil and mainly
inaccessible areas that probably carry contaminated water, as suggested 32.
On the other hand, the lettuce has broad leaves, firmly juxtaposed, which
hinders the adhesion of protozoan cysts, eggs and helminth larvae; another
hypothesis is that many helminth eggs can survive for more extended periods in
the environment, which could justify the higher frequencies of parasites found
in the watercress, whose cultivation requires land permanently humid, as
proposed others authors 32.
Also, fascioliasis risk is linked with the consumption of raw vegetables such
as lettuce, suggesting contamination when washing vegetables with untreated
water and in-plant cultures using natural water for irrigation, as indicated 33.
PCA analysis for microbiological quality
The number of
microorganisms for taraxacum and lemon balm according to PCA statistical
analyses (Figure 3) is influenced highly by pH, with values of 0.56 and 0.42
for the first principal component, respectively, what means that at basic or
neutral pH value, the growth of aerobic mesophilic microorganisms is more
significant than an acid pH values. Also, the percentage of ash influences the
number of mesophilic aerobic organisms in the case of taraxaco, lettuce and
watercress, with values of 0.64 and 0.28 for the first principal component,
respectively.

Figure 3. Scores plot of the
watercress (N. officinale) (A), lettuce (L.
sativa) (B), taraxacum (T. officinale)
(C) and lemon balm (M. Officinalis) (D) using the two first principal components
obtained by PCA of weight, dry material, ash, pH, soluble solids, titrable
acidity, mesophiles and parasites
CONCLUSIONS
The present study
supports the idea that lemon balm, taraxaco, watercress and lettuce meet the
bromatological, microbiological and heavy metals requirements in the Distrito
Metropolitano de Quito markets. In general, the size of the products under
study showed better characteristics for needs in the north and center of the
city. At the same time, heavy metals did not exceed the limits allowed by
Ecuadorian regulations such as CODEX and European regulations (0.3 ppm for Pb
and 0.2 ppm for Cd).
On the other hand,
according to our microbiological results, it is suggested that the species
studied have lower quality hygiene (outside acceptable microbiological limits).
The study results show that 76 to 100% of the samples commercialized in markets
from Quito were contaminated with at least one parasite structure on overage.
Therefore, improvement is needed in sanitary conditions during the planting and
distribution of vegetables to reduce the contamination and the risks to food
safety to humans. Vegetables likely to be eaten raw should not be obtained from
areas where these practices are known, or suspected, to be unhygienic.
Author Contributions: methodology, Coyago
Elena, Méndez Gabriela; formal analysis, Acurio Daniel.; investigation, Coyago
Elena.; resources, Coyago Elena.; writing—original draft preparation, Méndez Gabriela, Coyago Elena, Acurio Daniel;
writing—review and editing, Coyago Elena, Acurio Daniel, Méndez Gabriela;
project administration, Coyago Elena.; funding acquisition, Coyago Elena. All
authors have read and agreed to the published version of the manuscript.
Funding: "This research
received no external funding."
Conflicts of Interest: "The authors
declare no conflict of interest."
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Received: 28 September 2023/ Accepted: 15 November
2023 / Published:15 December 2023
Citation:
Coyago-Cruz
E, Méndez G , Acurio D. Assessment of the microbiological quality and heavy metal risk in
vegetable species marketed in outdoor fairs. Revis Bionatura 2023;8 (4) 18. http://dx.doi.org/10.21931/RB/2023.08.03.18