Abstract
Fresh fruits and vegetables are great sources of
vitamins and minerals; however, they can be vectors of various parasitic
infections. Therefore, this study aimed at assessing the occurrence and
prevalence of parasitic infections contaminating the fruits and vegetables
obtained from Modern and Tomato markets located in Lafia metropolis, Nasarawa
state, Nigeria. The study design involved a cross-sectional survey. A total
number of 178 fruit and vegetable samples including 72 fruits (apple orange,
tomato, mango) and 106 vegetables (garden egg, spring onion, spinach, water
leaf, carrot) were collected and tested for parasites using standard
parasitology methods. According to the results, about 13.48% of all samples
contained at least one parasitic infection. It should be noted that fruits
contained fewer parasites (5.56%) than vegetables (18.87%). Statistical
analysis showed that there was a significant difference (P = 0.01093) between
contamination rates of fruits and vegetables. Ascaris lumbricoides was identified in 50.00% of fruit samples, Trichuris trichiura occurred in
25.00% of samples, Entamoeba
histolytica and Giardia lamblia
were found in 12.50% of the fruit samples. In the case of vegetables, Ascaris lumbricoides was also the
major type of parasites (59.09%), Strongyloides
stercoralis occurred in 22.73%, while Entamoeba histolytica and Trichuris
trichiura were present in 9.09% of samples. Parasites occurred more
frequently in samples obtained from Modern market (20.00%), than in samples
purchased from Tomato market (6.82%). Furthermore, knowledge, attitude and
practice of fruit and vegetables vendors' (n=40) regarding parasitic
contamination of products revealed that only 62.50% of vendors knew about
parasitic infections in fruits and vegetables, while improper handling
practices (e.g. keeping the produce on the floor) were common. These findings
suggest that there is a significant public health risk due to the consumption
of raw or poorly washed produce. Proper consumer food safety education, improved
hygiene conditions in markets, installation of display stands should be
considered.
Keywords: Public health implication, Fruits,
Vegetables, Parasitic helminths, Markets
1. Introduction
The edible portions of plants that do not include starchy
roots, tubers, cereals, nuts, seeds, medicinal herbs and stimulants are called
fruits and vegetables1. Plants
have very important contributions in the human nutrition because of their
health promoting properties such as supplying essential vitamins, minerals,
dietary fiber, antioxidants, phytoestrogens and anti-inflammatory agents2,3. These natural constituents in plant
foods have proven effective in reducing the likelihood of contracting
non-communicable diseases like cardiovascular diseases, obesity, diabetes and
certain types of cancers4,5. The
recommended daily intake of fruits and vegetables for healthy adults by the WHO
and FAO is 400 grams to prevent diet-related diseases6. The ingestion of contaminated food leads
to various health issues from simple digestive disturbances to serious ones,
such as malnutrition, anemia and mental impairment especially in children,
pregnant females and immune-compromised individuals6.
Food safety is not guaranteed in most low and
middle-income countries, like Nigeria, because of poor sanitary practices in
agriculture as well as at points of sales of fruits and vegetables that
increase their risk of parasitic contamination. Factors such as using
contaminated irrigation water, improper use of animal wastes as fertilizers,
unhygienic harvesting practices, inadequate storage facilities for fresh
produce at points of sales are among the causes for the presence of pathogens
in plants6. Besides increasing
the risk of foodborne disease outbreaks, all these practices facilitate the
spread of parasites like A.
lumbricoides, T. trichiura,
G. lamblia and S. stercoralis.
High levels of parasitic contaminants in fruits and
vegetables offered for sale in the outdoor markets in different urban centers
of Nigeria have been reported in several studies. Lafia city, the capital of
Nasarawa State, is characterized by a high consumption of fresh fruits and
vegetables, mostly in raw form, increasing thus the risk of acquiring diseases
via food. The risk is higher in light of certain factors, for instance, the use
of wastewater as irrigation source, poor hygiene practices among vendors and
poor conditions of fruit and vegetable stalls7.
For this reason, the present study was conducted to investigate the occurrence
and prevalence of parasitic contaminants in fresh fruits and vegetables in two
main markets in Lafia. This study also aims to assess the food safety
knowledge, attitude and practices of the vendors.
2. Materials and Methods
2.1. Study area
Nasarawa State, found within Nigeria’s North-Central
geopolitical axis, falls under the category of Guinea Savannah ecological zone
with geographical location coordinates of 8.4998° N, 8.1997° E7. The climatic condition experienced within
Nasarawa is tropical with an average rainfall. There is variation in topography
with the existence of plains and rolling lands that have elevations ranging
between 300 ft above sea level. The research was conducted in Lafia, the
capital of Nasarawa State. Lafia town serves as the administrative headquarters
of the Lafia local government area. Being the largest urban area in the
Nasarawa State, Lafia is vital in agricultural activities, especially in the
production of major cash crops like yam, cassava and melon (Figure 1).
Figure 1: Map of Nasarawa State and the Location of Sample
Collection (Generated using QGIS version 3.40.1-Bratislava).
2.2. Sample collection
The samples were taken from the two largest markets,
which include Lafia Modern Market and Lafia Tomato Market. A total number of
178 samples, consisting of 72 fruits and 106 vegetables were randomly taken
from various sellers. The fruits involved in this study are orange (Citrus sinensis), tomato (Lycospersicon esculentum), mango (Mangifera indica) and apple (Malus domestica). On the other hand,
the vegetables are garden egg (Brassica
oleracea), spinach (Spinacia
oleracea), spring onion (Allium
spp.), water leaf (Talinum fruticosum)
and carrot (Daucus carota).
These samples were packed in sterile plastic bags that were labeled.
2.3. Sample processing
and parasitological analysis
2.3.1. Sedimentation
technique: The ten grams of the samples were washed
using normal saline 0.9% in order to remove the parasitic stages (ova, larvae,
oocysts and cysts). This was done after which fifteen milliliters of the
washing fluid was transferred into the centrifuge tube using a sieve in order
to remove unwanted particles. The process was done by centrifuging the fluid in
the tube at 3000 rpm for five minutes in order to remove the parasitic stages,
Ishaku et al. and Cheesbrough8,9.
A drop of the supernatant was removed and placed on a slide covered by a
coverslip.
2.3.2. Saturated
sodium chloride flotation technique: According to Cheesbrough9, the samples were rinsed using saturated
sodium chloride before being strained to filter out large debris. They were
thereafter introduced to a tube and allowed to stand in an upright position on
the rack. Additional fluid was added into the tube to make sure that the tube
is completely full. Subsequently, a clean cover glass was placed onto the tube.
It was allowed to stay there for around 30 to 45 minutes so that the eggs/cysts
could float. The cover glass was thereafter taken out from the tube using an
upward pull and placed downward on a slide. It was thereafter analyzed under a
microscope using both 10x and 40x objectives.
2.3.3. KAP survey: The survey questionnaire was
conducted among 40 traders dealing with fruits and vegetables, with an equal
number of participants coming from each of the two markets and who were
randomly selected when collecting the sample. This tool was used to gauge their
awareness on the contamination of their commodities by parasites, attitude
toward hygiene and behaviors.
2.4. Data analysis
Version 2.1.2. of Minitab statistical software was
used for analysis of data. The comparison of prevalence of contamination among
sample types and markets and within various produce items was made by using
descriptive statistics (in percentages) and χ² test. In all cases, probability
p < 0.05 was taken as significant.
3. Results
Overall, of parasites
Contamination of fruits and vegetables in modern Markets and Tomatoes markets.
The finding of this study revealed an overall
prevalence of 24(13.48%) in the both fruits and vegetables sold at the two
major markets of Lafia (Table 1). A comparison between the two selected markets
shows that the Modern Market had a significantly higher proportion of
contaminated produce 18(20.00%) compared to the Lafia Tomato Market 6(6.82%)
(χ² = 6.477, df = 1, P = 0.01093). Furthermore, vegetables were significantly
more contaminated (18.87%) than fruits (5.56%) (Table 1).
Table 1: Contamination of Fruits and Vegetables Collected
from Selected Markets.
|
Market |
No. of fruits examined |
No. contaminated (%) |
No. of vegetables |
No. contaminated (%) |
Total No. Examined |
Total No. contaminated (%) |
|
Modern Market |
36 |
2(5.56) |
54 |
16(29.63) |
90 |
18(20.00) |
|
Tomatoes market |
36 |
2(5.56) |
52 |
4(7.69) |
88 |
6(6.82) |
|
Total |
72 |
4(5.56) |
106 |
20(18.87) |
178 |
24(13.48) |
χ2 = 6.477, df = 1, p = 0.01093.
3.1. Parasitic contamination
in fruits
Amongst the total 72 samples of fruits analyzed, only
4 fruits types (5.56%) were infected with parasitic worms as shown in Table 2
below. Ascaris lumbricoides is
the most frequently isolated (3 or 42.6%) parasite species found on tomatoes. Trichuris trichiura was the second
most commonly identified (2 or 28.56%) parasite species found on oranges. On
the other hand, there was no isolation of Strongyloides stercoralis in all the fruits that were analyzed.
Statistically significant difference (χ² = 6.0, df = 2, P = 0.0498) was found
between these parasite species (Table 2).
Table 2: Prevalence of Parasites in Contaminated Fruits at
Selected Markets in Lafia.
|
Parasites |
Fruit
Type |
Total
(72) |
Prevalence
(%) |
|||
|
Apple
14(%) |
Mango
12(%) |
Orange
18(%) |
Tomatoes
28(%) |
|||
|
Ascaris
lumbricoides |
0(0.00) |
0(0.00) |
0(0.00) |
3
(10.71) |
3 |
42.86 |
|
Entamoeba
histolytica |
0(0.00) |
0(0.00) |
0(0.00) |
1
(3.57) |
1 |
14.29 |
|
Giardia
lamblia |
0(0.00) |
1
(8.33) |
0(0.00) |
0(0.00) |
1 |
14.29 |
|
Strongyloides
stercoralis |
0(0.00) |
0(0.00) |
0(0.00) |
0(0.00) |
0 |
0.00 |
|
Trichuris
trichiura |
0(0.00) |
0(0.00) |
1
(100) |
1
(3.57) |
2 |
28.56 |
|
Total
(%) |
0(0.00) |
1(8.33) |
1
(5.56) |
5
(17.86) |
7 |
100.00 |
χ2 = 53.053, df = 4, P<0.001
3.2. Parasitic contamination
in vegetables
The prevalence of parasites among all 106 samples
tested was 22(20.75%). Ascaris
lumbricoides was the leading parasite detected, as seen in 13(59.09% of
all contaminated vegetables), mainly in the samples from Spring onion
10(50.00%), followed by 3(18.75%) samples from Spinach. The second most common
parasite was Strongyloides stercoralis,
at 5(22.73%), occurring in Carrot, Spinach and Water leaf. Entamoeba histolytica and Trichuris trichiura each occurred in
2 (9.09%) samples from Vegetables. Giardia
lamblia was absent in all vegetable samples. There was difference in the
prevalence of parasite species among vegetables in Lafia markets (ꭓ2 =
108.68, df = 4, p < 0.001) (Table 2).
Table 3: Prevalence of Parasites in Contaminated Vegetables
at Selected Markets in Lafia.
|
Parasites |
Vegetable Type |
Total 106 |
Prevalence (%) |
||||
|
Carrot 28(%) |
Garden Egg 26(%) |
Spinach 16(%) |
Spring Onion 20(%) |
Water 16Leaf (%) |
|||
|
Ascaris lumbricoides |
0(0.00) |
0(0.00) |
3(18.75) |
10(50.00) |
0(0.00) |
13 |
59.09 |
|
Entamoeba histolytica |
0(0.00) |
0(0.00) |
2(12.5) |
0(0.00) |
0(0.00) |
2 |
9.09 |
|
Giardia lamblia |
0(0.00) |
0(0.00) |
0(0.00) |
0(0.00) |
0(0.00) |
0 |
0.00 |
|
Strongyloides stercoralis |
1(3.57) |
0(0.00) |
2(12.5) |
0(0.00) |
2(12.50) |
5 |
22.73 |
|
Trichuris trichiura |
1(3.57) |
0(0.00) |
0(0.00) |
1(0.50) |
0(0.00) |
2 |
9.09 |
|
Total (%) |
2(7.14) |
0(0.00) |
7(43.75) |
11(55.00) |
2(12,50) |
22 |
100.00 |
χ2=108.68,
df = 4, P<0.001
3.3. Hygiene conditions
of produce display
From
observation of the method used by vendors in displaying the fruits and
vegetables sold by them, a clear contrast existed. Most of the fruit sellers
(67.007%) used tables to display their products, which is fairly hygienic (Figure
2). However, most of the vegetable sellers (44.44%) used the ground as
their surface, leaving them at risk of contamination with dirt, followed by
those that used Wheelbarrows (22.22%), then Rubbers (19%) while only 15%
contaminants were found on vegetables displayed on Table (Figure 3).
Figure 2: Hygiene Conditions under which the Fruits are
displayed.
Figure 3: Hygiene Conditions under which the Vegetables are
displayed.
3.4. Knowledge, attitude
and practices (KAP) of vendors
However, it was found through the KAP survey that
there are large areas of ignorance when it comes to food safety issues. The
majority of the participants in the study, out of the total 40 people, did not
know that the produce can cause parasitic infections. This was found to be
statistically significant (χ² = 6.25, P = 0.01242). The vendors obtained the
produce from places such as Jos, Plateau state, which is 70 percent of the
time, while only 30 percent obtain it from Lafia (Table 4).
Table 4: Knowledge, Attitude and Practice of Vendors on the
Contamination of Fruits and Vegetables.
|
Question |
Response |
Frequency |
Proportion |
χ2 |
df |
P value |
|
Are you aware of
parasitic contamination of fruits and vegetables |
Yes |
15 |
37.50 |
6.25 |
1 |
0.01242 |
|
No |
25 |
62.50 |
|
|
|
|
|
Total |
|
40 |
100.00 |
|
|
|
|
Where do you source
for your fruits and vegetables |
Jos |
28 |
70.00 |
16 |
1 |
P<0.001 |
|
Lafia |
12 |
30.00 |
|
|
|
|
|
Total |
|
40 |
100.00 |
|
|
|
|
Which water source do
you use to wash your fruits and vegetables |
Borehole |
24 |
60.00 |
50.375 |
2 |
P<0.001 |
|
Tap Water |
15 |
37.50 |
|
|
|
|
|
Well water |
1 |
2.50 |
|
|
|
|
|
Total |
|
40 |
100.00 |
|
|
|
4. Discussion
The results from the current investigation
demonstrated that the fresh fruits and vegetables sold in Lafia markets are
contaminated with parasites that are of public health importance, with an
overall parasitic contamination of 13.48%. This rate is lower when compared to
the findings from Abuja market (33.3%), as reported by Moshood10, yet much higher than in Ibadan market
(5%) as reported by Obebe, et al.6.
Indeed, the current findings reflect the reality of the challenges associated
with food safety in developing countries due to the poor post-harvest handling
practices and environmental conditions in the markets6,7,11. Parasites including Ascaris lumbricoides, Strongyloides stercoralis, Trichuris trichiura, Entamoeba histolytica and Giardia lamblia suggest that there is
a lot of faecal pollution of the environment caused by the usage of
contaminated water for irrigation/ washing and poor handling of the produce.
It is also apparent that there is a statistically
significant difference in the prevalence of parasitic contamination of fruits
and vegetables (18.87% vs. 5.56%), which is consistent with previously reported
research studies8,12. It can be
explained by morphologic and physiological features of fruits and vegetables,
as well as different handling procedures. Specifically, vegetables like spinach
and spring onions show very high rates of contamination and this might be
attributed to their large and rough surface area that facilitates the
accumulation of parasites. Moreover, they remain in prolonged contact with the
soil while growing up, as well as with the ground when being exposed at the
vendor stands13,14. This view is
supported by a similar study by Abubakar, et al.9,
who observed a high prevalence of vegetable contamination in Keffi markets
(Nasarawa State). Fruits, on the other hand, were demonstrated to have rather
smooth surfaces and were mostly displayed on the table.
Ascaris lumbricoides
was the parasite that had been isolated the most frequently from the samples
collected during this study. The reason for this can be related to the fact
that Ascaris lumbricoides is
the most commonly found soil-transmitted helminth in Nigeria and most of
tropical countries. Several reasons for its high prevalence include daily
discharge of millions of eggs by infected people, high egg resistance to
environmental conditions, as well as easy dissemination through soil15. The findings concerning the second-most
common parasite, Strongyloides
stercoralis, should be highlighted too because larvae of this species
can penetrate the skin6.
Statistically significant differences in parasitic
contamination of fruits and vegetables in the two investigated markets (Modern
Market and Lafia Tomato Market) were also observed. In particular, the
prevalence of contamination in the former was significantly higher (20.00% vs.
6.82%). Such findings can be linked to the market size and the amount of waste
produced in such markets. The higher the number of vendors and customers is,
the greater amount of waste is accumulated within a shorter period and this, in
turn, makes the contamination more probable.
The results obtained from the KAP survey help to
explain the parasitological findings. First, a high percentage (62.5%) of
respondents was not aware about the risk of parasitic infections. In fact, in
this case, they cannot apply preventive measures. Second, the habit of laying
the vegetables on the ground is one of the key sources of contamination with
soil-transmitted helminths, such as Ascaris
or Trichuris. Third, it can be
stated that, despite the fact that 60% of respondents use borehole water, the
remaining 40% use the tap well water, which increases the risk of
re-contamination of the produce after washing. Finally, it can be mentioned
that the majority of produce comes from the town of Jos, which means that
contamination is likely to occur on the farm. Thus, it is crucial to follow
GAPs.
The overall parasitic contamination of fresh fruits
and vegetables (13.48%) in Lafia markets is lower than that in some other
cities in Nigeria, for instance, in Abuja (33.3%)10
and Keffi (53.5%)7. On the contrary,
in Ibadan the percentage of parasitic contamination was lower (5%)6. It is hard to say whether the discrepancy
in the contamination level is real or methodical. However, regardless of this,
the presence of the mentioned pathogenic parasites on produce consumed by the
public is dangerous for people's health1,16.
5. Conclusion
The current study reveals that fruits and vegetables
consumed from markets within Lafia are contaminated by parasitic organisms of
medical importance such as Ascaris
lumbricoides, Strongyloides
stercoralis and Trichuris
trichiura. This observation can be attributed to poor sanitation of the
markets, as indicated by the higher level of contamination at the Modern
Market. In addition, the common practice of displaying vegetables on the ground
indicates that vegetables can be easily contaminated. Moreover, most vendors
lack the knowledge concerning the possibility of fruits and vegetables to act
as vectors of disease. Based on these observations, an urgent action is
required in order to combat this problem. Firstly, public health agencies
should initiate food safety education campaigns aimed at raising the knowledge
of vendors concerning the role of food hygiene in the spread of disease.
Secondly, the market managers should improve their sanitation facilities
through providing display tables and adequate amounts of clean water.
6. References
3. https://www.fao.org/3/cb2395en/cb2395en.pdf
7. https://hummingbirdjournals.com/jaesr/article/view/168
13.
Adamu NB, Adamu JY,
Mohammed D. Prevalence of helminth parasites found on vegetables sold in
Maiduguri, Northeastern Nigeria. Food
control, 2012;25(1):
23-26.