Good food hygiene and safety practices help prevent the risk of food-borne illnesses, which can have a serious impact on public health. Street foods are an essential source of nutrition and employment in developing countries, but the absence of adequate standards can lead to the spread of bacteria, viruses and toxins
[1]
.
Street food plays an important role in the life of the urban population. The sale of street food in developing countries like Niger can lead to a number of health problems. Food that is unfit for consumption is a global health threat, putting everyone at risk. Infants, young children and pregnant women are particularly vulnerable
[2]
.
“Fura” is a cereal dumpling made from millet flour mixed with spices. “Nono” is a dairy product obtained by fermenting animal milk (cow, small ruminant). It is a traditional food in many West African countries, including Niger, Nigeria, Ghana, Cameroon and Burkina-Faso
[3]
.
The “fura da nono” blend is a two-in-one product of a cereal (millet), “fura” made from millet and “nono”, a fermented dairy product. “Fura” is generally prepared by mixing the dry flour ingredients (millet and spices together), then adding a little water to bind the dry ingredients. It is then ground into medium-sized balls, and when the water begins to boil, the molded balls are plunged into the water and left to boil for around 20 minutes, then transferred to a mortar and pounded. They are then stirred into small balls by hand. The “fura” is served by placing it in a calabash or bowl, then adding the “fura” to the “nono”, stirring and adding sugar according to the consumer’s taste. This food combination is called “fura da nono”.
The manual labor involved in local “Fura” production, particularly hand-molding, can be a source of contamination, which can lead to food poisoning or toxi-infection. These foods are generally prepared and sold in deplorably unhygienic conditions.
National food control systems play a fundamental role in protecting consumer health and ensuring fair practices in the food trade
[4]
. The public therefore has the right to expect that the food they consume is safe and fit for consumption. Like other countries around the world, Niger is committed to implementing the “National Food Safety Plan for Niger” approach to achieving Sustainable Development Goal (SDG) 2 of ensuring food security. According to the World Health Organization (WHO), every year almost one person in ten worldwide (i.e. nearly 600 million people) falls ill, and 410,000 of them die as a result of eating food contaminated by bacteria, viruses, parasites or chemical substances
[2]
.
In order to protect this population, it is necessary to inspect and analyze street foods, which meet a vital need for the population. It is therefore important to identify the consequences of poor hygiene management among street food sellers.
The aim of the present work is to analyze the hygienic and microbiological quality of ready-to-eat “fura da nono” (dumpled cereal and milk) sold at the Dolé market in Zinder (Niger).
2. Materials and Methods2.1. Study Area
Zinder’s large market, called “Kassua’n Dolé”, whose name “Dolé” means “obligatory” in Hausa, offers a real multitude of interests that go beyond the mere need to buy goods. It contributes both to the modernization of the town through its architectural character and to the economic development of the region. Zinder’s large “Dolé” market is located to the south of the health center “CSI Dispensaire” and to the north of the Sabon gari district. The Zinder Dolé market is a recently renovated infrastructure; it was modernized 6 years ago but the official opening took place on September 20, 2018. It is an infrastructure with a capacity of 8.6 hectares, 2152 stores, including 2136 medium-capacity stores with a surface area of 9 m2 and 16 large-capacity stores with a surface area of 63 m2, medium shed spaces, 539 floor spaces with 16 toilets, 8 mosques and 8 parking lots. The market boasts several “fura da nono” sellers, 18 of whom are permanent as shown in
Figure 1
.
Figure 1. Location map of the Zinder Dolé market.
2.2. Data Collection Techniques
The population of our study consisted mainly of permanent sellers of “fura da nono” from the Dolé market in Zinder and the person in charge of the hygiene and sanitation department of the health district of the city of Zinder. The study lasted six (6) months, from November 2023 to May 2024.
An exhaustive sampling of stationary sellers of “fura da nono” from the Zinder Dolé market was carried out. “Fura da nono” was collected from eighteen 18 permanent vendors, and a single sample was taken from each of these outlets for a total of eighteen 18 samples.
All eighteen permanent “fura da nono” sellers located inside the Zinder Dolé market are included in this study, while those located in the vicinity of the Zinder Dolé market are not.
2.3. “fura da nono” Sampling
Samples are taken from 1 p.m. onwards, the time at which saleswomen arrive at the points of sale. Three to four samples were taken and analyzed per day. Once there, the fura balls are placed in a calabash or bowl, and some volume of nono and water is added before mixing.
This mixture is then aseptically removed using the same ladle that was used to introduce it into the sterile bottle. Once the sample has been labelled (sample number, time and date of collection), it is placed in the cooler (temperature between 4˚C and 10˚C) and sent as quickly as possible to the laboratory for analysis. The pH of the samples was measured using a Palintest pH meter. The pH meter electrode is immersed in the “fura da nono” sample residue after sampling. The materials and equipment used to minimize contamination include autoclave, bacteriological oven, optical microscope, sterile 50 ml bottles for sampling “fura da nono”, cooler containing cold accumulators for transporting samples, Calibrated handles, spatula, beakers, Erlenmeyer flasks, graduated test tubes, sterile 90 mm-diameter Petri dishes, sterile graduated pipettes, sterile test tubes, sterile hemolysis tubes, gloves, object slides, marker, staining tray.
2.4. Sample Dilution Preparation
A 10−1 dilution of the stock solution was made for each sample by introducing 90 ml of sterile physiological water and 10 ml of “fura da nono” into sterile vials, before homogenizing with a vortex. Next, successive dilutions from 10−2 to 10−5 are made by taking 1 ml of the diluted solution and transferring it to tube number 1 containing 9 ml of sterile physiological water. A sample is then taken from this tube and transferred to the next, and so on until the 10−5 dilution is reached. All 18 samples underwent the same treatment, with dilutions of 10−2 and 10−3 chosen for inoculation.
2.5. Germ Research and Enumeration
Principle
This is the enumeration of all microorganisms forming colonies in aerobic conditions on nutrient agar or PCA (Plate Count Agar) after 24 to 72 hours incubation at 35˚C to 37˚C.
This test is used to assess the sanitary quality of the food, as it gives an idea of whether the food is fresh or decomposed.
Procedure
Reading the results
The total flora appears in the form of whitish colonies of different sizes and shapes.
Principle
Coliforms are counted on Methylene Blue Eosin (MBE) agar. After spreading the test sample over the entire surface of the medium, the plates are incubated for 24 hours at 37˚C for total coliforms and 44˚C for faecal coliforms.
Procedure
Reading the results
On medium incubated at 44˚C, fecal coliform colonies (Escherichia coli) appear as 2 to 3 mm colonies, flat, very dark purple with generally a metallic green sheen.
On plates incubated at 37˚C, total coliform colonies appear as large to medium-sized, convex, pinkish-gray, sometimes mucous colonies (Klebsiella), with a tendency to coalesce.
Principle
The sample is inoculated onto Baird Parker agar or Chapman mannite medium, then incubated at 37˚C for 24 hours.
Procedure
Reading results
Staphylococcus appear as bulging golden-yellow colonies surrounded by a yellow halo resulting from mannitol reduction.
Non-pathogenic Staphylococci generally form small red colonies which do not alter the color of the medium. The presence of Staphylococcus aureus is confirmed by the catalase test.
1) Catalase test
This is the test generally used to differentiate catalase-positive from catalase-negative staphylococci.
Procedure
Reading results
2) Coagulase test
Coagulase or staphylocoagulase is an enzyme capable of coagulating blood plasma. The demonstration of free coagulase activity in a Staphylococcus strain is one of the criteria for identifying Staphylococcus aureus.
Procedure
Introduce into a sterile hemolysis tube:
Reading
If the plasma coagulates in less than 24 hours, the germ possesses coagulase.
Research and enumeration of fungi:
For fungi (candida), we inoculated Chromatic TM Candida medium with yeast colonies from Sabouraud medium by direct streaking. Incubation took place aerobically at 30˚C - 37˚C for 24 - 48 hours. After incubation, colony color and morphology are observed and results are interpreted as indicated in the identification
Table 1
below.
It helps to identify bacteria by classifying them into two groups: Gram-positive bacteria stain violet and Gram-negative bacteria stain pink.
3. Results3.1. Results of Microbiological Analysis of “fura da nono” de Marche Dole Zinder
Colony counts for total germs (GT) range from 300 × 103 UCF/g to 15,680 × 103 UCF/g, highlighting a significant variation in bacterial load among samples. Poor hygiene levels are associated with the highest GT counts (Samples 12 and 14). Total coliform (TC) counts ranged from 5 × 103 UCF/g to 25,600 × 102 UCF/g, showing substantial differences in the presence of coliforms. High TC counts are associated with poor hygiene levels (Samples 12 and 14). Samples with Questionable hygiene levels show elevated microbial counts in several categories, including total germs, total coliforms and yeasts. The presence of fecal coliforms and staphylococci in some of these samples is also of concern, and indicates significant contamination (
Table 2
).
<xref ref-type="bibr" rid="scirp.142570-"></xref>Table 2. Results of microbiological germ analysis (CFU/g) of “fura da nono” samples.
N˚ of samples
GT/g
CT/g
CF/g
Yeast/g
Staphylococci/g
Hygiene level
1
2700 × 102
410 × 102
170 × 102
240 × 102
103 × 102
Good
2
300 × 103
170 × 103
13 × 103
14 × 103
17 × 103
Very good
3
1070 × 102
720 × 102
80 × 102
190 × 102
66 × 102
Good
4
660 × 102
308 × 102
21.7 × 102
38 × 102
50 × 102
Good
5
800 × 102
440 × 102
110 × 102
68 × 102
33 × 102
Good
6
300 × 103
5 × 103
0
186 × 103
0
Very good
7
1300 × 102
38 × 102
0
450 × 102
2 × 102
Very good
8
2180 × 102
55 × 102
0
1040 × 102
0
Very good
9
3140 × 102
110 × 102
0
840 × 102
15 × 102
Very good
10
3700 × 102
348 × 102
0
330 × 102
100 × 102
Good
11
3360 × 103
17 × 103
0
210 × 103
2 × 103
Good
12
35,000 × 102
25,600 × 102
372 × 102
6200 × 102
120 × 102
Poor
13
4400 × 103
200 × 103
0
600 × 103
0
Very good
14
15,680 × 103
2300 × 103
140 × 103
920 × 103
0
Poor
15
4160 × 103
500 × 103
3120 × 103
110 × 103
0
Questionable
16
3880 × 103
580 × 103
130 × 103
118 × 103
0
Questionable
17
1580 × 103
290 × 103
0
1360 × 103
960 × 103
Questionable
18
6000 × 103
1520 × 103
210 × 103
3800 × 103
0
Questionable
Escherichia coli is the most common bacterium, detected in all samples (100%). Staphylococcus spp, Klebsiella pneumoniae and Staphylococcus aureus are also significantly present, with 38.9%, 33.3% and 22.2% respectively. Pseudomonas aeruginosa and Citrobacter koseri are the least frequent, each present in 5.6% of samples (
Table 3
).
<xref ref-type="bibr" rid="scirp.142570-"></xref>Table 3. Different bacteria identified in “fura da nono” samples.
Bacteria
Frequences
%
Escherichia coli
18
100
Staphylococcus spp
7
38.9
Klebsiella pneumoniae
6
33.3
Staphylococcus aureus
4
22.2
Pseudomonas aeruginosa
1
5.6
Citrobacter koseri
1
5.6
Candida glabrata is the most common fungus, detected in 77.8% of samples. Candida krusei and Candida albicans are also significantly present, with 33.3% and 22.2% respectively (
Table 4
).
<xref ref-type="bibr" rid="scirp.142570-"></xref>Table 4. Different fungi identified in “fura da nono” samples.
Fungi
Frequences
%
Candida glabrata
14
77.8
Candida krusei
6
33.3
Candida albicans
4
22.2
Figure 2
shows the culture on petri dishes, of different fungi identified from “fura da nono” samples.
The pH measurements of “fura da nono” samples show that they are almost acid. The distribution was shown in
Figure 3
.
Figure 2. Different fungi identified in “fura da nono” samples.
Figure 3. pH distribution of “fura da nono” samples.
3.2. Results of Questionnaire Sent to “fura da nono” Sellers at the Zinder Dolé Market
1) Time of preparation and storage of fura for sale
According to the results of our survey, all eighteen (18) saleswomen, i.e. 100%, prepare the fura destined for sale on the same day and keep the remainder (unsold) at room temperature until the following day.
2) Saleswomen’s knowledge of the risk of consuming unhealthy food and training in food hygiene
According to our results, 78% of “fura da nono” saleswomen are aware of the risks associated with consuming unhealthy foods, while 22% are not. The majority of saleswomen (72%) have not had any training in food hygiene, while 28% have received at least one course in food hygiene. The saleswomen were asked how often they washed their hands, in order to assess the regularity of this hygienic gesture during the sale of “fura da nono”. The survey revealed that 67% of saleswomen did not wash their hands regularly, only 17% washed regularly and 16% washed their hands before starting the sale. The results show that none of the permanent “fura da nono” saleswomen have a health book and does not carry out a medical examination. The aim here is to observe the hygiene of the sales environment, which is a factor that can contaminate the food.
The results in
Table 5
show that all samples were sold on the ground, and that the majority of sales environments were affected by the presence of garbage, flies and dust, which could compromise the quality and safety of the products sold.
<xref ref-type="bibr" rid="scirp.142570-"></xref>Table 5. Quality of the “fura da nono” sales environment at the Zinder Dolé market.
Sales environment
Frequencies
Percentage
P-value
Sale of fura on the ground
Yes
18
100 %
No
0
0%
Garbage presence
Yes
10
55.6%
<0.0001
No
8
44.4%
Presence of flies
Yes
14
77.8%
0.000
No
4
22.2%
Presence of dust
Yes
13
72.2%
0.000
No
5
27.8%
3) Unhygienic behavior
These are unhygienic behaviors by the sellers that could contaminate the dish during service.
Observations show varied hygiene practices among sellers. Positive points include the fact that most sellers do not clean their hands with clothes or cough near food. However, worrying practices such as talking on food, not covering food, not washing utensils after each use and handling money while selling are common, which could compromise food safety (
Table 6
).
<xref ref-type="bibr" rid="scirp.142570-"></xref>Table 6. Gestures observed during the sale of “fura da nono” at Zinder Dolé Market.
Gestures observed during the sale
Frequencies
Percentage
P-value
Cleans hands with clothes
Yes
5
27.8
0.000
No
13
72.2
Talking on food
Yes
15
83.3
0.001
No
3
16.7
Coughing around food
Yes
2
11.1
0.007
No
16
88.9
Food is covered
Yes
3
16.7
0.001
No
15
83.3
Wash utensils after each use
Yes
4
22.2
0.000
No
14
77.8
Taking money by hand while selling food
Yes
18
100
Non
0
0
4. Discussion
In our study, germ counts for “fura da nono” showed 300 × 103 CFU/g to 15,680 × 103 CFU/g for total germs, from 5 × 103 CFU/g to 25,600 × 102 CFU/g for Total Coliforms (TC) and from 14 × 103 CFU/g to 6200 × 102 CFU/g for yeasts. As for fecal coliforms, the numbers vary from 0 to 3120 × 103 CFU/g and for Staphylococci, from 0 to 960 × 103 CFU/g. In a study carried out in Nassarawa (Nigeria) by Ajobiewe et al. (2022), bacterial counts ranged from 4.0 × 104 to 7.0 × 104 CFU/ml
[5]
. These results are lower than those obtained in our study. On the other hand, a study carried out in Kebbi, Nigeria by Abbas et al., (2020) showed higher results than ours, with viable bacterial colonies in “fura da nono” ranging from 8.3 × 105 to 1.25 × 108 CFU/ml
[6]
. This high bacterial load could be due to contamination of the utensils used during processing and to the hygiene of the sellers. It could also be attributed to micro-organisms present in the raw materials, in the environment and in the processing water. But even the milk used in preparation is not free from microorganisms. Like other dairy products, “fura da nono” is frequently contaminated by microbial agents. The microbiological analysis carried out in this study revealed the presence of six (6) bacterial species (Staphylococcus aureus, staphylococcus spp, Escherichia coli, klebsiella pneumoniae, Pseudomonas aeruginosa, Citrobacter koseri). These results are not very similar to those of Ajobiewe et al., (2022); Nneoma Confidence, (2019) who identified bacteria such as Staphylococcus, Escherichia, Lactobacillus, Streptococcus, Leuconostoc, Pseudomonas and Bacillus
[5]
[7]
.
Microorganisms such as staphylococcus aureus and Escherichia coli were found by Abbas et al., (2020) and also by Eluchie, et al., (2019) in the “fura da nono”
[6]
[8]
.
These bacterial organisms identified in their study corroborate the results found in this study. Furthermore, some of the bacteria identified in this present study such as Staphylococcus aureus, Escherichia coli, Pseudomonas aeruginosa, Klebsiella pneumoniae have also been reported by Edem, et al., (2022)
[9]
. Then E. coli is present in all “fura da nono” samples in our study, this result is consistent with that of Eluchie, et al., (2019)
[8]
. The presence of E. coli in “fura da nono” may be an indication of faecal contamination. It also indicates that hygiene standards are not respected during the “fura da nono” preparation and sale processes. Our results show the presence of pathogenic micro-organisms that can be a potential source of food-borne infections and related illnesses for consumers. The presence of S. aureus is probably due to poor handling by saleswomen using contaminated bare hands. It is an indicator germ of human contamination. Its main habitat is the nasal mucosa, mouth, throat and skin of healthy individuals. This bacterium is easily disseminated in the environment and can thus contaminate foodstuffs. At certain concentrations, this bacterium is considered dangerous and responsible for many cases of food poisoning.
Pseudomonas aeruginosa is widely distributed in soil and water, and can therefore contaminate food products. This can lead to infection if ingested. Klebsiella pneumoniae can cause hospital-acquired infections. Escherichia coli causes haemorrhagic diarrhoea and poisoning. While Streptococcus spp are also implicated in urinary tract infections, nausea, vomiting and diarrhea in humans. The three species of fungi isolated from the “fura da nono” samples in our study were Candida glabrata, Candida krusei and Candida albicans. These results are not in line with those of Abbas et al., (2020) in kebbi (Nigeria) who detected Aspergillus niger, Aspergillus flavus and Saccharomyces cerevisiae
[6]
. The same species were found by Edem et al., (2022), with the exception of Penicillium spp and Mucor spp which were not also found in this study
[9]
. A study carried out in the Nigerian capital by Nneoma Confidence, (2019) identified two species of fungi, Rhizopus stolonifera and Aspergillus niger
[7]
. These results are not as identical to those of our study. Also, these fungi found in “fura da nono” can cause invasive candidiasis or mucosal infections according to a World Health Organization study, (2022), the presence of these species may be due to changes in the pH or microbial environment of the skin and mucosa
[10]
. This may be due to poor hygiene practices on the part of “fura da nono” sellers. While the reinforcement of hygiene in activities could be a general infection control measure to prevent the health of consumers. The presence of bacteria and fungi in “fura da nono” can be due to many factors. Female sellers are the main source at various stages from preparation to sale, and this could explain the failure of “fura da nono” sellers to comply with hygiene rules.
In fact, the average pH in our study was 4.34, with a range of 3.52 to 5.6. All “fura da nono” samples have an acid pH. The results of our study are almost similar to those of Abbas et al., (2020) in their study carried out in Kebbi Nigeria, where the pH ranges from 3.1 to 6.8
[7]
. Ajobiewe et al., (2022) in a study carried out in Nasarawa Nigeria also showed that all the “fura” samples they studied were in the acid phase
[6]
. A study carried out by Omola et al., (2019) identified the pH of these samples as 3.5 to 5.36, these results are in line with our findings
[11]
. This acidity may be explained by the addition of spices to the preparation, but also by the process of carbohydrate fermentation by microorganisms, favored by the environmental temperature of manufacture and storage.
The sale of “fura da nono” at the Dolé market is an economic activity reserved for women. The sources of contamination of these foods can be grouped into the materials used in direct contact with “fura da nono”, which may constitute potential sources of contamination. The environment in which the food is handled (sales environment): all saleswomen sell “fura da nono” on the ground. This can be a source of contamination. The methods used to prepare, store and preserve these foods can be considered a source of contamination. For example, 100% of “fura da nono” sellers don’t preserve their products, keeping their leftovers (unsold) at room temperature until the next day to resell. This method of preservation by fura sellers is a source of microbial proliferation. This poor preservation could be explained by the sellers’ ignorance of the importance of good preservation, but also by a lack of resources.
“fura da nono” is mixed with water to improve mixing. The equipment used, such as buckets, cans, calabashes, bowls and ladles, which are not well maintained, are therefore the most important sources of microbial contamination. What’s more, the majority of “fura da nono” sellers don’t wash their hands before starting their shift, despite the fact that controlling food safety necessarily involves hand-washing, which should become a reflex. This shows how little “fura da nono” sellers know about food hygiene. Secondly, not all sellers cover the “fura and nono” balls during the entire sales period. 100% of sellers hold the money in their hands while selling fura, and 83.3% talk on the food, which can be a source of contamination. This demonstrates the lack of respect for hygiene rules at the Zinder Dolé market. Observation of the sales environment also reveals the presence of flies in 77.8% of sites, and dust in 72.2% of sales outlets. This is a major source of microbial contamination of foodstuffs. This poor practice is due to the position of the sales site, but also to the negligence of saleswomen despite their knowledge of the involvement of flies and dust in food contamination. It should be noted that 100% of “fura da nono” sellers operating on the Dolé market do not have food sales permits issued by the relevant authorities. This shows that medical examinations are not carried out. This proves that saleswomen are not informed about what they need to do to carry out their activity legally, in particular to obtain a sales authorization booklet. Whereas the appointment is given on a quarterly basis. What’s more, if the staff handling the “fura da nono” are not in good health, or have skin or hand infections, bacteria can be added to the “fura da nono”, hence the importance of the periodic medical check-up, which can detect illnesses in saleswomen. In Niger, article 4 of Decree 2008-224/PRN/MSP of July 17, 2008 stipulates that “personnel involved in the production or trade of foodstuffs must undergo medical examinations every three (3) months at the health police laboratory or any other approved laboratory. The medical examinations concerned are as follows: KOPA stool examination; urinary bile examination; physical examination.
Despite the rigor of this study’s methodology, it has certain limitations that it is important to highlight. Firstly, sampling was limited to stationary “fura da nono” vendors located inside Zinder’s Dolé market, thus excluding vendors located on the outskirts. This may reduce the representativeness of the results, as the hygiene practices of mobile vendors or those outside the main market may differ. Secondly, collecting a single sample per outlet may not reflect possible variations in preparation or hygiene conditions over time.
5. Conclusion
This shows that the “fura da nono” sold by permanent sellers are contaminated with micro-organisms. Some of the species identified in this study are known to be pathogenic and may therefore present a danger to public health. This is due to the fact that “fura da nono” sellers at the Dolé market have poor hygiene practices and little knowledge of good hygiene practices. It is therefore necessary to raise their awareness of handling, preparation, sales methods and hygiene to avoid illnesses linked to the organisms encountered in this study. It can be concluded that prepared “fura da nono” contains pathogenic bacteria. Their presence indicates unhygienic handling during production. For this reason, the microbiological quality of “fura da nono” at the Dolé market should be improved by respecting and applying Good Manufacturing Practices (GMP) and Good Hygiene Practices (GHP).
Ethical Approval
This study does not require approval from an ethics committee, as it does not involve human participants or animal experiments.
Data Availability Statement
The data used to support the results of this study are available upon request from the corresponding author.
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