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. 2022 Apr 14;17(4):e0258435. doi: 10.1371/journal.pone.0258435

Microbiological quality assessment of five common foods sold at different points of sale in Burkina-Faso

Muller Kiswendsida Abdou Compaore 1,2,*, Stéphane Dissinviel Kpoda 1,3,#, Raoul Bazoin Sylvain Bazie 1,2,#, Marcelline Ouedraogo 1,‡, Mahamady Valian 1,‡, Marie-Louise Gampene 1,‡, Alphonse Yakoro 1,‡, Fulbert Nikiema 1,‡, Asseto Belemlougri 1,‡, Naamwin-So-Bawfu Romaric Meda 1,#, Naa-Imwine Stanislas Dimitri Meda 1,‡, Souleymane Sanon 4,#, Moumouni Bande 1,5,#, Hervé Hien 4,#, Nicolas Barro 2,#, Elie Kabre 1,5,#
Editor: Guadalupe Virginia Nevárez-Moorillón6
PMCID: PMC9009693  PMID: 35421088

Abstract

The aim of the present study was to assess the microbial quality of five ready-to-eat food such as bread, pasta, rice with sauce, beans and milk sold in five localities of Burkina Faso namely, Ouagadougou, Bobo-Dioulasso, Dakola, Cinkansé and Niangoloko. One hundred and one samples were collected and microbial quality were assessed by evaluating the food hygiene indicators such as total aerobic mesophilic flora, total coliforms, thermotolerant coliforms, yeast and mould. Food safety indicators such as Escherichia coli, Salmonella, coagulase-positive staphylococci, Clostridium perfringens and Bacillus cereus were also tested for contamination. Samples were tested according to ISO guidelines for all parameters.

The results showed that 74 (73.27%) of samples were satisfactory while 15 (14.85%) were acceptable and 12 (11.88%) were not satisfactory according to international standards. Among the food safety indicators sought, Escherichia coli was detected in two samples and Bacillus cereus in four samples. Most of the analyzed food exhibited good hygiene behavior within the acceptable limits and the highest of not satisfactory rate was observed in milk powder and rice with sauce. Ouagadougou samples recorded the highest number of not satisfactory samples.

Despite the general quality was satisfactory, the presence of specific microorganisms such as coliforms is indicative of the poor hygiene surrounded these foods. It is therefore necessary to train and follow up the vendors in the handling of equipment, hand-washing practices and selling environment hygiene for better improvement of the quality of the street foods.

Introduction

Food quality is always a concern when intended to human consumption. Food-borne diseases have been increasing in recent years, with a greater impact on the health and economy of developing countries than developed countries [1]. According to [2] access to sufficient amounts of safe and nutritious food is key to sustaining life and promoting good health and unsafe food containing harmful bacteria, viruses, parasites or chemical substances, causes more than 200 diseases ranging from diarrhea to cancers. An estimated 600 million (almost 1 in 10 people in the world) fall ill after eating contaminated food and 420 000 die every year, including 125 000 children under the age of 5 years [2]. Common foods such as bread, beans, pasta, rice with sauce and powdered milk are common dishes suited as well as to many low-income people as to living conditions in large cities. These foods refer to street foods that play an important role in developing countries such as Burkina Faso. According to the [3], Street foods are ready-to-eat foods and beverages prepared and/or sold by vendors and hawkers especially in streets and other similar public places. This definition emphasizes the retail location on the street, with foods sold from pushcarts, bicycles, baskets or balance poles, or from stalls that do not have four permanent walls [4]. These street foods feed millions of people daily with a wide variety of ready-to-eat foods and beverages sold and sometimes prepared in the street or public places, relatively cheap and easily accessible [5, 6]. Although in developing countries the informal food vending sector has in recent years grown into a lucrative trade that competes with the formal sector, ignorance in regard to and inadequate knowledge of food handling practices, together with a lack of formal education, have prevailed among the majority of informal food handlers [7, 8]. Food can serve as ideal culture medium for the growth of microorganisms which can cause decomposition, spoilage and also serve as a vehicle for transmission of food borne illnesses [9]. The food production sites are generally located either in living spaces or near workplaces or on sale sites. The majority of these vending sites lacks basic infrastructure and services such as potable running water and waste disposal facilities, hand and dishwashing water is usually insufficient and often reused, sometimes without soap, waste water is discarded in the street and garbage often disposed of in the vicinity of the stall [7, 10].

Street food quality is a concern around the world. Studies conducted in many countries such as Mozambique [11], Malaysia [8, 12], Brazil [13], Bangladesh [14], Kenya [15] and so on have been reported. In developing countries, street foods are driven by men and women that knowledge and expertise in food handling are often limited and they often engage in street food mainly to escape poverty, especially as little start-up capital is required [3]. However, it is important to consider the health and safety impact of these food products, because foodborne infections are more and more frequent, hence the need for control strategies to ensure food safety and consumer protection. According to previous studies conducted by [9], foodborne illness is a major universal health issue in developing countries due to difficulties in safe guarding food from cross-contamination.

Burkina Faso is a land lock country neighbored by six countries, with which it shared almost the same habits of street food accessibility. Vending foods on the street is a common aspect of lifestyle in countries in which there are high unemployment, low salaries, limited work opportunities and limited social programs [16, 17]. Foods sanitary quality controls are often limited to large urban centers to the detriment of rural populations. This study is intended to investigate and shed light on the microbial safety of five common street foods sold at different points of sale in five localities of Burkina-Faso.

Material and methods

Sample collection and storage

One hundred and one samples divided into five groups including 15 bread samples, 12 for beans samples, 12 pasta samples, 19 rice with sauce samples and 43 milk powder samples were collected from November to December 2021 in five localities of Burkina Faso. Samples were purchased at local stores markets, street food and restaurants. Briefly, 100 g of each sample were taken aseptically and put in a sterile plastic bag, type Wagtech, (United Kingdom) certify ISO 9001, and sealed. Sample were kept less than 4°C in a cooler containing ice box and carry in laboratory for analysis. Samples reached the laboratory were analyzed immediately or within the following 24 hours.

Table 1 shows the repartition of all the food samples submitted to this study.

Table 1. Subtotal of ready-to-eat food samples.

SAMPLES OUAGADOUGOU BOBO-DIOULASSO DAKOLA CINKANSÉ NIANGOLOKO QUANTITY PERCENTAGE %
BEANS 4 2 2 2 2 12 11.88
MILK POWDER 15 9 6 6 7 43 42.57
BREAD 4 3 2 3 3 15 14.85
RICE WITH SAUCE 6 4 3 3 3 19 18.81
PASTA 3 3 2 2 2 12 11.88
TOTAL 32 21 15 16 17 101 100
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Sampling sites include ordinary restaurants, local markets and shops. The concerned localities are Ouagadougou, Bobo-Dioulasso, Dakola, Cinkansé and Niangoloko. All samples were taken aseptically in sterile plastic bag, kept in an insulated cold box containing ice boxes or stored at room temperatures. Samples reached the laboratory are immediately analyzed or kept under 4°C until used.

Analysis parameters

Parameters applied to each group of samples were those recommended by the Codex Alimentarius for cooked foods namely, Total aerobic mesophilic flora, Coliforms, Thermotolerant coliforms, Yeast and mould, Escherichia coli, Salmonella spp. and Coagulase-positive staphylococci. In addition, Anaerobic Sulfito Reductive (ASR) bacteria, Clostridium perfringens and Bacillus cereus were investigated in milk only.

  • Microbial Analysis, twenty-five (25) grams of each food sample were added into 225 mL of sterile buffered peptone water (Liofilchem diagnostic, Italy) and homogenized in a Bag Mixer (Interscience, France) for one minute at speed 6. Further tenfold serial dilutions were made with sterile buffered peptone water. Duplicate plates were made for each sample at each dilution under ISO 6887–1: 2017 standard methods. Microbial counts were expressed as Colony-Forming Units per gram (CFU/g).

Evaluation of the food hygiene indicators

  • Total aerobic mesophilic flora, were counted among all the food samples onto standard Plate Count Agar (PCA); (Conda Pronadisa, Spain) under NF ISO 4833: 2013. Plates were incubated at 30 ± 1°C for 72 h. After incubation the number of colonies were counted on the culture plate with less than 300 colonies. For culture plates with less than 15 colonies, averages were calculated to estimate the number of CFU/g.

  • Coliforms were counted onto standard violet red bile lactose (VRBL) agar (Conda Pronadisa, Spain) and incubated at 37°C for 24 hours under ISO 4832:2006. Culture plates containing less than 150 colonies were considered. For culture plates with less than 15 colonies, averages were calculated to estimate the number of CFU/g.

  • Thermotolerant coliforms are known to be an indicator of fecal contamination were counted onto standard violet red bile lactose (VRBL) agar (Conda Pronadisa, Spain) and incubated at 44.5 ± 0.5°C for 24 hours under NF V60-2009. Culture plates containing less than 150 colonies were considered. For culture plates with less than 15 colonies, averages were calculated to estimate the number of CFU/g.

  • Yeast and mould were counted onto standard yeast extract glucose chloramphenicol (YGC) agar (HiMedia Laboaratories, India) and incubated at 25 ± 1°C for 5 days following NF V08-59:2002. The growth of moulds was checked every day in order to avoid invading colonies. Considered culture plates for bacterial counting were less than 150 colonies. For culture plates with less than 15 colonies, averages were calculated to estimate the number of CFU/g.

Evaluation of food safety indicators

Escherichia coli

E. coli were identified through the IMViC test from thermotolerant coliforms. Briefly, suspected colonies from thermotolerant coliforms were selected and subcultured on Nutrient Agar at 37°C for 24 hours. Pure cultures grown on Nutrient Agar were used for Oxidase test and determination of IMViC pattern (indole production, methyl red reaction, Voges Proskauer and citrate utilization test) under the Standard Procedures for food Analysis. Positives colonies were transferred into Levine Eosin Methylene Blue Agar (EMB) (France), which was incubated at 37 ± 1°C for 24 hours. Colonies with green metallic sheen were considered to be Escherichia coli. Escherichia coli ATCC 8739 was used as positive control for all analyses.

Salmonella spp

Salmonella species were investigated according to the standard—Horizontal method for detection of Salmonella spp ISO 6579–1:2017. Briefly, the non-selective enrichment was done by adding 25 g of each sample into 225 mL buffered peptone water (Liofilchem diagnostic, Italy) and homogenized in a Bag Mixer (Interscience, France). Incubation was done at 37°C for 18 to 20 hours. The selective enrichment step was performed onto both tetrathionate (Müller-Kauffman) (Liofilchem diagnostic, Italy) and Rappaport Vassiliadis Soy (Difco laboratories) broths incubated respectively at 37 ± 1°C and 42 ± 1°C for 18 to 20 hours. A brilliant green at 0.95% was added to the selective media Tetrathionate broth in order to inhibit the growth of Gram-positive bacteria. Selective isolations were performed onto Xylose Lysine Deoxycholate (HiMedia Laboaratories, India) and Salmonella-Shigella (HiMedia Laboaratories, India) agars. Five suspected colonies of each sample were streaked onto nutrient agar and were performed using API 20E (BioMérieux, France) test for biochemical confirmation. Salmonella typhimurium (ATCC 14028) and Salmonella enteritidis (ATCC 13076) was used as positive control. The Key biochemical tests included the fermentation of glucose, negative urease reaction, lysine decarboxylase, negative indole test, H2S production, and fermentation of dulcitol [18].

Coagulase-positive staphylococci

Staphylococci were isolated under ISO 6888–3:2003. Briefly, 25 g of each food sample were dissolved in 225 ml of Peptone Water (Liofilchem diagnostic, Italy). and homogenized in a Bag Mixer (Interscience, France). A loop of 100μl of each sample were then spread onto Baird Parker Agar (BP) supplemented with egg-yolk tellurite emulsion (HIMEDIA) and incubated under aerobic conditions at 37°C for 24 and 48 h. The samples producing typical colonies (grey-black, surrounded by a dull halo) were considered. Biochemical confirmation to determine whenever these colonies are Coagulase positive was performed using rabbit lyophilized plasma.

Anaerobic Sulfito Reductive (ASR) bacteria and Clostridium perfringens

ASR were isolated under ISO 15213:2003. For this purpose, 25 g of each food sample were dissolved in 225 ml of Peptone Water (Liofilchem diagnostic, Italy) and homogenized in a Bag Mixer (Interscience, France). 1 ml from each dilution were mixed with tryptose sulfite cycloserine agar and after solidification the plates were overlayed by using the same medium. After incubations at 46°C for 18 to 20 h under anaerobic condition, characteristic colonies were isolated for biochemical confirmation of Clostridium perfringens under ISO 7937:2004. Briefly, five black colonies were picked, and each was inoculated into 10 ml of fluid thioglycolate broth. After 18 to 20 h at 37°C, thioglycolate tubes were used to inoculated complete lactose sulfite broth containing Durham tubes and then incubated at 37°C for 18 to 20 h. Tubes with black butt and gas in the Durham tubes are considered as Clostridium perfringens. Clostridium perfringens ATCC 13124 was used as a positive control for all biochemicals tests.

Bacillus cereus

Enumeration of Bacillus cereus was performed by surface plating techniques of 100μl on mannitol-egg yolk-polymyxin under ISO 7932:2020. This media use polymyxin B as the selective agent and permit presumptive identification by the lecithinase reaction on the egg yolk and the inability of Bacillus cereus to catabolize mannitol. The media were incubated at 35°C for 24 h. The number of Bacillus cereus was determined after enumeration of the colonies having its characteristic appearance and submitted to biochemical characterization. Bacillus cereus ATCC 11778 was used as a positive control.

The appreciation criteria of microbiological food quality, namely “satisfactory”, “acceptable” and “not satisfactory”, of all food samples are enumerated in Table 2

Table 2. Quality appreciation criteria of ready to eat meals (A) and conditioned milk powder (B).
Parameters Criteria m CFU/g M (3m) CFU/g
A
Ready meals Salmonella Absence/25g ---
Staphylococci 102/g 3x102/g
Total aerobic mesophilic flora 3x103/g 9x103/g
Coliforms 103/g 3x103/g
Thermotolerants Coliforms 10/g 3x10/g
E. coli Absence ---
Yeast and Mould 104/g 3x104/g
B
Conditioned milk powder Salmonella Absence/25g ---
Staphylococcus aureus 10/g 30/g
Total aerobic mesophilic flora 5x104/g 1.5x105/g
Coliforms 1/g 3/g
Thermotolerants Coliforms 1/g ---
E. coli Absence ---
Yeast and Mould 1/g ---
ASR 10/g 30/g
Clostridium perfringens 1/g 3/g
Bacillus cereus 1/g ---
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Source: The bacteriological criteria retained are those stipulated by the Ministerial Decree of the French Republic of December 21, 1979 relating to ready-to-eat foods and cited by [19].

m and M are respectively lower and upper the limits of appreciation.

CFU ≤ m = Satisfactory.

m < CFU ≤ M = Acceptable.

CFU > M = Not Satisfactory.

Results

The results showed that out of 101 samples submitted to this study, 73.27% were satisfactory according to the criteria used, while 14.85% were acceptable and 11.88% were not satisfactory (Fig 1). Table 3 summarizes the raw results of the evaluation of the bacterial load and the presence of pathogens in all the samples submitted to this study. Only 6.93% (7 samples over 101) of the analyzed samples did not show any microorganism. The highest number of coliforms, total aerobic mesophilic flora, thermotolerant coliforms and yeast and mould were recorded in the same sample of rice with sauce in Ouagadougou and values are respectively 2x104, 2.4x105, 1.7x104 and 1.6x104. E. coli were found in two (02) samples of Ouagadougou namely bean and pasta. On the other hand, Bacillus cereus was found in four (04) samples of milk namely two in Ouagadougou and two in Cinkansé. Neither Salmonella nor Clostridium perfringens were found in any samples.

Fig 1. The overall appreciation of samples quality.

Fig 1

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Table 3. Bacterial count of sample according to localities.

Locality Food type Total Coliforms Total aerobic mesophilic flora Thermotolerants Coliforms E. Coli Coagulase-positive staphylococci Salmonella yeast and mould Anaerobic Sulfito Reductive (ASR) Clostridium perfringens Bacillus cereus
CIN Beans <1E+01 7.0E+01 <1E+01 <1E+01 <1E+02 Absent <1E+01 - - -
CIN Beans <1E+01 3.0E+01 <1E+01 <1E+01 <1E+02 Absent <1E+01 - - -
NIA Beans <1E+01 1.3E+03 <1E+01 <1E+01 <1E+02 Absent <1E+01 - - -
NIA Beans <1E+01 <1E+01 <1E+01 <1E+01 <1E+02 Absent <1E+01 - - -
DAK Beans <1E+01 <1E+01 <1E+01 <1E+01 <1E+02 Absent <1E+01 - - -
DAK Beans <1E+01 7.8E+03 <1E+01 <1E+01 <1E+02 Absent <1E+01 - - -
BOB Beans <1E+01 5.0E+01 <1E+01 <1E+01 <1E+02 Absent <1E+01 - - -
BOB Beans <1E+01 5.0E+01 <1E+01 <1E+01 <1E+02 Absent <1E+01 - - -
OUA Beans <1E+01 9.0E+01 <1E+01 <1E+01 <1E+02 Absent <1E+01 - - -
OUA Beans 1.0E+02 1.2E+04 4.0E+01 2.0E+01 <1E+02 Absent <1E+01 - - -
OUA Beans <1E+01 5.6E+03 <1E+01 <1E+01 <1E+02 Absent <1E+01 - - -
OUA Beans <1E+01 1.5E+04 <1E+01 <1E+01 2.9E+02 Absent 4.0E+01 - - -
CIN Bread 4.0E+01 2.5E+02 <1E+01 <1E+01 <1E+02 Absent 1.0E+01 - - -
CIN Bread <1E+01 <1E+01 <1E+01 <1E+01 <1E+02 Absent <1E+01 - - -
CIN Bread <1E+01 1.0E+03 <1E+01 <1E+01 <1E+02 Absent 2.0E+01 - - -
NIA Bread <1E+01 2.7E+02 <1E+01 <1E+01 <1E+02 Absent 3.0E+01 - - -
NIA Bread <1E+01 6.5E+03 <1E+01 <1E+01 <1E+02 Absent 3.7E+02 - - -
NIA Bread <1E+01 8.0E+01 <1E+01 <1E+01 <1E+02 Absent <1E+01 - - -
DAK Bread <1E+01 2.0E+01 <1E+01 <1E+01 <1E+02 Absent <1E+01 - - -
DAK Bread <1E+01 8.0E+01 <1E+01 <1E+01 <1E+02 Absent <1E+01 - - -
BOB Bread <1E+01 7.0E+03 <1E+01 <1E+01 <1E+02 Absent 5.1E+02 - - -
BOB Bread <1E+01 2.7E+02 <1E+01 <1E+01 <1E+02 Absent 1.0E+01 - - -
BOB Bread <1E+01 7.9E+02 <1E+01 <1E+01 <1E+02 Absent 2.0E+01 - - -
OUA Bread 1.8E+02 1.3E+03 4.0E+10 <1E+01 <1E+02 Absent 2.0E+02 - - -
OUA Bread <1E+01 6.5E+02 <1E+01 <1E+01 <1E+02 Absent 5.3E+02 - - -
OUA Bread <1E+01 2.0E+01 <1E+01 <1E+01 <1E+02 Absent <1E+01 - - -
OUA Bread <1E+01 3.8E+02 <1E+01 <1E+01 <1E+02 Absent 1.0E+01 - - -
CIN Pasta <1E+01 <1E+01 <1E+01 <1E+01 <1E+02 Absent <1E+01 - - -
CIN Pasta <1E+01 8.0E+01 <1E+01 <1E+01 <1E+02 Absent <1E+01 - - -
NIA Pasta <1E+01 1.1E+02 <1E+01 <1E+01 <1E+02 Absent <1E+01 - - -
NIA Pasta <1E+01 3.4E+02 <1E+01 <1E+01 <1E+02 Absent <1E+01 - - -
DAK Pasta 4.0E+01 1.4E+03 1.0E+10 <1E+01 <1E+02 Absent 4.2E+02 - - -
DAK Pasta <1E+01 1.3E+02 <1E+01 <1E+01 <1E+02 Absent <1E+01 - - -
BOB Pasta <1E+01 1.6E+02 <1E+01 <1E+01 <1E+02 Absent <1E+01 - - -
BOB Pasta <1E+01 <1E+01 <1E+01 <1E+01 <1E+02 Absent <1E+01 - - -
BOB Pasta <1E+01 2.0E+01 <1E+01 <1E+01 <1E+02 Absent <1E+01 - - -
OUA Pasta <1E+01 <1E+01 <1E+01 <1E+01 <1E+02 Absent <1E+01 - - -
OUA Pasta <1E+01 1.0E+01 <1E+01 <1E+01 <1E+02 Absent <1E+01 - - -
OUA Pasta 5.0E+01 4.9E+04 3.0E+01 3.0E+01 <1E+02 Absent <1E+01 - - -
CIN Rice+Sauce <1E+01 6.0E+01 <1E+01 <1E+01 <1E+02 Absent <1E+01 - - -
CIN Rice+Sauce <1E+01 2.9 E+03 <1E+01 <1E+01 <1E+02 Absent <1E+01 - - -
CIN Rice+Sauce <1E+01 5.0E+01 <1E+01 <1E+01 <1E+02 Absent <1E+01 - - -
NIA Rice+Sauce <1E+01 2.7E+02 <1E+01 <1E+01 <1E+02 Absent <1E+01 - - -
NIA Rice+Sauce 1E+01 2.5E+03 <1E+01 <1E+01 <1E+02 Absent <1E+01 - - -
NIA Rice+Sauce 1.1E+02 2.9E+04 <1E+01 <1E+01 <1E+02 Absent 5.1E+03 - - -
DAK Rice+Sauce <1E+01 2.3E+02 <1E+01 <1E+01 <1E+02 Absent <1E+01 - - -
DAK Rice+Sauce <1E+01 2.0E+01 <1E+01 <1E+01 <1E+02 Absent <1E+01 - - -
DAK Rice+Sauce <1E+01 1.1E+02 <1E+01 <1E+01 <1E+02 Absent <1E+01 - - -
BOB Rice+Sauce <1E+01 4.0E+01 <1E+01 <1E+01 <1E+02 Absent <1E+01 - - -
BOB Rice+Sauce <1E+01 5.0E+01 <1E+01 <1E+01 <1E+02 Absent <1E+01 - - -
BOB Rice+Sauce <1E+01 3.0E+04 <1E+01 <1E+01 <1E+02 Absent 1.0E+01 - - -
BOB Rice+Sauce <1E+01 6.7E+03 <1E+01 <1E+01 <1E+02 Absent <1E+01 - - -
OUA Rice+Sauce <1E+01 5.8E+03 <1E+01 <1E+01 <1E+02 Absent <1E+01 - - -
OUA Rice+Sauce <1E+01 5.6E+03 <1E+01 <1E+01 <1E+02 Absent <1E+01 - - -
OUA Rice+Sauce <1E+01 3.0E+01 <1E+01 <1E+01 <1E+02 Absent <1E+01 - - -
OUA Rice+Sauce 2.0E+04 2.4E+05 1.7E+04 <1E+01 <1E+02 Absent 1.6E+04 - - -
OUA Rice+Sauce 7.9 E+02 5.5E+03 1.5E+02 <1E+01 <1E+02 Absent 1.0E+01 - - -
OUA Rice+Sauce 5.0 E+01 2.6E+03 3.0E+10 <1E+01 <1E+02 Absent 2.1E+02 - - -
NIA Milk <1E+01 1.8E+02 <1E+01 <1E+01 <1E+02 Absent <1E+01 <1E+01 not detected not detected
NIA Milk <1E+01 3.2E+02 <1E+01 <1E+01 <1E+02 Absent <1E+01 <1E+01 not detected not detected
CIN Milk <1E+01 2.3E+02 <1E+01 <1E+01 <1E+02 Absent <1E+01 <1E+01 not detected Detected
CIN Milk <1E+01 1.3E+02 <1E+01 <1E+01 <1E+02 Absent <1E+01 <1E+01 not detected not detected
CIN Milk <1E+01 <1E+01 <1E+01 <1E+01 <1E+02 Absent <1E+01 <1E+01 not detected not detected
CIN Milk <1E+01 2.8E+02 <1E+01 <1E+01 <1E+02 Absent <1E+01 <1E+01 not detected Detected
CIN Milk <1E+01 4.5E+01 <1E+01 <1E+01 <1E+02 Absent <1E+01 <1E+01 not detected not detected
CIN Milk <1E+01 2.0E+01 <1E+01 <1E+01 <1E+02 Absent <1E+01 <1E+01 not detected not detected
DAK Milk <1E+01 2.0E+01 <1E+01 <1E+01 <1E+02 Absent <1E+01 <1E+01 not detected not detected
DAK Milk <1E+01 2.5E+02 <1E+01 <1E+01 <1E+02 Absent <1E+01 <1E+01 not detected not detected
DAK Milk <1E+01 2.0E+01 <1E+01 <1E+01 <1E+02 Absent <1E+01 <1E+01 not detected not detected
DAK Milk <1E+01 2.5E+01 <1E+01 <1E+01 <1E+02 Absent <1E+01 <1E+01 not detected not detected
DAK Milk <1E+01 3.0E+01 <1E+01 <1E+01 <1E+02 Absent <1E+01 <1E+01 not detected not detected
DAK Milk <1E+01 1.0E+01 <1E+01 <1E+01 <1E+02 Absent <1E+01 <1E+01 not detected not detected
OUA Milk <1E+01 4.0E+02 <1E+01 <1E+01 <1E+02 Absent <1E+01 <1E+01 not detected Detected
OUA Milk <1E+01 5.3E+02 <1E+01 <1E+01 <1E+02 Absent <1E+01 <1E+01 not detected not detected
BOB Milk <1E+01 1.5E+01 <1E+01 <1E+01 <1E+02 Absent 1.0E+01 <1E+01 not detected not detected
BOB Milk <1E+01 6.2E+02 <1E+01 <1E+01 <1E+02 Absent <1E+01 <1E+01 not detected not detected
BOB Milk <1E+01 2.0E+02 <1E+01 <1E+01 <1E+02 Absent <1E+01 <1E+01 not detected not detected
BOB Milk <1E+01 4.0E+01 <1E+01 <1E+01 <1E+02 Absent <1E+01 <1E+01 not detected not detected
BOB Milk <1E+01 3.8E+02 <1E+01 <1E+01 <1E+02 Absent <1E+01 <1E+01 not detected not detected
BOB Milk <1E+01 1.1E+02 <1E+01 <1E+01 <1E+02 Absent <1E+01 <1E+01 not detected not detected
BOB Milk <1E+01 2.3E+02 <1E+01 <1E+01 <1E+02 Absent <1E+01 <1E+01 not detected not detected
BOB Milk <1E+01 5.5E+02 <1E+01 <1E+01 <1E+02 Absent 1.0E+01 <1E+01 not detected not detected
BOB Milk <1E+01 4.3E+02 <1E+01 <1E+01 <1E+02 Absent 1.5E+01 <1E+01 not detected not detected
OUA Milk <1E+01 3.0E+02 <1E+01 <1E+01 <1E+02 Absent <1E+01 <1E+01 not detected not detected
OUA Milk <1E+01 3.3E+02 <1E+01 <1E+01 <1E+02 Absent <1E+01 <1E+01 not detected not detected
OUA Milk <1E+01 1.1E+02 <1E+01 <1E+01 <1E+02 Absent <1E+01 <1E+01 not detected not detected
OUA Milk <1E+01 2.2E+02 <1E+01 <1E+01 <1E+02 Absent <1E+01 <1E+01 not detected not detected
OUA Milk <1E+01 4.1E+02 <1E+01 <1E+01 <1E+02 Absent <1E+01 <1E+01 not detected not detected
OUA Milk <1E+01 2.8E+02 <1E+01 <1E+01 <1E+02 Absent 6.0E+01 <1E+01 not detected not detected
OUA Milk <1E+01 3.6E+02 <1E+01 <1E+01 <1E+02 Absent <1E+01 <1E+01 not detected Detected
OUA Milk <1E+01 1.8E+02 <1E+01 <1E+01 <1E+02 Absent <1E+01 <1E+01 not detected not detected
OUA Milk <1E+01 2.0E+02 <1E+01 <1E+01 <1E+02 Absent <1E+01 <1E+01 not detected not detected
OUA Milk <1E+01 1.7E+02 <1E+01 <1E+01 <1E+02 Absent <1E+01 <1E+01 not detected not detected
OUA Milk <1E+01 1.7E+02 <1E+01 <1E+01 <1E+02 Absent 1.0E+01 <1E+01 not detected not detected
OUA Milk <1E+01 3.2E+02 <1E+01 <1E+01 <1E+02 Absent <1E+01 <1E+01 not detected not detected
OUA Milk <1E+01 2.2E+02 <1E+01 <1E+01 <1E+02 Absent <1E+01 <1E+01 not detected not detected
NIA Milk <1E+01 2.2E+02 <1E+01 <1E+01 <1E+02 Absent 1.0E+01 <1E+01 not detected not detected
NIA Milk <1E+01 1.4 E+02 <1E+01 <1E+01 <1E+02 Absent <1E+01 <1E+01 not detected not detected
NIA Milk <1E+01 2.2E+02 <1E+01 <1E+01 <1E+02 Absent 1.0E+01 <1E+01 not detected not detected
NIA Milk <1E+01 1.9E+02 <1E+01 <1E+01 <1E+02 Absent <1E+01 <1E+01 not detected not detected
NIA Milk <1E+01 1.6 E+02 <1E+01 <1E+01 <1E+02 Absent 2.0E+01 <1E+01 not detected not detected
Open in a new tab

NIA: Niangoloko; CIN: Cinkansé; DAK: Dakola; BOB: Bobo and OUA: Ouagadougou.

Fig 2 summarizes the overall appreciation of all samples according to cities. Ouagadougou has the highest number of samples and the highest number of not satisfactory (7.9%). Off set Dakola, all the other localities showed at least one sample that is not satisfactory.

Fig 2. Appreciation according to cities.

Fig 2

Open in a new tab

The Fig 3 gives an overview of the appreciation of the samples according to their nature. The milk samples represent the highest number of samples, 43 out of 101 (42.57%). All samples showed at least one case that is not satisfactory. Milk powder and rice with sauce recorded the highest cases of not satisfactory at equal value, i.e., 3.96%.

Fig 3. Appreciation according to samples.

Fig 3

Open in a new tab

Depending on the profile of the microorganism sought in the overall samples, the total aerobic mesophilic flora was present in 93.07%, yeast and mould in 24.75%, total coliforms in 9.90%, thermotolerant coliforms in 6.93%, E. Coli in 1.98% and coagulase-positive staphylococci in 0.99%. Bacillus cereus was present in 9.30% of milk sample only. Neither Salmonella and anaerobic sulfito reductive (ASR) nor Clostridium perfringens were detected in any samples.

Discussion

The control of foodborne pathogens is an essential measure in preventing the appearance and spread of foodborne diseases in the population [20]. According to FAO (2009), unsafe food poses global health threats, endangering everyone; infants, young children, pregnant women [2]. Foods submitted to this study feed millions of low-income persons daily and therefore must be of very good nutritional and microbiological quality.

Despite the relatively poor sale environment hygiene noticed on the field; these foods were in general, microbiologically safe as only 11.88% were not satisfactory according to the standards used. Satisfactory results of street food were reported with breakfast and snack foods in Ghana [5], with meat and chicken stews and maizemeal porridge.in South Africa [21]. Most of the unacceptable limits derived from the total viable counts where microorganisms were present in 93,07% of samples, independently of their pathogenicity and the presence of coliforms. We can hypothesize that the total viable numbers, might come from all sources surrounding the foods, mostly from air helped by wind. The highest total viable counts recorded was 2.4x105 and was found in rice with sauce. Published papers report high total viable counts in street foods from 105 to 109 CFU/g [13, 22, 23]. According to previous study reported by [24] many foods provide an environment conducive to microbial growth, and indicator counts in such foods may reflect the time and conditions of storage. Otherwise, total viable counts cannot be used as a safety indicator, as there is generally no correlation between its value and the presence of pathogens or their toxins [24]. Except milk samples, all food samples submitted to our study undergo heating step that should normally reduce the microorganism population. That might be one of the reasons, we found out low total viable counts as compared to other studies as well as the total flora is an indication of good conservation of hot or cold chain. Microorganisms detected seems to have post contamination origin due to food and material handling. Street foods contamination mainly occur through hands [1, 6, 11, 25]. Moreover, the presence of indicator bacteria in ready-to-eat food, although not inherently a hazard, can be indicative of poor practice that may be poor quality of raw materials or food components; undercooking; cross-contamination; poor cleaning and poor temperature and time control [26]. The presence of thermotolerants coliforms and total coliforms respectively at 6.93% and 9.90%, in the study samples confirm these finding of post-processing contamination. The thermotolerant coliforms have the same properties as the total coliforms at the difference that lactose fermentation occurred at 44.5°C ± 0.5. However, coliforms are known to be a possible fecal contamination indicator. Their presence in food suggests the potential presence of other enteric bacteria that can be pathogens. E. coli were detected in 1.98% (2/101) of study samples specifically in bean and paste samples from Ouagadougou city. Their presence in heat treated foods might therefore signify inadequate cooking or post-processing contamination. Samples collected during the holding period after the food had already been exposed to high temperature processing, any presence of E. coli could only be attributed to faecal contamination from the hands of food handlers and/or from contaminated working surfaces and utensils [7]. Therefore, special attention should be paid to the street food chain with reference to the 5Ms (Main œuvre, Matière, Milieu, Matériels et Méthode) as decreed in the Codex Alimentarius. In addition, all food handlers must pay particular attention to their personal hygiene and hand washing after handling raw food and after using the toilet.’

Coagulase-positive staphylococci were detected in a bean sample of Ouagadougou at the level of 2.6x102 CFU/g. Staphylococcus aureus is considered the third most important cause of food-borne diseases in the world [27]. The main reservoir of staphylococci in humans is the nostrils, although staphylococci can also be found on hand [1]. One might think that Coagulase-positive staphylococci contamination of our bean sample comes from handling, perhaps because of more frequent hand contact during preparation and serving. Staphylococcal food poisoning is one of the most common food-borne diseases in the world following the ingestion of staphylococcal enterotoxins that are produced by enterotoxigenic strains of coagulase-positive staphylococci, mainly Staphylococcus aureus [28]. Coagulase-positive staphylococci have been found in a large number of commercial foods by a wide range of investigators [7, 9, 14, 22, 23, 27] but they appear to be more present with high numeration as compared to our results.

Yeasts and molds are commonly enumerated in foods as quality indicators and they have no predictive value for the occurrence of toxigenic fungi or other pathogens [24]. They are responsible of food spoilage when these foods are exposed to ambient condition without any protection. This study exhibits 24.75% of yeast an molds contamination that load varying from 1.0x10 to 1.6x104 CFU/g. The presence of yeasts and molds in heat-treated foods might also has its roots in inadequate cooking, post-processing contamination, cross-contamination or even poor quality of raw materials. Previous studies find out similar results on yeast load varying from 1.2 up to 5.2 logCFU/g while assessing the microbiological quality of ethnic street foods in the Himalayas [29].

Control parameters applied to milk samples differ from those applied to the others samples as Anaerobic Sulfito-Reductive bacteria (ASR), Clostridium perfringens and Bacillus cereus were also searched. Large numbers of Bacillus cereus are needed to cause illness either by releasing toxin into the food prior to consumption (emetic syndrome) or by producing a different toxin or toxins in the gut after eating the food (diarrheal syndrome) [26]. Bacillus cereus was isolated from only four milk powder samples (9.30%). Milk powder samples submitted to this study were somehow reconditioned by the vendors. The predominance of Bacillus cereus was probably due to cross contamination of bacillus spores present at the conditioning environment. Similar results were obtained in South Africa where nine meat/chicken samples (10.3%) and 6 maizemeal porridge samples (5.3%) were positive for Bacillus cereus [21].

Dakola, Cinkansé and Niangologo localities, which are the border post cities with high traffic and where food handlers lack of hygiene facilities (water supply, food inspectors…) like Ouagadougou and Bobo, were expected to have a high contamination load. Surprisingly, Ouagadougou recorded the highest rates of not satisfactory sample followed by Cinkansé. It can be hypothesized that this might be due to the high number of Ouagadougou sampling (31.68%) as compared to the other samples.

The food safety indicators such as Salmonella, the Anaerobic Sulfito Reductive (ASR) and Clostridium perfringens were not detected in any of all samples. Similar results were found in South Africa while trying to determine the health risks associated with street food vending [21]. It appears that important hygiene measures are practiced by almost all food handlers and this is very encouraging. Furthermore, the overall microbiological quality and safety of foods submitted to this research study were within the acceptable limits. Even there is no data for comparison, one might speculate that the advent of covid-19 that has profoundly destabilized developing countries people and fundamentally changed their habits and behaviors might have contributed to reduce the contamination of food through handling. Indeed, the media fuss around handwashing with soap and the use of hydro-alcoholic gels have been accepted by Burkinabe around the country. One of this positive impact might be the reduction of microbial contamination through the hands.

The presence of the different type of microorganisms and the not satisfactoriness samples observed suggested a post contamination during food handling and the possible microbial attacks propagated from the surrounding environment. It is well known that infections caused by microorganisms can be reduced by maintaining correct hand hygiene. Thus, training and education can improve the knowledge of street food handlers and play an important role in risk mitigation. Specific attention should be given for storage and packing processes specific to each food is also required, and the control of water used for utensils and hands washing. That might be one of the best ways to assure constantly a good hygienic quality of street foods.

Conclusion

This research work highlighted that street food vendors of the study regions of Burkina Faso were able to produce relatively safe foods with low percentage of not satisfactory samples. A study that was necessary to be done, namely the quality of the meals that was normally consumes by common Burkinabe every day, especially in border areas and urban centers. The microbial quality of these foods was acceptable in general even some fecal indicators are still presents suggesting the possibility of potential presence of other enteric bacteria that can be pathogens. As the different part of the country share the same street foods habit, one could extrapolate those similar behavioral patterns may be found elsewhere within the whole country. Therefore, education and training of foods handlers is crucial to control potential food borne illness.

Supporting information

S1 Table. Sample GPS site.

(DOCX)

Click here for additional data file. (50.3KB, docx)
S1 File. Raw data.

(XLSX)

Click here for additional data file. (95.1KB, xlsx)

Acknowledgments

This work was initiated by the PAASME-UE project (“Productions et analyses des données pour améliorer la santé de la mère et de l’enfant au Burkina Faso”) in collaboration with the INSP.

At the end of this work, it is important to thank:

  • The National Institute of Public Health (INSP) for the scientific collaboration;

  • The Health Research Ethics Committee for authorizing the conduct of this study;

  • The Regional Health Directorates of the Centre, Hauts-Bassins, Cascades and Centre-East regions for authorizing the conduct of this study;

  • The populations of the Centre, Hauts-Bassins, Cascades, Centre-East and Centre-South regions for their collaboration.

Data Availability

All relevant data are within the paper and its Supporting information files.

Funding Statement

This research project is jointly implemented by the National Institute of Public Health and the National Public Health Laboratory. It was fully funded by the European Union (EU) under number FED/2019/407-596 The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Grant Recipient: Pr. Elie KABRE.

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Decision Letter 0

Guadalupe Virginia Nevárez-Moorillón

24 Oct 2021

PONE-D-21-30741Microbiological quality assessment of five common foods sold at different points of sale in Burkina-FasoPLOS ONE

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Reviewer #2: Yes

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4. Is the manuscript presented in an intelligible fashion and written in standard English?

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Reviewer #1: Yes

Reviewer #2: No

**********

5. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: The results do not support the discussion. The description of the samples should be completed, number of outlets, number of samples per outlet.....

The statistical analysis should be extended, certainly in the form of distribution (mean, median...) for a discussion on the level of hygiene of street food, by localities, by type of food...

It is also necessary to describe and justify the choice of the hygiene indicators chosen (production hygiene, hand hygiene...) to reinforce the discussion.

Comments have been attached

I am not an English speaker

Reviewer #2: Microbiological quality assessment of five common foods sold at different

points of sale in Burkina-Faso

The study is important from food safety perspectives where microbiological quality assessment has been focused on five different foods in five regions of Burkina Faso. The study is interesting though the sample size is not big enough to draw a conclusion about the food safety issue in different areas of Burkina Faso. The abstract of the manuscript is incomplete considering the findings as there is a lack of information such sampling localities, foods sampling sites (restaurants or street food), bacterial count (colony forming unit, CFU) etc. Besides, how many samples were contaminated with hygiene and safety indicator organisms? In methods, EMB agar is not selective for only E. coli, other gram-negative bacteria might grow. How did author confirm E. coli colony through EMB agar culture? There is no cfu count limit of each parameters tested in methods sections. The results were described partially and no information about the count of hygiene and safety indicators in text. The abstract shows that 11.88% foods are satisfactory in terms of microbiological standards where the results show 24% food samples were contaminated with yeast and molds, which is contradictory. In my opinion, this manuscript is not well organized. We have observed many spelling mistakes and grammatical errors throughout the manuscripts. The following comments should be addressed throughout the manuscript:

­ All percentage data should be provided with number. e.g. 43 (13%) or 13% (n=43).

­ The word ‘satisfactory/appreciation was used in multiple places of the manuscript but there is no definition of it. Is it according to international food safety criteria or guidelines?

­ The sample collection method was not described in the manuscript, only the sites of collection and sample types were mentioned.

­ In line 20, 101 is not required to write.

­ In line 23 & 24, ‘All samples were analyzed under ISO methods’ should be ‘Samples were tested according to ISO guidelines for all parameters.

­ Sampling period was not mentioned in ‘Materials and methods’ section.

­ In line 23, ‘Bacillus cereus were checked too’ should be ‘Bacillus cereus were also tested for contamination’.

­ In line 30, recorded” should be placed in lieu of “record”

­ In line 39-42, there is no reference for “According to……diarrhea to cancers” statement.

­ Line 59: “Illnesses” should be placed in lieu of “illness”.

­ Line 66-68 “In developing countries…..capital is required” is not clear to me. Rewording is required. Drove in the sentence should be driven.

­ Lin 71, not proper style of citation. Suggestion: according to previous study or something like that.

­ Line 78: Common” should be placed in lieu of “commons

­ Line 90: are should be were.

­ In line 92, ‘Figure 1 indicated the sampling localities.’ Should be ‘Figure 1. Sample collection sites in the map of Burkina Faso.’

­ Line 97, parameters name should be mentioned. And “are” should be “were”.

­ Line 100-101, homogenized in water and again homogenized in mixer bag. How many times you homogenized?

­ In line 101, add time and rotation per minute for homogenization in bag mixer.

­ In line 102, ‘with in’ should be ‘with’.

­ Line 107, what is PCA?

­ In line 108, replace ‘was’ with ‘were’.

­ In line 108, 112, 116, 121 it was not mentioned why the plates with low number of colonies were selected.

­ In line 112, ‘Only the Petri dish’ should be ‘culture plates’

­ In line 116, ‘Only the Petri dish’ should be ‘culture plates’.

­ Line 124, what is IMViC?

­ Line 128, positive clones or colonies? What is BBLTM?

­ In line 129, remove ‘agar’ after ‘(EMB)’ and ‘France’ should be in the bracket.

­ In line 130, “was used”: should be written.

­ Footnote is missing for table 2. what is m or M? what is UFC?

­ Use ‘CFU/g’ instead of in ‘UFC/g’ throughout the manuscript according to ISO guidelines.

­ What is the use of statistical analysis in Methods section? Application of significance test described in study analysis is missing in entire manuscript. Suggestion: please remove this form methods.

­ In line 134, they mentioned sesame seeds but they are not using any sesame samples. please remove sesame.

­ In line 142, ‘purified on’ should be ‘streaked onto’.

­ In line 142, remove ‘then submitted to’ and add ‘were performed using API 20E (BioMérieux, France) test’. How many colonies were undergone for API 20E biochemical tests for each parameter. Please mention in detail in the methods section.

­ In line 144, “key” and “included” should be used instead of “Key” and “including”

­ In line 145, replace ‘H2S’ with ‘H2S’.

­ In line no. 149 pepton should be replaced with peptone.

­ In line 150, replace ‘seeded’ to ‘spread’.

­ In line 157, remove ‘full stop’ after ‘(Liofilchem diagnostic, Italy)’.

­ In line 175, it was not defined what appreciation criteria is.

­ Line 188, please mention criteria of what? is it food safety criteria according to international guidelines or regulation? which food items were found to be contaminated?

­ Line 194, it is difficult to say pathogenic e. coli without performing molecular test like PCR.

­ In Table 3, data for all samples is not necessary to present in details. Data could be presented graphically. Title of Table 3 is not complete, it should be more elaborative.

­

­ In line 205, “one sample” should be written instead of “sample one”

­ Line 210, what do mean by “the milk samples represent the highest percentage i.e., 42.57%”.

­ In line no. 211 of result section “record” should be “recorded”

­ Line 217, how 11.88% food samples were satisfactory where 24.7% were contaminated with yeast and molds.

­ Reference missing in the statement “Total….wind” from line 232-234 .

­ Line 235, 105 up to109 should be 105 to109

­ Line 236, [24] report that…. This is not appropriate style of citing. Suggestion: according to previous report or something like that.

­ In line no 239 of discussion section “Foods samples” should be “food samples”.

­ In line 239, it should be written Except instead of Excepted

­ In line 247, it will be 6.93% and 9.90%. entire manuscripts had these errors.

­ Line 250, Coliforms should be coliforms.

­ Entire manuscripts show percentage of satisfactory or appreciation. Number of samples found to be contaminated should be mentioned in the parentheses along with %.

­ Line 253, signifies should be signify.

­ Line 254, According to [6] is not proper style of referencing.

­ There was no reference against the statement “That should…..other studies”; line 241-242.

­ The rationale behind the statement “That suggest the …..pathogens” (line 251-252) was not clear.

­ Unit of the count was missing in line 262 after 2.6×102

­ In line 269 it should be written, they appear to be present in higher number….

­ In line 277, it should be written “previous studies find out….”

­ In line 284, it will be 9.30%.

­ Line 284 and 287, either word or number should be written. Ex. Four or 4. No need to write both.

­ Line 290, expertise..?

­ Line 317-319: The statement “A void that was necessary…. areas and urban center” is not clear.

­ Line 324-326: too ambitious conclusion which is difficult to evaluate from this study findings. Suggestions: removed.

­ They have stated “One might believe that the advent of covid-19 that has profoundly destabilized developing countries people and fundamentally changed their habits and behaviors might have contributed to reduce the contamination of food through handling.” from line 300-302, but they don't have any data to compare with the situation before covid 19.

------------The End-----------

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Reviewer #1: No

Reviewer #2: Yes: Dr. Mohammed Badrul Amin

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PLoS One. 2022 Apr 14;17(4):e0258435. doi: 10.1371/journal.pone.0258435.r002

Author response to Decision Letter 0

18 Jan 2022

Answers

The authors would like to deeply thanks all the PLOS ONE board member for the best platform they provide for microbiological sciences promotion. Without any favor, it will be and honor for us if this manuscript is accepted for publication in PLOS ONE.

Authors also deeply thank the two reviewers for their valuable and pertinent critics that aim to improve the quality of the manuscript. We are already satisfied with the work done and will tried to bring answers for all the remarks they pointed out. Authors hope these answers will get reviewers approval.

Thank you very much

Reviewer 1

All observations of reviewer 1 have been taken into account

Line 210, “the milk samples represent the highest percentage i.e., 42.57%” mean that portion of milk samples over all samples is 42.57%

Line 217, how 11.88% food samples were satisfactory where 24.7% were contaminated with yeast and molds: 11.88% is the overall appreciation and 24.7% is appreciation focused in only yeast and molds.

Reviewer 2

All observations of reviewer 2 have been taken into account.

L.24-26: There is no scientific reason why the percentage of contaminated food is expressed to the nearest hundredth.

L.107, L.116...The standards mentioned have been cancelled or revised. Our laboratory still used these standards because we did not buy new standard yet.

A.185: Have you verified the homogeneity within each type of food, since the points of sale are different: we did not verify the homogeneity within each type of food and I think it will not be possible to do so.

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Decision Letter 1

Guadalupe Virginia Nevárez-Moorillón

16 Feb 2022

Microbiological quality assessment of five common foods sold at different points of sale in Burkina-Faso

PONE-D-21-30741R1

Dear Dr. COMPAORE,

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Acceptance letter

Guadalupe Virginia Nevárez-Moorillón

6 Apr 2022

PONE-D-21-30741R1

Microbiological quality assessment of five common foods sold at different points of sale in Burkina-Faso

Dear Dr. Compaore:

I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department.

If your institution or institutions have a press office, please let them know about your upcoming paper now to help maximize its impact. If they'll be preparing press materials, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information please contact onepress@plos.org.

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on behalf of

Dr. Guadalupe Virginia Nevárez-Moorillón

Academic Editor

PLOS ONE

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