Occurrence of Escherichia coli, Salmonella spp. and Staphylococcus aureus and Antimicrobial Susceptibility Profile in Locally and Commercially Produced Yogurt Sold in Addis Ababa, Ethiopia

doi:10.21203/rs.3.rs-3644589/v1

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Occurrence of Escherichia coli, Salmonella spp. and Staphylococcus aureus and Antimicrobial Susceptibility Profile in Locally and Commercially Produced Yogurt Sold in Addis Ababa, Ethiopia

https://doi.org/10.21203/rs.3.rs-3644589/v1

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The present study was conducted to assess the occurrence and antimicrobial susceptibility profile of Escherichia coli and Salmonella spp. and Staphylococcus aureus isolates from locally and commercially produced yogurt sold in Addis Ababa, Ethiopia. A total of 40 yogurt samples (20 commercially and 20 locally produced) were collected from retail markets. Samples were cultured according to standard microbiology techniques, and the Vitek 2XL compact systems (bioMérieux) were used both to confirm the presumptive colonies and antimicrobial sensitivity testing following the manufacturer’s instructions. E. coli and Salmonella spp. were found to be 9 (45%) and 2 (10%) and 5 (25%) and 1 (5%) of locally and commercially produced yogurt samples, respectively. However, S. aureus was not detected in any of the yogurt samples. Interestingly, 7–28% of E. coli isolates were resistant to ampicillin, amoxicillin, cephalexin, cefalotin, cefpodoxime, enrofloxacin, marbofloxacin, pardofloxacin, doxycycline, tetracycline, nitrofurantoin, chloramphenicol and cotrimoxazole (thrimethoprim-sulfamethoxazole). Similarly, Salmonella spp. isolates were resistant to ampicillin, pardofloxacin, doxycycline, and tetracycline. Our findings indicate that. E. coli and Salmonella spp. isolates with a high percentage of antimicrobial resistance highlight the health risk for consumers. Therefore, yogurt producers and handlers need to place more emphasis on quality assurance.

antibiotic

E. coli

Salmonella spp.

Vitek 2XL

yogurt

In Ethiopia, food safety regulations are fragmented [1, 2, 3], and there is a lack of surveillance systems for monitoring foodborne pathogens to ensure food safety [2, 3]. Yogurt is a fermented product that is the most popular dairy product worldwide [4] and a good source of probiotics [5], but very careful processing is essential for the production of safe and high-quality yogurt [6, 7]. Essentially, even a little contamination may deteriorate the quality of yogurt, which may have negative effects on consumer health [6, 7]. A previous study conducted in Ethiopia has also indicated that yogurt is a potential reservoir for different pathogenic microorganisms of public health concern [8, 9, 10, 11, 12], and fermentation of yogurt does not control this pathogen [13]; therefore, yogurt can be a potential health hazard if it is prepared from milk contaminated with this pathogen and does not show any off odor [13]. Thus, it is difficult to depend on sensory evaluation as a sign of safety [13].

Studies and observations have indicated that in recent years, widespread overuse and misuse of antimicrobial agents in food animal production have contributed to the development of numerous bacteria with multiple drug resistance patterns that have emerged in Ethiopia [14, 15, 8, 9, 10, 11, 12, 16]. Thus, the prevalence of major foodborne pathogens and antimicrobial resistance patterns continues to be a topic of concern in the rapidly growing Ethiopian dairy supply chain [3]. Hence, the research community considers this a priority work area, and in this context, accelerated efforts to develop rapid and reliable alternative methods for bacterial identification and antimicrobial susceptibility testing [17, 18] of dairy products are essential. In this regard, the Vitek 2XL compact system has been gaining ground in the ease of execution and improves reporting times for microbe identification and AST results in wastewater treatment plant effluents [17]. However, currently, usage of this system in yogurt samples has been minimal, and to the best of our knowledge, this study represents the first Vitek 2XL compact system used to assess the occurrence and antimicrobial susceptibility profile of Escherichia coli and Salmonella spp. and Staphylococcus aureus isolates from locally and commercially produced yogurt sold in Addis Ababa, Ethiopia.

2.1. Description of Study Area

The study was conducted in Addis Ababa, the capital city of Ethiopia, from February 2022 to May 2022. Addis Ababa lies in the central highlands of Ethiopia at an altitude of 2350 m above sea level and is located at 9° 1′48″N and 38° 44′ 24″E. The average annual temperature

is 16.3°C, whereas the average annual precipitation is 1143 mm. The relative humidity varies from 70–80% during the rainy season and 40–50% during the dry season, and there is bimodal rainfall with an average of 1800 mm [18].

2.2. Study Design and Sample Collection Procedure

A total of 20 commercially produced yogurt samples represent 5 different brands with 4 samples per brand purchased from supermarkets using purposive sampling techniques. Similarly, 20 locally produced yogurt samples were collected through random sampling techniques from retail dairy product vendors. The samples were collected on 15 daily bases for three months from February 2022 to May 2022. Commercially produced yogurt was kept in silver/glass vessels until consumption. Approximately 300 ml of each yogurt sample was collected aseptically in sterile screw-capped bottles. Strict aseptic procedures were followed when collecting yogurt samples to prevent contamination. The bottles containing samples were labeled and transported to the laboratory of animal products, veterinary drugs, and feed quality testing center (APVDFQTC) in Addis Ababa using an icebox and stored at + 40°C until laboratory work was conducted. For ethical considerations, the samples were coded blindly throughout the study.

2.3. Isolation and Identification of Escherichia coli

Approximately 10 gm of yogurt was preenriched in 90 ml of sterile buffered peptone water (BPW) (Oxoid, UK) to yield a 1/10 dilution and incubated at 37°C for 24 hr. A loop full of the incubated culture was streaked onto MacConkey agar (Oxoid, UK) and incubated at 37°C for 24 hr. A single pink colony from the MacConkey agar plate was subcultured on Eosin Methylene Blue (EMB) agar (Oxoid, UK) and incubated at 37°C for 24 hr. The presumptive E. coli colonies (metallic sheen) were transferred onto nutrient agar (Oxoid, UK) and incubated at 37°C for 24 hr. A pure isolated single colony from a nutrient agar plate was confirmed using the automated Vitek 2XL compact system using Gram Negative (GN) cards with 47 biochemical tests following the manufacturer’s instructions (BioMérieux).

2.4. Isolation and Identification of Staphylococcus aureus

Approximately 10 gm of yogurt was preenriched in 90 ml of sterile buffered peptone water (BPW) (Oxoid, UK) to yield a 1/10 dilution and incubated at 37°C for 24 hr. A loop full of suspension was taken from the incubated BPW culture, streaked on blood agar and incubated at 37°C for 24 hr. A single pink colony was taken from incubated blood agar and subcultured on mannitol salt (MSA) (Oxoid, UK) and incubated at 37°C for 24 hr. The presumptive S. aureus colonies (golden yellowish) were transferred onto nutrient agar (Oxoid, UK) and incubated at 37°C for 24 hr. A pure isolated single colony from a nutrient agar plate was confirmed using the automated Vitek 2XL compact system using Gram-Positive (GP) cards with 43 biochemical tests following the manufacturer’s instructions (bioMérieux).

2.5. Isolation and identification of Salmonella species

Approximately 25 gm of sample was preenriched in 225 ml of buffered peptone water (BPW) to yield a 1/10 dilution and incubated at 37°C for 24 hr. Then, the selective enrichment media was prepared by mixing 1 ml of the preenrichment culture with 10 ml of Rappaport Vassiliadis (RVS) broths (Oxoid, UK) and inoculated at 41.5°C for 24 hr. A loop full culture from selective enrichment broth was transferred to selective agar media (xylose lysine deoxycholate agar (XLD) agar (Oxoid, UK)) and incubated at 37°C for 24 hr. Presumptive Salmonella colonies (reddish or pink) were transferred onto nutrient agar (Oxoid, UK) and incubated at 37°C for 24 hr. A pure isolated single colony from a nutrient agar plate was confirmed using the automated Vitek 2XL compact system using Gram Negative (GN) cards with 47 biochemical tests following the manufacturer’s instructions (bioMérieux).

2.6. Antimicrobial Susceptibility Test (AST) with the Vitek 2XL compact system

AST-GN96 (E. coli) and AST-G79 (Salmonella spp.) cards were used for AST with a fully automated Vitek 2XL compact system following the manufacturer’s instructions. E. coli and Salmonella spp. were suspended in 3 milliliters (ml) of sterilized saline (aqueous 0.45–0.50% NaCl, pH 4.5-7.0) using different clear polystyrene tubes for each target bacteria and thoroughly mixed. The turbidity of the bacterial suspensions was adjusted with a DensiCHEK Plus meter (turbidity meter) to match that of a McFarland 0.5–0.63 standard. Then, AST GN cards were used for E. coli and Salmonella spp. scanned by a barcode scanner, and the straw of the cards was inserted into the empty tubes in the slot of the cassette next to the bacterial suspension. All the necessary information about the taste sample was entered into the Vitek computer through Vitek 2 FLEXprep data entry, and the two priority bacteria identified were selected from the database. The cassette holding the suspension tubes with cards was loaded into the Vitek XL compact system instrument at the cassette load station. Then, the Vitek 2XL compact system automatically proceeds to process the cards once all the cards are loaded. The results were interpreted by the Vitek database, and the final results were obtained automatically. The susceptibility results of bacteria were available in less than 19 hrs. The break point of antimicrobial activity was expressed numerically in µg/ml as the minimum inhibitory concentration (MIC) for AST/AMR interpretation. AST results were interpreted following the Clinical and Laboratory Standard Institute (CLSI) guidelines [19]. The results interpretations for AST/AMR given by the Vitek 2XL compact system were Susceptible (S), Intermediate (I), and Resistant (R).

2.7. Data management and analysis

All collected data were entered into a Microsoft Excel Sheet and analyzed using SPSS version 21. Accordingly, descriptive statistics such as percentages and frequency distribution were used to describe the bacterial isolates, antimicrobial susceptibility was expressed as percent of resistant, intermediate, or susceptible, and the chi-square (x²) test was applied to assess the association.

3.1. The occurrence of Escherichia coli, Salmonella spp. and Staphylococcus aureus

Out of the total 40 yogurt samples, 14 (35%) were found to be positive for E. coli. The sample-based positivity for locally and commercially produced yogurt samples was 9 (45%) and 5 (25%), respectively. There was no significant difference (χ² = 1.785; p = 0.185) between locally and commercially produced yogurt samples (Table 1). Similarly, out of the total 40 yogurt samples, 3 (3.7%) were found to be positive for Salmonella spp. The sample-based positivity for locally and commercially produced yogurt samples was 2 (10%) and 1 (5%), respectively. There was no significant difference (χ² = 0.360; p = 0.548) between locally and commercially produced yogurt samples (Table 1). However, S. aureus was not detected in any of the yogurt samples.

Table 1

Occurrence of *Escherichia* coli, Salmonella spp. and *Staphylococcus aureus* from locally and commercially produced yogurt sold in Addis Ababa, Ethiopia
Sample type	Number tested	E. coli		Salmonella spp.		S. aureus
Sample type	Number tested	Positive	Negative	Positive	Negative	Positive	Negative
Locally yogurt	20	9(45%)	11(55%)	2(10%)	18(90%)	0	20(100%)
Commercially yogurt	20	5(25%)	15(75%)	1(5%)	19(95%)	0	20(100%)
Total	40	14(35%)	26(65%)	3(7.5%)	37(92.5%)	0	100%
χ² (p- value)		1.785(0.185)		0.360(0.548)

3.2. Antimicrobial Susceptibility in Escherichia coli and Salmonella spp.

Interestingly, the Antimicrobial Susceptibility test indicated that seven (7%) to 28% of E. coli isolate were resistant to Ampicillin 3(21%), Amoxicillin(Clavulanic acid) 1(7%), Cephalexin 2(14%), Cefalotin 2(14%), Cefpodoxime 1(7%), Enrofloxacin 1(7%), Marbofloxacine 1(7%), Pardofloxacin 1(7%), Doxycycline 2(14%), Tetracycline 4(28%), Nitrofurantoin 2(14%), Chloramphenicol 3(21%) and Cotrimoxazole(Thrimethoprim-Sulfmethoxazole) 3(21%). However, no isolate was resistant to cefovecin, ceftiofur, amikacin, or neomycin. The isolates also showed intermediate resistance to amoxicillin (7%), cefalotin (7%), cefpodoxime (7%), cefovecin (14%), ceftiofur (14%), amikacin (7%), neomycin (14%), enrofloxacin (7%), doxycycline (14%) and chloramphenicol (7%). In addition, 14 (100%) isolates were susceptible to gentamicin (Table 2). In the current study, all Salmonella spp. isolate were resistant to ampicillin 3 (100%), pardofloxacin 3 (100%), doxycycline 3 (100%), and tetracycline 3 (100%). However, 67% of Salmonella spp. isolates were susceptible to amoxicillin (clavulanic acid), cefpodoxime, cefovecin, ceftiofur and neomycine (Table 2).

Table 2

Antimicrobial Susceptibility in *E. coli* and Salmonella spp. isolates from locally and commercially produced yogurt sold in Addis Ababa, Ethiopia
Antimicrobials	Species	Susceptible	Intermediate	Resistant
Ampicillin	E. coli	11(79%)	-	3(21%)
Ampicillin	Salmonella spp	-	-	3(100%)
Amoxicillin/Clavulanic acid	E. coli	12(86%)	1(7%)	1(7%)
Amoxicillin/Clavulanic acid	Salmonella spp	2(67%)	-	1(33%)
Cephalexin	E. coli	12(86%)	-	2(14%)
Cephalexin	Salmonella spp	1(33%)	-	2(67%)
Cefalotin	E. coli	11(79%)	1(7%)	2(14%)
Cefalotin	Salmonella spp	1(33%)	-	2(67%)
Cefpodoxime	E. coli	12(86%)	1(7%)	1(7%)
Cefpodoxime	Salmonella spp	2(67%)	1(33%)	-
Cefovecin	E. coli	12(86%)	2(14%)	-
Cefovecin	Salmonella spp	2(67%)	1(33%)	-
Ceftiofur	E. coli	12(86%)	2(14%)	-
Ceftiofur	Salmonella spp	1(33%)	2(67%)	-
Amikacin	E. coli	13(93%)	1(7%)	-
Amikacin	Salmonella spp	1(33%)	-	2(67%)
Gentamicin	E. coli	14(100%)	-	-
Gentamicin	Salmonella spp	1(33%)	-	2(67%)
Neomycine	E. coli	12(86%)	2(14%)	-
Neomycine	Salmonella spp	2(67%)	1(33%)	-
Enorfloxacin	E. coli	12(86%)	1(7%)	1(7%)
Enorfloxacin	Salmonella spp	-	1(33%)	2(67%)
Marbofloxacine	E. coli	13(93%)	-	1(7%)
Marbofloxacine	Salmonella spp	1(33%)	1(33%)	1(33%)
Pardofloxacin	E. coli	13(93%)	-	1(7%)
Pardofloxacin	Salmonella spp	-	-	3(100%)
Doxycycline	E. coli	10(72%)	2(14%)	2(14%)
Doxycycline	Salmonella spp	-	-	3(100%)
Tetracycline	E. coli	10(72%)	-	4(28%)
Tetracycline	Salmonella spp	-	-	3(100%)
Nitrofurantoin	E. coli	12(86%)	-	2(14%)
Nitrofurantoin	Salmonella spp	1(33%)	-	2(67%)
Chloramphenicol	E. coli	10(72%)	1(7%)	3(21%)
Chloramphenicol	Salmonella spp	1(33%)	-	2(67%)
Trimethoprim/sulfamethoxazole	E. coli	11(79%)	-	3(21%)
Trimethoprim/sulfamethoxazole	Salmonella spp	1(33%)	-	2(67%)

The present study revealed that the overall E. coli prevalence was 14 (35%) (Table 1). The prevalence of E. coli found by other authors in yogurt samples in Ethiopia is diverse. Most of the studies reported that the prevalence of E. coli was lower than that found in this study. Abebe et al., 2023 [8] analyzed 35 yogurt samples from Dessie and Kombolcha towns, Ethiopia, and detected E. coli in 5 (13.9%) samples. Gugsa et al., 2022 [9] studied 48 yogurt samples from Mekelle, Tigray, Ethiopia, and reported a prevalence of 11 (22.9%) and Bedasa et al., 2018 [10] reported a prevalence of 9/35 (25.71%) E. coli after analyzing 35 yogurt samples in and around Bishoftu, Central Ethiopia. Additionally, Muluken et al., 2016 [20] could not detect E. coli in the tested yogurt samples from Addis Ababa, Ethiopia. The difference might be the sample procedures and the detection methods employed for different studies. Its presence in yogurt indicates other enteropathogenic microorganisms that constitute a public health hazard [21]. A previous study also indicated that E. coli O157:H7 infections from dairy products (such as yogurt and cheese derived from raw milk) are more severe, have higher rates of hospitalization and hemolytic uremic syndrome, and occur more frequently in children than infections associated with beef consumption[22].

There are a limited number of reports on the prevalence of Salmonella spp. in yogurt in Ethiopia. However, a zero percent (0.0%) prevalence of Salmonella in yogurt was reported by [23] in Addis Ababa, Ethiopia. A study conducted by Addis et al.,2011 [14], Alemayehu et al.,200) [15], and Zewdu and Cornelius, 2009 [24] reported that the prevalence of Salmonella among individuals working on dairy farms in Addis Ababa was 13.63%, 6% and 7.6%, respectively. Food handlers, who may be carriers of Salmonella, are definite sources of contamination if they are not following basic hygienic principles during food handling [14, 24]. According to Ethiopian standards, the yogurt shall be free from pathogenic microorganisms and shall comply with the microbiological limit, and Salmonella must be absent [25]. It is generally accepted that the presence of any Salmonella in food should be regarded as a potential hazard to humans [14]. Therefore, the occurrence of Salmonella spp. in yogurt signifies a serious public health threat, as the practice of consuming raw dairy products in the study area is widespread [12]. Studies performed elsewhere have indicated that dairy items are important vehicles of Salmonella for raw consumers [26]. Previous studies indicated that Salmonella is inactivated during the fermentation of high-acid products such as yogurt in which the pH value is less than 4.55 [27]. However, lowering the pH to a level that is inactivated may cause unacceptable sensory quality due to overly sour tastes [13]. The prevalence values encountered in this study, as well as those reported in other studies in Ethiopia, clearly demonstrate that E. coli and Salmonella spp. are frequently detected in yogurt, are sometimes present in concentrations above the normative levels, and consequently may have adverse effects on consumer health [6, 7].

The result of tetracycline resistance was more frequently observed compared with the other antibiotics of E. coli isolates in this study, in agreement with the reports of Tadesse et al,. 2021 [28] (27.7%) and lower than the findings of Gugsa et al.,2022 [9] (41.7%), Messele et al.,2017 [29] (47.6%), Ahmed and Shimamoto,2015 [30] (80.6%), Disassa et al.,2017 [31] (81.8%), Ababu et al.,2020 [32] (63.63%), and Hailu,2020 [33] (60.61%) but was higher than the findings of Bekele et al.,2014 [34] (5.1%). Similar high levels of resistance to tetracycline in the current and previous studies could be due to the overuse of these antimicrobials for the treatment and prevention of various animal infections in the study area [12]. This study also revealed that E. coli isolates were sensitive to cefovecin at 86%, ceftiofur at 86%, amikacin at 93%, neomycine at 86%, enrofloxacin at 86%, marbofloxacine at 93% and pardofloxacin at 93%, which was in line with the reports of [35] from central Ethiopia. The result of the gentamicin susceptibility level (100%) of E. coli isolates in this study agrees with the reports of Ababu et al.,2020, [32] (100%) and is higher than the 81% reported by Kibret and Abera,2011 [36], Gugsa et al.,2022 [9] (91.7%), Bedasa et al.,2018[10] (82.5%), and Hailu,2020 [33] (81.82%). In the current study, gentamycin, amikacin, marbofloxacin, and pardofloxacin were found to be the most effective antimicrobials against E. coli isolates.

Interestingly, all Salmonella spp. isolated in the current study were 100% resistant to ampicillin, in line with previous reports from Addis Ababa [15]. The effectiveness of gentamycin in isolated Salmonella spp. in the current study is 33%, which is lower than that reported by 73.3%, 75%, and 100% by [15, 37, 38], respectively. The tetracycline resistance level of Salmonella spp. isolated (100%) was much higher than the 46.15% reported by [35] from central Ethiopia. Two out of the three isolates of Salmonella spp. resistance against chloramphenicol and cotrimoxazole (trimethoprim-sulfamethoxazole), which is higher than that of [39] from Bahir Dar, Ethiopia, [40] in Debre-Zeit and Addis Ababa, Ethiopia. As shown in Table 2, two out of three Salmonella spp. isolates were detected as susceptible to amoxicillin, cefpodoxime, cefovecin, and neomycine. However, only one out of three isolates was shown to be susceptible, which is incomparable with the study reported by [41] from Asella town, Ethiopia and the high level of resistance to gentamicin (75.6%) reported from Gondar, Northwest Ethiopia by [42]. Studies and observations conducted elsewhere in Ethiopia have also indicated that the increase in the proportion of antimicrobial-resistant strains could be due to the irrational use of antimicrobials and the inappropriateness of the prescription and dispensing methods in both the public veterinary and private health setups of the country [12, 43]. The scientific literature indicates that the presence of multidrug-resistant bacterial pathogens in ruminants, and consequently in dairy products, may cause drug-resistant infections in humans [14, 15, 8, 9, 10, 11, 12, 16].

Our findings indicate that E. coli and Salmonella spp. isolates with a high percentage of antimicrobial resistance highlight the health risk for consumers. Therefore, yogurt producers and handlers need to place more emphasis on quality assurance.

Acknowledgment

The authors would like to thank the Ministry of Ethiopia Agriculture and the Institute of Livestock Development for their financial support.

Competing interests

The authors declare that there is no financial or nonfinancial competing interest from anybody or the institute. We also want to assure you that we did not receive any technical assistance in developing the research concept or preparing the manuscript.

Authors’ contributions

The work reported in this manuscript was a component of a wider MSc study for MF. TW and UG were the university supervisors of the candidate. MF contributed to the writing of the research proposal and data collection. TW prepared the study design, data analysis and interpretation, and manuscript writing. UG contributed to research proposal writing and manuscript editing. All authors reviewed and agreed on the final draft of the manuscript.

Authors’ information

¹MF is an MSc student in the School of Animal and Range Sciences at Haramaya University, Ethiopia. ²Dr. Takele Wolkaro is an assistant professor in the School of Animal and Range Sciences at Haramaya University, Ethiopia, while ³Dr. Ulfina Galmassa is an associate professor at the Ethiopian Institute of Agricultural Research, Holeta Agricultural Research, Ethiopia

Availability of data and materials

The datasets used and/or analyzed during the current study available from the corresponding author on reasonable request

Ayalew H. Review on food safety system: Ethiopian perspective. Afr J Food Sci. 2013;7(12):431–40. https://doi.org/10.5897/ajfs2013.1064.
Birke W, Zawide F. Transforming Research Results in Food Safety to Community Actions: A Call for Action to Advance Food Safety in Ethiopia. Environ Ecol Res. 2019;7(3):153–70. https://doi.org/10.13189/eer.2019.070305.
Abdi K, Rolon ML, Aynadis T, Kindinew D, Vipham J, Kovac J, Ashagrie Z. Review of the prevalence of foodborne pathogens in milk and dairy products in Ethiopia. Int Dairy J. 2020;109:104762. https://doi.org/10.1016/j.idairyj.2020.104762.
Oliveira A, Alexandre EM, Coelho M, Lopes C, Almeida DP, Pintado M. Incorporation of strawberries preparation in yoghurt: Impact on phytochemicals and milk proteins. Food Chem. 2015;171:370–8.
Allgeyer LC, Miller MJ, Lee SY. Sensory and microbiological quality of yogurt drinks with prebiotics and probiotics. J Dairy Sci. 2010;93:4471–9.
Shah S, Ahmed A, Ahmad N. Role of packaging in consumer buying behavior. Int Rev Basic Appl Sci. 2013;1(2):35–41. https://doi.org/10.5267/j.msl.2019.11.040.
Wikström F, Williams H, Verghese K, Clune S. The influence of packaging attributes on consumer behavior in food-packaging life cycle assessment studies - A neglected topic. J Clean Prod. 2014;73:100–8. https://doi.org/10.1016/j.jclepro.2013.10.042.
Abebe E, Gugsa G, Ahmed M, Awol N, Tefera Y, Abegaz S, Sisay T. Occurrence and antimicrobial resistance pattern of E. coli O157:H7 isolated from foods of Bovine origin in Dessie and Kombolcha towns, Ethiopia. PLoS Negl Trop Dis. 2023;17(1). https://doi.org/10.1371/journal.pntd.0010706.
Gugsa G, Weldeselassie M, Tsegaye Y, Awol N, Kumar A, Ahmed M, Abebe N, Taddele H, Bsrat A. Isolation, characterization, and antimicrobial susceptibility pattern of Escherichia coli O157:H7 from foods of bovine origin in Mekelle, Tigray, Ethiopia. Front Veterinary Sci. 2022;9. https://doi.org/10.3389/fvets.2022.924736.
Bedasa S, Daniel S, Abraha A, Tesfanesh M. Occurrence and antimicrobial susceptibility profile of Escherichia coli O157:H7 from food of animal origin in Bishoftu town, central Ethiopia. Int J Food Contam. 2018;5(1). https://doi.org/10.1186/s40550-018-0064-3.
Deddefo A, Mamo G, Leta S, Amenu K. Prevalence and molecular characteristics of Staphylococcus aureus in raw milk and milk products in Ethiopia: a systematic review and meta-analysis. Int J Food Contam. 2022;9(1). https://doi.org/10.1186/s40550-022-00094-5.
Fikirte L, Haile A, Stringer A, Tadesse E. Prevalence and Antimicrobial Susceptibility Profile of Staphylococcus aureus in Milk and Traditionally Processed Dairy Products in Addis Ababa, Ethiopia. Biomed Res Int. 2021. https://doi.org/10.1155/2021/5576873.
Tsegaye M, Ashenafi M. Fate of Escherichia coli O157:H7 during the processing and storage of Ergo and Ayib, traditional Ethiopian dairy products. Int J Food Microbiol. 2005;103(1):11–21. https://doi.org/10.1016/j.ijfoodmicro.2004.12.006.
Zewdu E, Cornelius P. Antimicrobial resistance pattern of Salmonella serotypes isolated from food items and personnel in Addis Ababa, Ethiopia. Trop Anim Health Prod. 2009;41(2):241–9. https://doi.org/10.1007/s11250-008-9181-y.
Addis Z, Kebede N, Worku Z, Gezahegn H, Yirsaw A, Kassa T. Prevalence and antimicrobial resistance of Salmonella isolated from lactating cows and in contact humans in dairy farms of Addis Ababa: A cross-sectional study. BMC Infect Dis. 2011;11(1). https://doi.org/10.1186/1471-2334-11-222.
Kimera ZI, Mshana SE, Rweyemamu MM, Mboera LEG, Matee MIN. Antimicrobial use and resistance in food-producing animals and the environment: An African perspective. Antimicrob Resist Infect Control. 2020;9(1). https://doi.org/10.1186/s13756-020-0697-x.
Tshabuse F, Buthelezi N, Folami AM, Donnelly L, Swalaha FM. Rapid detection of drug-resistant Escherichia coli by Vitek 2 compact system. Water SA. 2022;48(4):450–6. https://doi.org/10.17159/wsa/2022.v48.i4.3941.
Ministry of Urban Development, Housing and Construction. : The Construction Industry Registration Final Draft Proclamation, Addis Ababa, Ethiopia 2013, 1–75. www.chilot.me.
Praça J, Furtado R, Coelho A, Correia CB, Borges V, Gomes JP, Pista A, Batista R. Listeria monocytogenes, Escherichia coli and Coagulase Positive Staphylococci in Cured Raw Milk Cheese from Alentejo Region. Portugal Microorganisms. 2023;11:322. https://doi.org/10.3390/microorganisms11020322.
Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing. CLSI supplement M100. Wayne, PA: Clinical and Laboratory Standards Institute; 2020. pp. 106–12.
Muluken AA, Cione E, Aquaro S. Microbiological Characteristics and Physico-chemical Parameters of Fermented Milk Product Ergo-A Traditional Yogurt Product of Ethiopia. Food Sci Qual Manage. 2016;49:42–5. .
Singh P, Prakash A. Isolation of Escherichia coli, Staphylococcus aureus and Listeria monocytogenes from milk products sold under market conditions at Agra region. Acta agriculturae Slovenica. 2008;92(1):83–8.
Heiman KE, Mody RK, Johnson SD, Griffin PM, Gould LH. Escherichia coli O157 outbreaks in the United States, 2003–2012. Emerg Infect Dis 2015. http://dx.doi.org/10.3201/eid2108.141364.
Tesfaw L, Taye B, Alemu S, Alemayehu H, Sisay Z, Negussie H. Prevalence and antimicrobial resistance profile of Salmonella isolates from dairy products in Addis Ababa, Ethiopia. Acad EdU. 2013;7(43):5046–50. https://doi.org/10.5897/AJMR2013.5635.
Alemayehu D, Molla B, Muckle A. Prevalence and antimicrobial resistance pattern of Salmonella isolates from apparently healthy slaughtered cattle in Ethiopia. Trop Anim Health Prod. 2003;35(4):309–19. https://doi.org/10.1023/A:1025189204496.
Ethiopian standard. of Yogurt and sweetened yogurt: Specification 2021, ES 3468.
Jay JM, Loessner MJ, Golden DA. Foodborne gastroenteritis caused by Salmonella and Shigella. Mod Food Microbiol 2005, 619–36.
Varnam AH, Evans MG. Food borne pathogens. An illustrated text Chap. 13: England wolfe publishing Ltd. ISBN: 1991. https://books.google.com.et/books?id=BLdyQgAACAAJ.
Tadese ND, Gebremedhi EZ, Moges F, Borana BM, Marami LM, Sarba EJ, Abebe H, Kelbesa KA, Atalel D, Tessema B. Occurrence and antibiogram of escherichia coli O157:H7 in raw beef and hygienic practices in abattoir and retailer shops in ambo town, Ethiopia. Veterinary Med Int. 2021. https://doi.org/10.1155/2021/8846592.
Messele YE, Abdi RD, Yalew ST, Tegegne DT, Emeru BA, Werid GM. Molecular determination of antimicrobial resistance in Escherichia coli isolated from raw meat in Addis Ababa and Bishoftu, Ethiopia. Ann Clin Microbiol Antimicrob. 2017;16(1). https://doi.org/10.1186/S12941-017-0233-X.
Ahmed AM, Shimamoto T. Molecular analysis of multidrug resistance in Shiga toxin-producing Escherichia coli O157: H7 isolated from meat and dairy products. Int J Food Microbiol. 2015;193:68–73. https://doi.org/10.1016/j.ijfoodmicro.2014.10.014.
Disassa N, Sibhat B, Mengistu S, Muktar Y, Belina D. Prevalence and Antimicrobial Susceptibility Pattern of E. coli O157:H7 Isolated from Traditionally Marketed Raw Cow Milk in and around Asosa Town, Western Ethiopia. Veterinary Med Int. 2017;1–7. https://doi.org/10.1155/2017/7581531.
Ababu A, Endashaw D, Fesseha H. Isolation and antimicrobial susceptibility profile of Escherichia coli O157: H7 from raw milk of dairy cattle in Holeta District, central Ethiopia. Int J Microbiol 2020, 1–8. https://doi.org/10.1155/2020/ 6626488.
Hailu S. Isolation, identification and antibiotic susceptibility of E. coli from diarrheic calves in and around Holeta Town, Central Ethiopia. J Veterinary Med Res. 2020;7(5):1197–203.
Bekele T, Zewde G, Tefera G, Feleke A, Zerom K. Escherichia coli O157:H7 in raw meat in addis ababa, Ethiopia: Prevalence at an abattoir and retailers and antimicrobial susceptibility. Int J Food Contam. 2014;1(1). https://doi.org/10.1186/S40550-014-0004-9.
Geletu US, Usmael MA, Ibrahim AM. Isolation, Identification, and Susceptibility Profile of E. coli, Salmonella, and S. aureus in Dairy Farms and Their Public Health Implication in Central Ethiopia. Veterinary Medicine International, 2022. https://doi.org/10.1155/2022/1887977.
Kibret M, Abera B. Antimicrobial susceptibility patterns of E. coli from clinical sources in northeast Ethiopia. Afr Health Sci. 2011;11:40. https://doi.org/10.4314/ahs.v11i3.70069.
Tadesse T, Dabassa A. Prevalence and antimicrobial resistance of Salmonella isolated from raw milk samples collected from Kersa district, Jimma Zone, Southwest Ethiopia. J Med Sci (Faisalabad). 2012;12(7):224–8. https://doi.org/10.3923/jms.2012.224.228.
Tesfaw L, Taye B, Alemu S, Alemayehu H, Sisay Z, Negussie H. Prevalence and antimicrobial resistance profile of Salmonella isolates from dairy products in Addis Ababa, Ethiopia. Acad EdU. 2013;7(43):5046–50. https://doi.org/10.5897/AJMR2013.5635.
Bayeh A, Biadegelgen F, Bezabih B. Prevalence of Salmonella typhi and intestinal parasites among food handlers in Bahir Dar Town, Northwest Ethiopia. Ethiop J Health Dev. 2010;24(1):46–50. https://doi.org/10.4314/ejhd.v24i1.62944.
Bayleyegn M, Mesfin A, Alemayehu D. Multiple antimicrobial-resistant Salmonella serotypes isolated from chicken carcass and giblets in Debre Zeit and Addis Ababa, Ethiopia. Ethiop J Health Dev. 2004;17(2). https://doi.org/10.4314/ejhd.v17i2.9854.
Takele B, Habtie Y, Bulako C, Fufa A, Ashenafi FB, Bedaso M, Dinka A, Duguma R. Identification and Antimicrobial Susceptibility Profile of Salmonella Isolated from Selected Dairy Farms, Abattoir and Humans at Asella Town, Ethiopia. J Veterinary Sci Technol. 2016;7(320). https://doi.org/10.4172/2157-7579.1000320.
Daniel A. Shigella and Salmonella serogroups and their antibiotic susceptibility patterns in Ethiopia. East Mediterr Health J. 2008;14(4):760–7.
Ejo M, Legesse G, Zabishwork A, Walelgn W. Prevalence and Antimicrobial Resistance of Salmonella Isolated from Animal-Origin Food Items in Gondar, Ethiopia. Biomed Res Int. 2016;8. https://doi.org/10.1155/2016/4290506.

No competing interests reported.

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Occurrence of Escherichia coli, Salmonella spp. and Staphylococcus aureus and Antimicrobial Susceptibility Profile in Locally and Commercially Produced Yogurt Sold in Addis Ababa, Ethiopia

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Version 1

Abstract

1. Introduction

2. Material and Method

2.1. Description of Study Area

2.2. Study Design and Sample Collection Procedure

2.3. Isolation and Identification of Escherichia coli

2.4. Isolation and Identification of Staphylococcus aureus

2.5. Isolation and identification of Salmonella species

2.6. Antimicrobial Susceptibility Test (AST) with the Vitek 2XL compact system

2.7. Data management and analysis

3. Results

3.1. The occurrence of Escherichia coli, Salmonella spp. and Staphylococcus aureus

3.2. Antimicrobial Susceptibility in Escherichia coli and Salmonella spp.

4. Discussion

5. Conclusion

Declarations

References

Additional Declarations

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Version 1