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A Systematic review on Prevalence, Serotypes and Antibiotic resistance of Salmonella in Ethiopia, 2010–2022
Authors Kahsay AG , Dejene TA , Kassaye E
Received 4 June 2023
Accepted for publication 4 October 2023
Published 13 October 2023 Volume 2023:16 Pages 6703—6715
DOI https://doi.org/10.2147/IDR.S424345
Checked for plagiarism Yes
Review by Single anonymous peer review
Peer reviewer comments 3
Editor who approved publication: Professor Sandip Patil
Atsebaha Gebrekidan Kahsay,1 Tsehaye Asmelash Dejene,1 Enquebaher Kassaye2
1Department of Medical Microbiology and Immunology, Mekelle University, Mekelle, Tigrai, Ethiopia; 2Department of Food Safety and Veterinary Microbiology, Mekelle University, Mekelle, Tigrai, Ethiopia
Correspondence: Atsebaha Gebrekidan Kahsay, Department of Medical Microbiology and Immunology, Mekelle University, P. O. Box: 1871, Mekelle, Tigrai, Ethiopia, Email [email protected]
Background: In Ethiopia, salmonellosis is one of the most common zoonotic and foodborne illnesses. Ethiopia continues to be at risk for its fast-expanding medication resistance. For the development of preventative and control methods, summarized knowledge regarding salmonellosis is necessary. Determining a thorough evaluation of the prevalence, serotypes, and antibiotic resistance of Salmonella in humans and animals from January 1, 2010, to December 30, 2022, in Ethiopia was our goal.
Methods: To find Salmonella related articles that published in English, we used the Google Scholar and PubMed search engines. Three researchers conducted the eligible studies using the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) checklist, making sure to include the necessary keywords. If studies were duplicates, incomplete publications, or reported without an antimicrobial test were excluded. Excel 2013 was used to calculate frequencies and tabulate data.
Results: There were a total of 43 investigations from food handlers, diarrhoeic patients, and animals. The prevalence rates ranged from 1% to 10% and 1% to 13% among food handlers and diarrhoea patients, respectively. The highest prevalence was among pigs (41.6%). S. Anatum in animals and S. Typhimurium in people were the predominant serotypes. Amoxicillin and ampicillin were claimed to be 100% resistant in human studies. The highest recorded resistances for ceftriaxone and ciprofloxacin were 16.7% and 100%, respectively. Animal studies revealed that Salmonella resistances to ampicillin, streptomycin and tetracycline were 100%, 90%, 86.4%, respectively. S. Kentucky showed complete resistance to tetracycline, ampicillin, gentamicin, ciprofloxacin, and streptomycin.
Conclusion: The prevalence of Salmonella among asymptomatic food handlers, diarrheal patients and animals were high in Ethiopia. S. Typhimurium that have the zoonotic importance was presented predominantly in human study. High levels of resistances were showed to tetracycline, ampicillin and streptomycin in animal studies. Salmonellosis prevention and control techniques should be strengthened.
Keywords: antibiotic resistance, prevalence, systematic review, serotypes, Salmonella, Ethiopia
Introduction
Salmonellosis continues to be a serious global public health issue, particularly in developing nations.1,2 One-fourth of 550 million diarrheic people worldwide are thought to contract Salmonella each year as a result of eating contaminated food.3 Human typhoid fever is caused by Salmonella Typhi and Salmonella Paratyphi.4 Some Salmonella are specific to animal species although others have wide variety of animals, in addition to humans, such as Salmonella Typhimurium and Salmonella Enteritidis.5
Red meat, carcasses, slaughterhouse equipment, and utensils can all get contaminated by the mesenteric lymph nodes and faeces of sick cattle, swine, sheep, or reservoir animals.6–10 As a result, eating raw or undercooked meat or eggs results in human infection.11 Salmonella infections can also be carried by human and animal faeces, which can contaminate crops.12 In addition, hospitalization has been implicated as a source of invasive non-typhoidal Salmonella.13 Salmonella infections can lead to outbreaks of human salmonellosis and a variety of clinical symptoms, such as mild gastroenteritis, bacteremia, and extra-intestinal localized infections affecting numerous organs.1
One of the present and expanding global risks to public health is Salmonella drug resistance. According to a study from Mexico, non-typhoidal Salmonella had a resistance range of 16.9% to 40.3% to the antibiotics trimethoprim-sulfamethoxazole, amoxicillin-clavulanic acid, chloramphenicol, and tetracycline.14 Similar to this, the Salmonella serotypes found in food and people in Italy were resistant to tetracycline (48%) and ampicillin (45%),15 and from China, the NTS resistance pattern to ceftriaxone was 37%.16 Additionally, 36,000 and 33,000 cases of salmonella infections resistant to ciprofloxacin and ceftriaxone, respectively, were reported annually from the United States.17 Salmonella serotypes resistant to ceftriaxone have also been reported in Kenya.18
According to the prior data, an article on Salmonella in Ethiopia had been published since 1985,19 and in 1994, Salmonella Newport had been discovered in suspected food poisoning cases among students and food handlers in Gondar, Ethiopia.20 From various regions in Ethiopia, a lot of papers about Salmonella have been published. These researches looked at the frequency of different Salmonella species, serotypes, and medication resistance patterns in people, animals, and vegetables. Numerous Salmonella isolates with high levels of antibiotic resistance have been discovered.21–24
Ethiopia had vast livestock animals in Africa, and living alongside people is prevalent there.25 This may cause the spread of zoonotic illnesses like non-typhoidal salmonella26 as individuals in Ethiopia do not fully comprehend how zoonoses, such as Salmonella are spreading.27 As a result, large number of vulnerable individuals like malnourished children may be exposed to the invasive form of non-typhoidal Salmonella.28,29
Despite the fragmented local studies about Salmonella that have been reported from various regions of Ethiopia, concise information from a systematic review is more helpful for scientific users to identify gaps for additional studies and for policymakers to develop prevention and control strategies based on the scientific information provided. Thus, we sought to conduct a systematic evaluation of the prevalence, serotypes, and antibiotic resistance of Salmonella in people, animals, and their products in Ethiopia from January 1, 2010, to December 30, 2022.
Methods
Literature Search
To find English-language publications concerning Salmonella that had already been published, we used the Google Scholar and PubMed search engines. Keywords like “prevalence”, “incidence”, “Salmonella”, “Salmonella serotypes”, “food handlers”, “diarrheic patients”, “antibiotic susceptibility”, “antimicrobial susceptibility”, “antibiotic resistance”, “antimicrobial resistance”, “animals”, “humans”, and “Ethiopia” were used to search the included studies.
The Inclusion and Exclusion Standards
Three researchers independently conducted the eligible studies using the PRISMA30 checklist to make sure all pertinent data was included. If a study met the requirements listed below, it was qualified for the systematic review: Salmonella resistance and prevalence in animals and humans are mentioned in the purpose, which is also stated in the design, sample size, description of the microbiological procedures, and number of isolates. The study was published in English. Studies were disregarded if they were duplicates, partial papers, or reported Salmonella without an antimicrobial test.
Obtaining and Analyzing Data
From each examined paper, the names of the authors, the publication year, the kind of media, the study setting, the sampling techniques, the study populations, the type of specimens, the sample size, the number of positive isolates, the antimicrobial susceptibility tests, and the list of serotypes (if any) were taken. Using Excel 2013, frequencies and percentages were examined.
Results
Between January 1, 2010, and December 30, 2022, the search engines Google Scholar and PubMed turned up a total of 207 published papers; 100 of those articles were disregarded from additional examination owing to duplication. After reviewing the 107 research titles and abstracts, it was determined that 52 did not meet the requirements for inclusion. Only 55 articles that met the requirements for eligibility were given a second evaluation, and 12 of them were disqualified for various reasons. Figure 1 shows that our systematic review only comprised 43 papers.
 |
Figure 1 Flow Diagram for Selection of Eligible Studies. Adapted from Moher D, Liberati A, Tetzlaff J, Altman DG, The PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009;6(7):e1000097. Creative Commons.30 |
Characteristics of Studies on Salmonella among Asymptomatic Food Handlers and Diarrhoea Patients
Of the 43 eligible studies that were conducted, 28 were asymptomatic food handlers from the community and diarrhoeic patients from public health facilities. While 13 types of research involved asymptomatic food handlers working in university and community cafeterias, 15 studies involved children and adults with diarrhoea. The only clinical specimens reported in any of the investigations for Salmonella isolation were faeces. The most frequently employed media were Xylose Lysine Deoxycholate, Deoxycholate Citrate Agar, MacConkey Agar, and Salmonella Shigella Agar. According to Table 1, convenience sampling was used in 19 of the investigations, while simple random sampling was used in the other nine.
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Table 1 A Systematic Review of Characteristics of Asymptomatic Food Handlers and Public Health Facility Diarrheic Patients in Ethiopia, January 1, 2010, to December 30, 2022 |
Salmonella Prevalence in Asymptomatic Food Handlers and Diarrheal Patients
Salmonella prevalence in asymptomatic food handlers (n=13) ranges from 1% to 10%, but it ranges from 1% to 13% in diarrhoeic patients (n=15). More than three-fourths of the reports among asymptomatic food workers had prevalence rates that were less than 5%. On the other hand, in more than two-thirds of the cases, including diarrheal patients, the prevalence rates were 5% or higher as shown in Table 2.
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Table 2 A Systematic Review of the Prevalence of Salmonella Among Asymptomatic Food Handlers and Public Health Facilities Diarrheic Patients in Ethiopia from January 1, 2010, to December 30, 2022 |
Characteristics of Research on Salmonella in Animal-Related Samples
The specimens used to isolate Salmonella came from cattle, poultry, pigs, goats, and sheep. These included the contents of the caecum, mesenteric lymph nodes, liver, tongue, hide swabs, rumen, faeces, and cecum, as well as the contents of market eggs and market eggshells. All studies involving animals used the following essential pre-enrichment, enrichment, and selective media: buffered peptone water, brilliant green phenol red lactose sucrose, xylose lysine deoxycholate, MacConkey agar, brilliant green agar, xylose lysine territory 4, selenite cysteine broth, Rappaport-Vassiliadis, and Tetrathionate broth.
Salmonella is present in all of the animal-related specimens, with prevalence ranging from 3.1% in poultry to 29.1% in pig mesenteric lymph nodes. Table 3 lists the results of the investigations that examined the tissue and faeces of pigs, cattle, poultry, sheep, and goats.
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Table 3 A Systematic Review of the Prevalence of Salmonella in Animals Associated Specimens in Ethiopia from January 1, 2010, to December 30, 2022 |
Salmonella Antibiotic Resistance Among Food Handlers and Diarrheal Patients
A minimum of nine antibiotics were used to assess the resistance of Salmonella isolates. Amoxicillin, ampicillin, tetracycline, trimethoprim-sulfamethoxazole, chloramphenicol, nalidixic acid, gentamicin, ciprofloxacin, and ceftriaxone were on the lists of antibiotics taken from the studies that qualified. In six investigations for amoxicillin (two from food handlers and four from diarrhoea patients) and eight for ampicillin (four from food handlers and four from diarrhoea patients), all of the isolates displayed 100% resistance. Seven investigations (three in food handlers and four in diarrhoea patients) and eight (two in food handlers and six in diarrhoea patients), respectively, identified resistant isolates for ciprofloxacin and ceftriaxone. Although diarrhoeic patients appear to have relatively significant resistance, Table 4 shows that the highest reported ciprofloxacin and ceftriaxone resistance rates were 16.7% and 100%, respectively. Among all the asymptomatic food handlers and diarrheal patients tested for Salmonella, only one study was found eligible for serotyping. The leading serotype that reported from that study was S. Typhimurium, whereas single isolate of S. Concord showed 100% resistance to amoxicillin, ampicillin, tetracycline, gentamicin, sulfamethoxazole trimethoprim and ciprofloxacin as indicated in Table 4.
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Table 4 A Systematic Review of Antibiotic Resistance of Salmonella Among Asymptomatic Food Handlers and Public Health Facility Diarrheic Patients in Ethiopia from January 1, 2010 to December 30, 2022 |
Animal Salmonella with Antibiotic Resistance
As shown in Table 5, all Salmonella isolates from investigations involving animal-related samples were resistant to ampicillin, 90% to streptomycin, 66.7% to chloramphenicol, 86.4% to tetracycline, 35.2% to ciprofloxacin, 29.4% to gentamicin, and 23.2% to ceftriaxone. When it comes to salmonella serotypes’ resistance to antibiotics, the ampicillin, gentamicin, ciprofloxacin, streptomycin, and tetracycline resistance in S. Kentucky was 100% although the leading isolates of salmonella serotypes reported from the researches were S. Anatum, S. Saintpaul, S. Newport, and S. Typhimurium.
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Table 5 A Systematic Review of Antibiotic Resistance of Salmonella in Species and Serotype Level in Animals Related Specimens in Ethiopia from January 1, 2010 to December 30, 2022 |
Discussion
One of the main contributors to foodborne and zoonotic diseases in underdeveloped nations is Salmonella.1,2 It is one of Ethiopia’s top seven priority zoonotic diseases73 and a significant source of foodborne pathogens.74
Salmonella prevalence among asymptomatic food handlers ranges from 1% to 10%, which was consistent with research from Pakistan (9.1%).75 Similar to this, the prevalence of Salmonella among individuals who have diarrhoea ranges from 1% to 13%. However, one instance at a hospital suggests that there are 30 other cases in the community who are unable to visit hospitals for a variety of reasons.76
The prevalence rates of Salmonella in animal-related sources range from 3.1% in poultry to 29.4% in pigs, followed by cloacal and cecal content of chicken (24.6%) which is consistent with studies from Burkina Faso,77,78 Italy,79 Kenya,80 South Africa,81 and Uganda,82 Vietnam,83 China,84 and Louisiana.85
S. Typhimurium were reported in all of the legible studies for serotyping which was also reported from Gambia,86 Mali,87 India,88 Mexico,89 and China.90 According to reports from sub-Saharan African nations, S. Typhimurium and S. Enteritidis are invasive forms of NTS, especially among susceptible people, such as those with HIV, malnourished children, and in malaria areas.77,91 It is possible that the existence of such Salmonella germs in cattle, poultry, pigs, and other animal sources is regarded as a potential source of contamination in humans and maybe the main risk factor for Salmonella outbreaks in humans.8
Six human studies found that every isolate of Salmonella tested had a 100% amoxicillin resistance rate, which is consistent with an Ethiopian study.24 Ciprofloxacin-resistant isolates were detected in seven human studies which is similar to studies from China,92 and Mexico.93
Salmonella isolates from two investigations had 100% ampicillin resistance, which was higher than the prior study in Japan.6 However, the streptomycin resistance patterns were consistent with earlier Japanese studies.6 For ciprofloxacin, gentamicin, and ceftriaxone, similar animal specimens showed at least 25% resistance. S. Kentucky showed 100% resistance to ampicillin, gentamicin, ciprofloxacin, streptomycin, and tetracycline out of the known serotypes from our systematic evaluation.
The results of our systematic review are very beneficial in helping people understand important information concerning Salmonella. We were unable to include Salmonella in food, fruits, or vegetables because of limited data. Additionally, no studies that were included in this systematic review performed molecular characterization of Salmonella and its resistance genes or invasive non-typhoidal salmonella among malnourished children because of no studies related.
Conclusions
The prevalence of Salmonella in animals, diarrhoeal patients, and asymptomatic food handlers was high. The prevalence of Salmonella among asymptomatic food handlers and diarrheal patients was nearly similar. S. Typhimurium that has the zoonotic nature was recovered from human and animal studies. Studies on animals revealed high levels of resistance to tetracycline, ampicillin, and streptomycin. Circulating of Salmonella in the community in Ethiopia is a homework for academic and non-academic researchers to overcome fear of future outbreaks. National and international organizations should work on strengthening the prevention and control of salmonellosis. Due to Ethiopia’s high prevalence of underweight children and the prevalence of those who are susceptible to the invasive form of NTS, invasive non-typhoidal salmonella among malnourished children should be examined.
Disclosure
The authors report no conflicts of interest in this work.
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