Journal of Infectious Diseases and Diagnosis

Systematic Review on Prevalence and Antimicrobial Resistance Patterns of Salmonella Isolates in Human Stools and Animal Origin Foods in Ethiopia

Dek Kahin Yosef^1* and Kader Muse^{2 1}Department of Microbiology and Veterinary Public Health, College of Veterinary Medicine, Jigjiga University, Ethiopia
²Department of Microbiology, College of Medical and Health Science, Jigjiga University, Ethiopia
^*Correspondence: Dek Kahin Yosef, Department of Microbiology and Veterinary Public Health, College of Veterinary Medicine, Jigjiga University, Ethiopia, Email:

Received: 11-Feb-2024, Manuscript No. JIDD-24-24890; Editor assigned: 13-Feb-2024, Pre QC No. JIDD-24-24890 (PQ); Reviewed: 24-Feb-2024, QC No. JIDD-24-24890; Revised: 02-May-2025, Manuscript No. JIDD-24-24890 (R); Published: 09-May-2025, DOI: 10.35248/2576-389X.25.10.328

Introduction

Salmonellosis is one of the major zoonotic diseases all over the world with annual estimates of 22 million cases and 200,000 deaths due to typhoid fever and 93.8 million cases of gastroenteritis and 155 000 deaths due to Non-Typhoidal Salmonellae (NTS) [1]. In resource-poor settings of Africa, enteric fever is a public health concern with an incidence of 10-100/100,000 cases per year [1].

Salmonella are members of the Enterobacteriaceae, facultatively anaerobic gram-negative bacilli able to grow on a wide range of relatively simple media and distinguished from other members of the family by their biochemical characteristics and antigenic structure. The genus Salmonella consists of only two major species: Salmonella enterica and Salmonella bongori. Salmonella enterica is divided into six subspecies, which are distinguished by certain biochemical characteristics and susceptibility to lysis by bacteriophage felix 01. Salmonella enterica is divided into seven phylogenetic groups, subspecies I, II, IIIa, IIIb, IV and VII. Subspecies I includes 1367 serovars, some of which are commonly isolated from infected birds and mammals, including humans. The other subspecies mainly colonize cold-blooded vertebrates [2].

Non-typhoidal Salmonella remains the major leading agent for millions of deaths related to food-borne illness by being responsible for 93 million cases of gastroenteritis and about 155,000 deaths each year [3]. In addition, outbreaks due to food borne illness became major suffering and public health problem for many countries in the world [3]. However, there are different contributions of animal products to human salmonellosis across the globe. For example, poultry was recorded as pathogenic for 20% and 7% for beef in USA and England respectively [4,5]. The problem is more serious in developing countries, where more than one billion cases of gastroenteritis are reported and five million individuals die annually [6].

During food processing and livestock feed non-typhoidal Salmonella can have access for entrance into the food chain by any means. Human salmonellosis outbreaks related to animal products had been recorded in many countries across the globe [7]. Poultry and other food animals are considered the common reservoirs of Salmonella where undercooked food products mainly consumption of contaminated food of animal origin such as poultry products, beef and pork as well as contact with infected animals are the major sources of human infection with non-typhoidal Salmonella [7,8].

Typhoid and paratyphoid fever are enteric infections caused by the bacteria Salmonella enterica serovar typhi (S. typhi) and Paratyphi A, B and C (S. paratyphi A, B and C), respectively, collectively referred to as typhoidal Salmonella and the causes of enteric fever [9].

Humans are the only reservoir for Salmonella typhi with disease transmission occurring via the fecal oral route, usually through the consumption of food or water contaminated by human feces. An estimated 17 million cases of typhoid and paratyphoid fever illnesses occurred globally in 2015, mostly in South Asia, Southeast Asia and sub-Saharan Africa, with both the largest burden and incidence occurring in South Asia. Left untreated; both typhoid and paratyphoid fever may be fatal with 178,000 deaths estimated worldwide in 2015 [9,10].

Typhoid fever is also called enteric fever. It is a prospectively, multi-systemic illness that has been a public health problem, especially in the developing world. It is caused by Salmonella typhi and Salmonella paratyphi.

Enteric fever is a cumulative term that illustrates both typhoid and paratyphoid fever. Paratyphoid is clinically indistinct from typhoid fever; thus, enteric and typhoid fever is used mutually. Typhoid fever is one of the major causes of mortality and morbidity in overcrowded and unhygienic areas though comprehensive research and public health interventions have decreased the occurrence. The disease course ranges from early gastrointestinal distress to nonspecific systemic illness but ultimately may lead to multiple complications. Salmonella is said to spread by the 'four Fs" (flies, fingers, feces, fomites). Fever characteristically comes in a step-wise pattern (i.e., rises and falls alternatively) followed by headache and abdominal pain [11].

Salmonella spp. exhibited wide antimicrobial resistance and this remains global public health threat; particularly the developing countries are most affected and this is commonly due to increased misuse of antimicrobial agents in humans as well as in animals [12]. Antimicrobial-resistant Salmonella is nowadays considered as one of the global problems in present-day clinical practices; in addition, recently, a strain on the verge of panresistance had been reported [13]. Multi-Drug Resistant (MDR) Salmonella spp. had showed increased prevalence and it was reported the presence of an outbreaks caused by multi-drug resistant Salmonella strains in sub-Saharan Africa [14,15]. It had been reported wider antimicrobial resistance in Salmonella spp. in Ethiopia [16]. Moreover; there is difficulty in therapeutic management due to lack of proper identification of Salmonella spp. and this is because of inadequate laboratory facilities required for the accurate detection of bacteria and to perform antimicrobial susceptibility testing [12].

Materials and Methods

Methods: This review was conducted adhering to Preferred Reporting Items for Systematic Reviews and Meta-analysis (PRISMA) recommendations for transparent reporting of systematic review and meta-analysis [17].

Objective: To review prevalence and antimicrobial susceptibility patterns of Salmonella species isolated from human stool and animal origin foods in Ethiopia.

Focused question: According to PRISMA guidelines a focused question was created according to the Participants, Interventions, Control and Outcomes (PICO) principle [17,18].

The focused question of this review was “how Salmonella species are prevalent in human stool and animal origin foods and resistant to antimicrobial agents in Ethiopia?

Inclusion and exclusion criteria

Inclusion criteria: All prospective cross-sectional studies with the aim of prevalence and antimicrobial susceptibility pattern which had engaged specimens from food handlers and patients in Ethiopia studies published from 2010 to 2021.

Studies reported both sample size of the study and the numbers of isolates/number of positive samples and published in English.

Articles detected Salmonella spp. and confirmed by biochemical tests and determined the sensitivity pattern for ceftriaxone (CRO, 30 mg), chloramphenicol (C, 30 mg), ciprofloxacin (CIP, 5 mg), gentamicin (GM, 10 mg), ampicillin (AMP, 10 mg) and tetracycline (TET, 30 mg)

Exclusion criteria: Studies conducted outside of Ethiopia.

• Articles that have used microscopic, molecular and serological methods to determine and isolate Salmonella spp.
• Articles with target populations having pre-existing medical conditions (chronic) such as HIV and diabetic mellitus.
• Articles with irretrievable full texts, records with unrelated outcome measures and articles with missing or insufficient outcomes.

Search strategy of literatures

PubMed (MEDLINE), Google Scholar and Science-direct databases were used in order to collect all relevant scientific research papers. All related scientific papers published in these databases up to October, 2021 were systematically searched with date of publication restricted to 2010-2021. The structured search strategy that was employed was as follows (Salmonella spp., prevalence and resistance) or (Salmonella spp. and Ethiopia) or (Salmonella spp. and antimicrobial resistance), (Salmonella spp. and isolation).

Data extraction and screening

The principal investigator (K.M) searched through the literatures, screened, retrieved the articles for inclusion and finally extracted the data of the included articles and the advisors will check the accuracy and completeness of the data. The selected articles’ results are shown in the following table.

Results

General characteristics of included articles

After systematic research of articles through three databases (PubMed, Google Scholar and Science direct) 350 articles were first encountered. These articles undergone screening such as duplication screening, abstract and full-document review and finally 52 articles were found eligible to this systematic review. From the included 52 articles, 35 emphasized on prevalence of salmonella isolates from human stool and animal origin foods whereas 15 articles were about antimicrobial susceptibility pattern of Salmonella isolates.

All of the selected and included articles were conducted in different regions (mostly related to southern regions followed by Oromia) of Ethiopia. The most included studies were published recently. 24 articles of the included articles had assessed prevalence of Salmonella species from human stool whereas 13 of others targeted isolation of Salmonella spp. from animal-related foods such as meat, milk and egg. Five teen articles of the included studies assessed the antimicrobial susceptibility patterns of Salmonella spp. from human stools and animal origin foods. In those articles on prevalence of Salmonella species from human stool and animal origin foods, 13 of them utilized animal origin foods, 11 used food handlers and vendors, 9 of them recruited children and 4 of them enrolled outpatient. In addition, all of the included articles were performed in Ethiopia no matter which region. Most of the articles that have passed the inclusion criteria of this systematic review had utilized similar study designs (cross-sectional) but they showed moderate variation in sampling technique where majority of them used convenient sampling technique and higher variation in sample size.

Prevalence of Salmonella isolates of the selected articles

The target populations of these articles were food handlers, outpatient and U-5 children with the complaints of gastroenteritis and animal origin foods such as meat, milk and egg. In this systematic review, the highest and the lowest Salmonella spp. prevalence of articles with food handlers as target populations showed 9.04% and 1.2% respectively [19,20]. In addition, the highest and lowest prevalence of Salmonella spp. prevalence of the articles that had recruited children and U-5 children is 12.6% and 0.9%. Regarding on studies that used animal related foods such as milk, meat and eggs, the highest prevalence of Salmonella species isolated from these animal origin foods was 20% followed by 16.4%. For more detail information on prevalence of the Salmonella isolates of the included articles are shown in the following table (Table 1).

Table 1: General characteristics of selected studies for systematic review of prevalence of Salmonella spp. isolated from human stool and animal origin foods in Ethiopia.

Antimicrobial susceptibility patterns of Salmonella isolates

Ten articles that were conducted in Ethiopia have been selected and included in this systematic review for antimicrobial susceptibility pattern assessment of Salmonella isolated from human stools and animal origin foods. Most of them addressed the susceptibility pattern of Salmonella species for at least three intended antimicrobial agents based on this systematic review’s inclusion and selection criteria of antibiotics. In summary, all most all of the selected studies had reported similar resistance of all Salmonella species isolated against Ampicillin (AMP). On the other hand; most of the included articles reported that all of the Salmonella spp. showed higher sensitivity for Ciprofloxacin (CIP) and Ceftriaxone (CRO). For further information for antimicrobial susceptibility patterns of isolated Salmonella spp. has been shown in the following table (Table 2 and Figure 1).

Table 2: General features of selected articles for systematic review of antimicrobial susceptibility patterns of Salmonella spp. isolated from human stool and animal origin foods in Ethiopia

Figure 1: Article selections flow chart for systematic review on prevalence and its antimicrobial susceptibility pattern of Salmonella spp. in Ethiopia.

Discussion

Food borne diseases caused by non-typhoidal Salmonella spp. remains critical public health threat globally. Human Salmonellosis resulted in millions of deaths worldwide where developing countries such as Ethiopia are mostly affected. Nowadays, globally Salmonella spp. isolated from human stools and animal origin foods exhibited wider antimicrobial resistance. I used a systematic method to identify articles reporting the prevalence and antimicrobial resistance profile of Salmonella in human stools and animal origin foods in Ethiopia. A total of 52 original articles, 24 of them on human stools, 13 of them on animal origin foods and 15 on antimicrobial susceptibility patterns were included in this systematic review to determine the pooled prevalence of Salmonella and its antimicrobial resistance status. All the included articles had utilized cross-sectional study design.

On this review, I qualitatively summarized that the included articles’ results where the summary revealed Salmonella spp. being prevalent in human stool of patients having Salmonellosis and wider antimicrobial resistance showed in particularly for Ampicillin. Study conducted in Addis Ababa on 233 food handlers reported prevalence (3.4%) of Salmonella species and this result is in line with study conducted in Hawassa on 236 food handlers with prevalence of 2.12%. In contrast, another study conducted in Sodo town on food handlers reported higher prevalence (9.04%) of Salmonella spp. compared to the above mentioned.

Study conducted in Adama had taken 66 meat samples for Salmonella spp. examination had reported prevalence of 6.1%. In contrast, another studies conducted in Debreziet, Shashamene and Kombolcha reported higher prevalence (14.6%, 13.3% and 11.5% respectively) of Salmonella species isolated from meat and egg. Study conducted in Arbaminch which was on under-five children reported higher prevalence of Salmonella species which was 12.6% and this was somehow in line with another study done in Bahirdar on under-five children which was 7.8%. In contrast to this, study which was performed in Wegera had stated lower prevalence (0.95%) of Salmonella species in underfive children. Concerning the antimicrobial susceptibility patterns of the articles included in this review for Salmonella species isolated from human stool and animal origin foods determines almost similar report of complete resistance of Salmonella spp. to ampicillin and widespread susceptibility of Salmonella species for ciprofloxacin and ceftriaxone according to the results of the included articles of this review.

Although the studies recruited different study subjects such as food handlers, under-five children and animal origin foods; the qualitative summary of the articles emphasized on antimicrobial susceptibility patterns shows that Salmonella species isolated from either human stool or animal related foods can no longer be treated with ampicillin. This might be due to inappropriate use of this drug and its ease availability and widely usage for human and livestock. Study conducted in Addis Ababa assessed the antimicrobial susceptibility of Salmonella spp. had reported fully resistance to ampicillin and fully susceptibility to ciprofloxacin and this was in line with study done in Bahirdar, Arbaminch, Hawassa and Addis Ababa.

From the studies which are included into this systematic review and assessed the prevalence of salmonella species from animal related foods such as meat, milk and egg, higher prevalence has been documented in milk followed by meat and egg. A study conducted in allege on egg had reported higher prevalence (13.3%) of Salmonella species and this is in contrast to another similar study performed in Gonder which was on egg and reported 5.5%. This might be due to difference in hygienic practices among the community.

Conclusion

After qualitative summarizing of the included articles, Salmonella species isolated from Human stools from individuals suspected of Salmonellosis and animal related foods showed elevated prevalence (specifically among under-five children followed by outpatients) and widespread and higher antimicrobial resistance of Salmonella spp. was observed particularly against ampicillin followed by tetracycline in Ethiopia.

Recommendation

Based on the above mentioned findings from this review, early and accurate laboratory diagnosis and performing antimicrobial susceptibility patterns are highly recommended before any antibiotic prescription. Capacitating Salmonella resistance surveillance, community health education regarding hygienic practices, maintaining adequate hygiene and sanitary measures, cooking food thoroughly and appropriated use of antimicrobial agents are necessary to reduce the prevalence and antimicrobial resistances of Salmonella species.

Limitations

This paper had qualitatively assessed only the prevalence and antimicrobial susceptibility pattern of Salmonella isolates in human stool and animal origin foods in Ethiopia. This lacks quantitative summary (meta-analysis). In addition, all the studies selected utilized similar study design which is cross-sectional and conducted in Ethiopia only.

References

1. Crump JA, Luby SP, Mintz ED. The global burden of typhoid fever. Bull World Health Organ. 2004;82(5):346-353.

   [Google Scholar]

2. Su L, Chiu CH. Salmonella: Clinical importance and evolution of nomenclature. Chang Gung Med J. 2007;30(3):210.

   [Google Scholar] [PubMed]

3. Andrews AH, Blowey RW, Boyd H, Eddy RG. Bovine medicine: Diseases and husbandry of cattle. John Wiley and Sons; 2008.

   [Google Scholar]

4. Hoffman S, Maculloch B, Batz M. Economic burden of major foodborne illnesses acquired in the United States. 2015.

   [Google Scholar]

5. Heredia NL, Wesley IV, Garcia JS. Microbiologically safe foods. John Wiley and Sons; 2009.

   [Google Scholar]

6. Gould GW, Russell NJ. Major, new, and emerging food-poisoning and food-spoilage microorganisms. InFood preservatives 2003. Boston, MA: Springer US.
7. Braden CR. Salmonella enterica serotype enteritidis and eggs: A national epidemic in the United States. Clin Infect Dis. 2006;43(4):512-517.

   [Crossref] [Google Scholar] [PubMed]

8. Foley SL, Nayak R, Hanning IB, Johnson TJ, Han J, Ricke SC. Population dynamics of Salmonella enterica serotypes in commercial egg and poultry production. Appl Environ Microbiol. 2011;77(13):4273-4279.

   [Crossref] [Google Scholar] [PubMed]

9. Buckle GC, Walker CL, Black RE. Typhoid fever and paratyphoid fever: Systematic review to estimate global morbidity and mortality for 2010. J Glob Health. 2012;2(1).

   [Crossref] [Google Scholar] [PubMed]

10. Mogasale V, Maskery B, Ochiai RL, Lee JS, Mogasale VV, Ramani E, et al. Burden of typhoid fever in low-income and middle-income countries: A systematic, literature-based update with risk-factor adjustment. Lancet Global Health. 2014;2(10):e570-e580.

    [Crossref] [Google Scholar] [PubMed]

11. Bhandari J, Thada PK, DeVos E. Typhoid fever. StatPearls. Treasure Island (FL). 2022.
12. Abate D, Assefa N. Prevalence and antimicrobial resistance patterns of Salmonella isolates in human stools and animal origin foods in Ethiopia: A systematic review and meta-analysis. Int J Health Sci (Qassim). 2021;15(1):43.

    [Google Scholar] [PubMed]

13. Le Hello S, Harrois D, Bouchrif B, Sontag L, Elhani D, Guibert V, et al. Highly drug-resistant Salmonella enterica serotype Kentucky ST198-X1: A microbiological study. Lancet Infect Dis. 2013;13(8):672-679.

    [Crossref] [Google Scholar] [PubMed]

14. Kariuki S, Revathi G, Kariuki N, Muyodi J, Mwituria J, Munyalo A, et al. Increasing prevalence of multidrug-resistant non-typhoidal salmonellae, Kenya, 1994–2003. Int J Antimicrob Agents. 2005;25(1):38-43.

    [Crossref] [Google Scholar] [PubMed]

15. Niehaus AJ, Apalata T, Coovadia YM, Smith AM, Moodley P. An outbreak of foodborne salmonellosis in rural KwaZulu-Natal, South Africa. Foodborne Pathog Dis. 2011;8(6):693-697.

    [Crossref] [Google Scholar] [PubMed]

16. Getachew M, Gebru M, Tsehaynesh L, Abraham A. Prevalence and antimicrobial susceptibility patterns of Salmonella serovars and Shigella species. Microb Biochem Technol. 2014;2:1-7.
17. Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. The PRISMA 2020 statement: An updated guideline for reporting systematic reviews. Rev Esp Cardiol (Engl Ed). 2021;74(9):790-799.

    [Crossref] [Google Scholar] [PubMed]

18. Boudin F, Nie JY, Bartlett JC, Grad R, Pluye P, Dawes M. Combining classifiers for robust PICO element detection. BMC Med Inform Decis Mak. 2010;10:1-6.

    [Crossref] [Google Scholar] [PubMed]

19. Solomon FB, Wada FW, Anjulo AA, Koyra HC, Tufa EG. Burden of intestinal pathogens and associated factors among asymptomatic food handlers in South Ethiopia: Emphasis on salmonellosis. BMC Res Notes. 2018;11:1-6.

    [Crossref] [Google Scholar] [PubMed]

20. Getie M, Abebe W, Tessema B. Prevalence of enteric bacteria and their antimicrobial susceptibility patterns among food handlers in Gondar town, Northwest Ethiopia. Antimicrob Resist Infect Control. 2019;8:1-6.

    [Crossref] [Google Scholar] [PubMed]