A Systematic review on Prevalence, Serotypes and Antibiotic resistance of Salmonella in Ethiopia, 2010–2022

Abstract

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.

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

Authors Name with Reference	Transport & Enrichment Media	Selective and Differential Media	Study Setting	Sampling Method	Study Population	Specimen
Food handlers
Gebreyesus et al, 2014^Citation31	SFB	XLD	University	Convenience	Food handlers	Stool
Getie et al, 2019^Citation32	CTM and SCB	XLD and SSA	Community	SRS	Food handlers	Stool
Abera et al, 2010^Citation33	SFB	SSA	Community	SRS	Food handlers	Stool
Solomon et al, 2018^Citation34	SFB	XLD and BGA	Community	SRS	Food handlers	Stool
Awol et al, 2019^Citation35	CTM	XLD and MAC	Community	SRS	Food handlers	Stool
Yesigat et al, 2020^Citation36	CTM and SFB	XLD and MAC	Community	SRS	Food handlers	Stool
Aklilu et al, 2015^Citation37	SFB	XLD	University	SRS	Food handlers	Stool
Kifelew et al, 2014^Citation38	SCB	RVB, TTB and XLD	University	SRS	Food handlers	Stool
Getnet et al, 2014^Citation39	SFB	XLD	University	Convenience	Food handlers	Stool
Mengist et al, 2018^Citation40	RVB	TTB, XLD, BGA	University	Convenience	Food handlers	Stool
Tadesse et al, 2019^Citation41	CTM and SFB	XLD and DCA	Community	SRS	Street Food vendor	Stool
Mama and Alemu, 2016^Citation42	SFB	XLD and MAC	University	Convenience	Food handlers	Stool
Diriba et al, 2020^Citation43	CTM and SFB	XLD and DCA	University	SRS	Food handlers	Stool
Diarrheic patients
Tosisa et al, 2020^Citation44	CTM and SFB	XLD, MAC	Healthfacility	Convenience	Diarrheic children	Stool
Abebe et al, 2018^Citation45	CTM and SFB	XLD, DCA	Healthfacility	Convenience	Diarrheic children	Stool
Getamesay et al, 2014^Citation46	CTM and SFB	XLD, DCA	Healthfacility	Convenience	Diarrheic children	Stool
Mamuye et al, 2015^Citation47	CTM	XLD, DCA, SSA	Healthfacility	Convenience	Diarrheic children	Stool
Mulu et al, 2017^Citation48	SFB	MAC, XLD	Healthfacility	Convenience	Diarrheic patients	Stool
Kebede et al, 2017^Citation49	SFB	XLD, MAC	Healthfacility	Convenience	Diarrheic patients	Stool
Amsalu et al, 2021^Citation50	CTM	MAC	Healthfacility	Convenience	Diarrheic patients	Stool
Beyene and Tasew, 2014^Citation51	CTM and SFB	XLD, DCA	Healthfacility	Convenience	Diarrheic children	Stool
Eguale et al, 2015^Citation52	RVB,	XLT 4	Healthfacility	Convenience	Diarrheic patients	Stool
Gebreegziabher, 2018^Citation53	SFB	MAC, XLD	Healthfacility	Convenience	Diarrheic children	Stool
Terfassa, 2018^Citation54	SFB	XLD, SSA	Healthfacility	Convenience	Diarrheic patients	Stool
Asefa et al, 2019^Citation55	SCB	HEA, SSA	Healthfacility	Convenience	Diarrheic children	Stool
Lamboro et al, 2016^Citation56	SFB	XLD	Healthfacility	Convenience	Diarrheic patients	Stool
Reda et al, 2011^Citation57	SFB	CTM, XLD, DCA	Healthfacility	Convenience	Diarrheic patients	Stool
Ameya et al, 2018^Citation58	Not use	XLD, MAC	Healthfacility	Convenience	Diarrheic children	Stool

Abbreviations: CTM, Cary Blair Transport media; DCA, Deoxycholate Citrate Agar; XLD, xylose Lysine Deoxycholate Agar; Selenite F broth; nr not reported; MAC, MacConkey agar; SSA, Salmonella Shigella agar; RVB, Rappaport-Vassiliadis; TTB, Tetrathionate broth; BGA, brilliant green; SRS, Simple Random sampling.

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.

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

Authors name with Reference	Sample size	Isolates	Percent
Food handlers
Gebreyesus et al, 2014^Citation31	307	3	1
Getie et al, 2019^Citation32	257	3	1
Abera et al, 2010^Citation33	384	6	1.6
Solomon et al, 2018^Citation34	387	35	2
Awol et al, 2019^Citation35	236	5	2
Yesigat et al, 2020^Citation36	243	6	2
Aklilu et al, 2015^Citation37	172	6	3
Kifelew et al, 2014^Citation38	423	13	3
Getnet et al, 2014^Citation39	233	8	3.4
Mengist et al, 2018^Citation40	220	8	4
Tadesse et al, 2019^Citation41	218	13	6
Mama and Alemu, 2016^Citation42	345	24	7
Diriba et al, 2020^Citation43	220	21	10
Diarrheic patients
Tosisa et al, 2020^Citation44	239	3	1
Abebe et al, 2018^Citation45	204	2	1
Getamesay et al, 2014^Citation46	158	4	3
Mamuye et al, 2015^Citation47	253	10	4
Mulu et al, 2017^Citation48	575	24	4
Kebede et al, 2017^Citation49	215	11	5
Amsalu et al, 2021^Citation50	150	8	5.3
Beyene and Tasew, 2014^Citation51	260	16	6
Eguale et al, 2015^Citation52	957	59	6.2
Gebreegziabher, 2018^Citation53	260	19	7
Terfassa, 2018^Citation54	422	30	7
Asefa et al, 2019^Citation55	422	29	7
Lamboro et al, 2016^Citation56	176	19	11
Reda et al, 2011^Citation57	244	28	11
Ameya et al, 2018^Citation58	167	21	13

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.

Table 3 A Systematic Review of the Prevalence of Salmonella in Animals Associated Specimens in Ethiopia from January 1, 2010, to December 30, 2022

Authors Name with Reference	Pre-Enrichment	Enrichment & Selective Media	BT	SAT	Participant	Type of Samples	Sample Size	Isolates	%
Eguale et al, 2016^Citation22	BPW	RVB, BPLS, XLD	Yes	Yes	Pig	Caecal content, MLN	556	162	29.1
Dagnew et al, 2020^Citation59	BPW	RVB, XLD	Yes	Yes	Poultry	Cloacal and fecal content	718	22	3.1
Worku et al, 2022^Citation60	BPW	MAC, XLD	Yes	Nr	Cattle	Meat and swab	556	23	4.1
Tadesse et al, 2019^Citation61	BPW	SCB, BGA, XLD	Yes	Nr	Egg	Market egg and eggshell	166	7	4.2
Eguale T, 2018^Citation62	BPW	RVB, BGA, XLD	Yes	Nr	Poultry	Faecal	549	26	4.7
Alemu and Zewde, 2012^Citation63	BPW	SCB, XLD	Yes	Nr	Cattle	MLN, Intestinal, carcass	558	26	4.7
Mustefa and Gebreedhin, 2018^Citation64	BPW	RVB, TTB, XLT4	Yes	Nr	Cattle	Faecal, MLN	300	17	4.7
Alemu et al, 2022^Citation65	BPW	RVB, BPLS, XLD	Yes	Yes	Goats and sheep	Carcass & skin swabs	345	21	6
Wabeto et al, 2017^Citation66	BPW	RVB, BGA, XLD	Yes	Nr	Cattle	Carcass	896	56	6.3
Addis et al, 2011^Citation67	BPW	RVB, TTB, XLT4	Yes	Nr	Cow	Fecal and milk	390	21	7
Takele et al, 2018^Citation68	BPW	RVB, MAC, XLD	Yes	Nr	Cattle	Caecal and fecal	390	33	8.9
Mohammed and Dubie, 2022^Citation69	BPW	RV	Yes	Nr	Poultry	Cloacal swab	168	21	12.5
Sibhat et al, 2011^Citation70	BPW	RVB, BPLS, XLD	Yes	Yes	Cattle	Hide, rumen, caecal, MLN	400	64	16
Usmael et al, 2022^Citation71	BPW	SCB, BGA, XLD	Yes	Nr	Dog	Rectal swab samples	415	26	6.3
Belachew et al, 2021^Citation72	BPW	RV, SSA, XLD, BGA	Yes	Nr	Chicken	Cloacal &cecum	289	71	24.6

Abbreviations: Nr, Not reported; BPW, Buffered Peptone Water; BPLS, brilliant green phenol red lactose sucrose; XLD, Xylose Lysine Deoxycholate; MAC, MacConkey; BGA, Brilliant Green Agar; XLT4, Xylose Lysine Tergitol 4; SCB, Selenite Cysteine Broth; RVB, Rappaport-Vassiliadis; TTB, Tetrathionate broth; BT, Biochemical tests; SAT, Slide Agglutination Test; MLN, Mesenteric Lymph Node.

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.

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

Authors name, Number of isolates and Reference	Antibiotics Resistance, n (%)
	AMO	AMP	T	SXT	C	NA	CN	CIP	CRO
Food handlers
Gebreyesus et al (n=3)^Citation31	ND	2 (66.7)	2 (66.7)	ND	3 (100)	ND	0	0	ND
Getie et al (n=3)^Citation32	1 (33.3)	0	2 (66.7)	1 (33.3)	0	0	1 (33.3)	0	0
Abera et al (n=6)^Citation33	ND	6 (100)	4 (66.7)	5 (83.3)	2 (33.3)	ND	2 (33.3)	ND	ND
Solomon et al (n=35)^Citation34	26 (74.3)	30 (85.7)	ND	24 (68.6)	9 (25.7)	15 (42.9)	ND	5 (14.3)	10 (28.6)
Awol et al (n=5)^Citation35	Nr	3 (60)	4 (80)	2 (40)	2 (40)	1 (20)	ND	0	0
Yesigat et al (n=6)^Citation36	ND	6 (100)	5 (83.3)	1 (16.7)	0	ND	ND	0	ND
Aklilu et al (n=6)^Citation37	6 (100)	6 (100)	0	ND	ND	ND	0	0	ND
Kifelew et al (n=13)^Citation38	6 (46.2)	7 (53.8)	6 (42.3)	2 (15.4)	ND	2 (15.4)	0	ND	0
Getnet et al (n=8)^Citation39	ND	7 (87.5)	1 (12.5)	1 (12.5)	1 (12.5)	Nr	0	1 (12.5)	0
Mengist et al (n=8)^Citation40	ND	8 (100)	5 (83.3)	3 (37.5)	2 (25)	ND	0	0	ND
Tadesse et al (n=13)^Citation41	12 (92.3)	12 (92.3)	10 (77)	2 (15.4)	1 (7.7)	2 (15.4)	2 (15.4)	0	0
Mama and Alemu (n=24)^Citation42	24 (100)	ND	ND	0	0	ND	0	ND	0
Diriba et al (n=21)^Citation43	15 (71.4)	17 (81)	ND	10 (47.6)	15 (71)	ND	ND	5 (23.8)	3 (100)
Diarrheic patients
Tosisa et al (n=3)^Citation44	0	3 (100)	2 (66.7)	2 (66.7)	1 (33.3)	0	0	0	ND
Abebe et al (n=2)^Citation45	ND	2 (100)	ND	1 (50)	0	0	2 (100)	0	0
Getamesay et al (n=4)^Citation46	0	0	0	0	0	1 (25)	0	0	4 (100)
Mamuye et al (n=10)^Citation47	8 (80)	8 (80)	ND	6 (60)	4 (40)	2 (20)	0	0	0
Mulu et al (n=24)^Citation48	8 (33.3)	22 (91.7)	0	8 (33.3)	4 (16.7)	ND	ND	4 (16.7)	9 (37.5)
Kebede et al (n=11)^Citation49	ND	ND	7 (63.7)	8 (72.7)	8 (72.7)	1 (9)	1 (9)	1 (9)	1 (9)
Amsalu et al (n=8)^Citation50	ND	ND	7 (87.5)	7 (87.5)	4 (50)	3 (37.5)	2 (25)	1 (12.5)	2 (25)
Beyene and Tasew (n=16)^Citation51	16 (100)	10 (62.5)	ND	5 (31.3)	3 (18.8)	2 (12.5)	0	0	0
Eguale et al, 2015^Citation52
S. Typhimurium (n=27)	4 (14.8)	6 (22.2)	3 (11.1)	1 (3.7)	1 (3.7)	0 (0)	0 (0)	0 (0)	1 (3.7)
S. Newport (n=2)	1 (50)	1 (50)	0 (0)	1 (50)	0 (0)	1 (50)	0 (0)	0 (0)	0 (0)
S. Virchow (n=21)	1 (4.8)	1 (4.8)	3 (14.3)	0 (0)	0 (0)	10 (47.6)	0 (0)	0 (0)	0 (0)
S. Kottbus (n=7)	0 (0)	0 (0)	1 (14.3)	0 (0)	1 (14.3)	0 (0)	0 (0)	1 (14.3)	0 (0)
S. Enteritidis (n=1)	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)
S. Braenderup (n=1)	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)
S. Concord (n=1)	1 (100)	1 (100)	1 (100)	1 (100)	0 (0)	0 (0)	1 (100)	1 (100)	0 (0)
S. Miami (n=3)	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)
S. Kentucky (n=2)	2 (100)	2 (100)	2 (100)	2 (100)	0 (0)	2 (100)	2 (100)	2 (100)	0 (0)
Gebregziabher et al (n=19)^Citation53	ND	17 (89.5)	17 (89.5)	11 (57.9)	15 (78.9)	6 (31.6)	3 (15.8)	0	2 (10.5)
Terfassa et al (n=30)^Citation54	27 (90)	ND	ND	ND	2 (6.6)	1 (3.3)	3 (10)	2 (6.7)	1 (3.3)
Asefa et al (n=29)^Citation55	29 (100)	ND	23 (79)	ND	9 (31)	ND	ND	0	0
Lamboro et al (n=19)^Citation56	ND	19 (100)	9 (47.6)	1 (5.3)	1 (5.3)	5 (26.3)	1 (5.3)	0	ND
Reda et al (28)^Citation57	28 (100)	28 (100)	20 (71.4)	ND	18 (64.3)	ND	1 (3.6)	ND	ND
Ameya et al (21)^Citation58	21 (100)	ND	ND	8 (38.1)	9 (42.9)	ND	4 (19)	0	ND

Abbreviations: AMP, Ampicillin; AMO, Amoxicillin; SXT, sulfamethoxazole-trimethoprim; NA, Nalidixic acid; CRO, Ceftriaxone; CIP, Ciprofloxacin; C, Chloramphenicol; CN, Gentamicin; T, Tetracycline; ND, Not Done.

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.

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

Authors Name, Number of Isolates and Reference	Antibiotics Resistance, n (%)
	AMP	GEN	CIP	C	S	T	CRO
Eguale et al, 2016^Citation22
S. Kentucky (n=5)	5 (100)	5 (100)	5 (100)	0 (0)	5 (100)	5 (100)	0 (0)
S. Virchow (n=5)	3 (60)	1 (20)	0 (0)	0 (0)	2 (40)	1 (20)	0 (0)
S. Saintpaul (n=6)	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)
S. Typhimurium (n=7)	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)
S. Dublin (n=3)	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)
Dagnew et al, 2020 (n=22)^Citation59	0 (0)	0 (0)	0 (0)	0 (0)	20 (90.1)	19 (86.4)	0 (0)
Worku et al, 2022 (n=23)^Citation60	ND	0 (0)	ND	ND	ND	6 (26)	0 (0)
Eguale 2018^Citation62
S. Saintpaul (n=20)	9 (45)	0 (0)	0 (0)	10 (50)	18 (90)	4 (20)	5 (25)
S. Typhimurium (n=3)	0 (0)	0 (0)	0 (0)	0 (0)	3 (100)	1 (33.3)	1 (33.3)
S. Kentucky (n=2)	2 (100)	2 (100)	2 (100)	1 (50)	2 (100)	2 (100)	0 (0)
Alemu and Zewde, 2012 (n=21)^Citation63	1 (4.8)	0 (0)	1 (4.8)	0 (0)	ND	2 (9.5)	0 (0)
Mustefa et al, (n=17)^Citation64	17 (100)	5 (29.4)	6 (35.2)	0 (0)	7 (41.1)	ND	0 (0)
Wabeto et al, 2017 (n=56)^Citation66	26 (46.4)	7 (12.5)	4 (7.1)	29 (51.8)	37 (66)	47 (83.9)	13 (23.2)
Addis et al, 2011 (n=21)^Citation67	21 (100)	4 (19)	0 (0)	2 (9.5)	16 (76.2)	7 (33.3)	ND
Takele et al, 2018 (n=42)^Citation68	13 (31)	3 (7)	0 (0)	3 (7)	10 (23.8)	10 (23.8)	0 (0)
Mohammed and Gebremedhin (n=21)^Citation69	7 (33.3)	(4.8)	(4.8)	7 (33.3)	13 (61.9)	15 (71)	ND
Sibhat et al, 2011^Citation70
S. Typhimurium (n=1)	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)	0 (0)
S. Newport (n=13)	0 (0)	0 (0)	0 (0)	0 (0)	4 (66.7)	0 (0)	0 (0)
S. Anatum (n=39)	2 (66.7)	0 (0)	0 (0)	0 (0)	3 (100)	2 (66.7)	0 (0)
Usmael et al, 2022^Citation71	11 (41.7)	0 (0)	ND	ND	ND	9 (21.2)	ND
Belachew et al, 20 (n=71)^Citation72	38 (53.5)	7 (10)	ND	47 (66.7)	43 (60.6)	56 (79)	ND

Abbreviations: AMP, Ampicillin; GEN, Gentamycin; CIP, ciprofloxacin; CAF, Chloramphenicol; S, streptomycin; TTC, tetracycline; CRO, ceftriaxone; ND, Not done.

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.