Prevalence and antimicrobial susceptibility profile of Listeria monocytogenes in humans, animals, and foods of animal origin in Ethiopia: a systematic review and meta-analysis

Abstract

Listeria monocytogenes is a food-borne bacterial pathogen known to cause a burden on human health and food safety globally. Regardless of the few available studies on Listeria monocytogenes, there is no comprehensive evidence of its prevalence and antimicrobial susceptibility in Ethiopia. We conducted to estimate the pooled prevalence and antimicrobial susceptibility profile of Listeria monocytogenes from various sources in Ethiopia. The study was conducted according to the Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA) Checklist. The quality of the studies was assessed based on the Newcastle–Ottawa scale. We found 18 studies that fit our inclusion criteria. Results were synthesized with random-effects meta-analyses and meta-regressions to evaluate heterogeneity between studies. The pooled prevalence of Listeria monocytogenes from various sources in Ethiopia was 4.2% (95% CI, 2.13, 6.22). The pooled prevalence was higher in human subjects 6.4% (95% CI, 0.27–15.6) when compared to animals 4.7% (95% CI, −0.40 to 9.1) and foods of animal origin 5.1% (95% CI, 0.42–10.6). Higher rate of resistance of Listeria monocytogenes against tetracycline (72.7%), amoxicillin (63.7%), nalidixic acid (63.6%), penicillin (63.6%), and cephalothin (54.5%) was observed. The prevalence of Listeria monocytogenes and the occurrence of resistant isolates in different source populations warn of a potential future threat to public health. Hence, increasing public awareness and designing effective policies and disease control measures are strongly recommended.

Keywords:

• Antimicrobial resistance
• Listeria monocytogenes
• meta-analysis
• systematic review

REVIEWING EDITOR:

• Pedro González-Redondo, [email protected], Senior Editor, University of Seville, Seville, Spain

SUBJECTS:

• Bioscience
• Epidemiology
• Food microbiology
• Food safety management

1. Introduction

Food-borne bacterial pathogens are compromising food safety and human health as a results of consuming animal products contaminated with vegetative pathogens or their toxins. Diverse food-borne zoonotic bacterial pathogens cause two-third of human food-borne infections globally, with under-developed nations bearing a disproportionate burden (Abebe et al., 2020). As stated by the WHO, 30% of the population in wealthy nations suffer from food-borne illnesses each year, with up to 2 million fatalities expected in underdeveloped countries (Abunna et al., 2016).

In Ethiopia, foodborne bacterial pathogens are the commonest cause of foodborne illness. Among these, the Diarrheagenic Escherichia coli (DEC), Non typhoidal Salmonella (NTS), Shigella spp. Listeria monocytogens and Campylobacter spp. are responsible for a large proportion of illnesses, deaths; and, particularly, as causes of acute diarrheal diseases (Asfaw et al., 2022). Moreover, all isolated foodborne bacterial pathogens showed high rates of antimicrobial resistance (AMR). In particular, the most studied foodborne pathogens, Staphylococcus spp., Salmonella spp., Listeria spp., and E. coli from specific sources, showing high levels of resistance to most of the antibiotics prescribed in Ethiopia. The occurrence and persistence of AMR in food is one of the main factors causing the spread of antimicrobial resistance in different compartments, humans, animals and the environment (Belina et al., 2021).

Listeriosis is a serious food-borne zoonotic illness that affects human health (Van de Venter, 1999). Listeria monocytogenes is the principal causative agent of listeriosis among the several species of the genus Listeria (Vitas & Garcia-Jalon, 2004). It is one of the most virulent pathogens that needs collaboration among different agencies across the globe to control and prevent (Odu & Okonko, 2017). Listeria monocytogenes is associated with a high case fatality rate of around 30%, unlike infection with other common foodborne pathogens (Mulu & Pal, 2016).

Listeria monocytogenes is frequently isolated from food of animal origins such as ready-to-eat meat and meat products (sausages) (Garedew et al., 2015) fish and fish products (Nayak et al., 2015), milk, and pasteurized dairy products like soft cheese (Hwa et al., 2015). Human infection with listeriosis from animal sources has been shown to be an occupational risk, particularly among farmers, butchers, poultry workers, and veterinary surgeons (Seyoum et al., 2015). Listeria species grow at temperatures ranging from 0 °C to 45 °C, making it a food-borne pathogen in chilled, refrigerated, and ready-to-eat foods. The occurrence of Listeria species in refrigerators and various frozen foods ranged from 1% to 60% and 1.3% to 73.9%, respectively (Cabedo et al., 2008). In healthy humans, the disease spectrum can vary from a moderate and self-limiting flu-like illness or febrile gastroenteritis to serious systemic infections such as meningitis, septicemia, and abortion in vulnerable persons (Rahimi et al., 2015).

In Ethiopia, the culture of consuming raw meat (Kurt, Kitfo, and Dulet) and milk (raw milk, cottage cheese, cream cake) products supplemented with the presence of a high-risk population, inadequate sanitary conditions, and poor personal hygiene may pose a high risk of being infected by Listeria monocytogenes (Tassew et al., 2010). Humans can also acquire resistant Listeria monocytogenes organism via direct contact with contaminated animals and indirect exposure through consumption of food of animal origin. In addition to the occurrence of foodborne zoonotic pathogens like Listeria monocytogenes, the increased demands for animal-sourced protein have brought an uncontrolled use of antimicrobials in food-producing animals which facilitate the emergence of antimicrobial resistance. Likewise, studies in Ethiopia and elsewhere indicated the presence of antimicrobial-resistant and multidrug-resistant Listeria monocytogenes in raw food of animal products suggesting an important public health implication (Derra et al., 2013; Gebretsadik et al., 2011; Sharma et al., 2012).

Despite some local information on the prevalence and antimicrobial susceptibility pattern of Listeria monocytogenes from different sources (Derra et al., 2013; Gebretsadik et al., 2011; Seyoum et al., 2015; Tassew et al., 2010; Vaidya et al., 2018), there is no nationwide comprehensive data generated from a pooled estimate of the results of individual studies. Hence, this review aims to investigate the prevalence and antimicrobial susceptibility of Listeria monocytogenes in humans, animals, and foods of animal origin. The findings of the current study can provide useful epidemiological data to control and prevent the disease and curb the emergence and spread of antimicrobial resistance.

2. Methods

2.1. Study design

This study was carried out based on the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) Statement and Reporting Guidelines for Observational Studies (Von Elm et al., 2008) and Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA) Checklist (Page and Moher, 2017). The guidelines included study design, literature search, study eligibility criteria, selection procedures, data extraction, and analysis. The study protocol is registered on PROSPERO with reference ID: CRD 42021249639.

2.2. Literature search strategies

A comprehensive literature search was carried out for articles published from 2000 to 2022 on biomedical databases such as Google Scholar, Science Direct, PubMed, Medline, Web of Science, and Cochrane Library. Experts and researchers were also contacted for a potential source of articles. The following MeSH terms, ‘Listeriosis’ or ‘Listeria’ or ‘Listeria monocytogenes’, and ‘Human’, ‘Animal’, ‘Food’ and ‘Prevalence’ and ‘antibiotic resistance’ or ‘antimicrobial susceptibility’, and ‘Ethiopia’ and the Boolean operating connector (AND and OR), and truncation were used for the above-listed databases for appropriate search and identification of literature. When search engines provided abstract only and a link for free to access full-text articles, we further searched some research website as ResearchGate, which offer an option of direct full-text requests from authors.

2.3. Study eligibility criteria

All articles that report the prevalence and antimicrobial susceptibility profile of Listeria monocytogenes in humans, animals, or foods of animal origin in Ethiopia were downloaded. Studies published in English, conducted in Ethiopia, cross-sectional studies, studies conducted in the period 2000–2022 and reporting the prevalence of the organism in human-animal and food of animal origin and studies with antibiotic susceptibility test done in a laboratory setting were included. Articles that did not have full text, with inadequate sample size, not followed standard diagnosis, and duplicate articles were excluded.

2.4. Study selection procedures

Articles that met the above criteria were considered for the final meta-analysis and systematic review. Articles identified from different sources were exported to the Mendeley reference manager to avoid missing data and to remove duplicates. Two authors screened the article’s full text for eligibility criteria for the final decision. In case differences were found between the authors, whether to include or not, the author resolved the issues via discussion and consensus.

2.5. Data extraction

Data extraction was done on a predesigned suitable data extraction format on Microsoft excel version 2013 developed for this purpose. Two authors independently extracted the data related to study characteristics (Primary author, study area, quality score, sample size, diagnosis method, sample type, study population, and prevalence). Besides, the number of positive isolates, the antimicrobial agents used, and the resistance profile were extracted. The two authors then cross-checked and compared the extracted data to avoid duplicates and missing data.

2.6. Article quality assessment

The quality of each study was assessed using the Newcastle–Ottawa scale adapted for cross-sectional studies (Modesti, 2016) and graded out of 10 points (10 stars). The scale has three main sections; (1) selection of representative sample and ascertainment of exposure, (2) comparability of subjects and confounding factors controlled, and (3) assessment of outcomes and statistical test used for analysis which accounted 5, 2, and 3 maximum stars respectively. The average score of the two authors was considered and articles that scored equal to or greater than five total stars were included in systematic review and meta-analysis.

2.7. Data processing and analysis

Relevant data were extracted on Microsoft excel format. The data prepared on Microsoft excel were imported to STATA 16.0 software for analysis of pooled estimate of outcome measures and subgroup analysis. The random effect model was used to estimate the pooled prevalence and resistance rate of Listeria monocytogenes to different antimicrobials. The estimated pooled prevalence with a 95% confidence interval was presented by forest plot and the presence of publication bias using a funnel plot. Sub group analysis was conducted to determine the potential sources of heterogeneity among studies based on the study population, publication year and region. Heterogeneity among reported prevalence was assessed by computing p-values of the Cochrane Q-test and I² statics. Cochrane Q-test evaluates the existence of heterogeneity and p < .1 was considered as statistically significant. The I² statistics provides an estimate of the percentage of the variability in effect estimates that is due to heterogeneity rather than sampling error or chance differences (Rücker et al., 2008). Begg’s rank test and Egger’s tests at a 5% significant level were used to check publication bias. Begg’s rank test was used to examine the correlation between the effect sizes and their corresponding sampling variances and a strong correlation implies publication bias. Egger’s test regresses the standardized effect sizes on their precisions; in the absence of publication bias, the regression intercept is expected to be zero (Lin & Chu, 2018).

3. Results

The database search yielded a total of 104 studies. Mendeley and manual tracing found 36 duplicate studies, and removed. The remaining 68 studies were further screened, and 20 studies were excluded because they were review articles, only viewed abstracts, limited to the genus Listeria, or books. A review of 48 articles revealed that 19 did not report the prevalence or total number of isolates. Furthermore, 11 studies had methodological flaws and unrepresentative sample size. Finally, 18 studies that met the eligibility requirements, were evaluated for quality and subjected to a systematic review and meta-analysis (Figure 1). Eligible studies were divided into two groups: those that reported on the prevalence of Listeria monocytogenes or its antimicrobial resistance pattern, and those that reported on both the prevalence and the antimicrobial resistance pattern of Listeria monocytogenes.

Figure 1. Flow chart of study selection for systematic review and meta-analysis of the prevalence of Listeria monocytogenes in Ethiopia.

3.1. Description of search results

All the included 18 studies (Table 1) were cross-sectional in their study design and published from 2000 to 2022. The total sample size for these selected studies was 5527 (ranging from 35 to 768). These studies were conducted in three regional states, namely Tigray, Amhara, and Oromia, and Addis Ababa city in Ethiopia. Half (50%) of the studies were conducted in the Oromia region (Ahimed et al., 2022; Borena et al., 2022; Gebremedhin et al., 2021; Girma et al., 2021; Hussien et al., 2021; Mereta et al., 2020; Seyoum et al., 2015; Teshome et al., 2019; Wosilla et al., 2013). The studies involved humans, animals, and food of animal origin; 75% of the studies were conducted on foods of animal origin whereas only 25% of the studies were conducted on humans and animals. From 18 studies, 10 reported the antimicrobial susceptibility profile of Listeria. monocytogenes for 15 antimicrobials. The inclusion of antimicrobials in each study ranged from 7 to 13 antimicrobials and 55% of the studies tested the susceptibility of Listeria monocytogenes to nine or more antimicrobials.

Table 1. Summary of 18 studies reporting the prevalence of Listeria monocytogenes in different parts of Ethiopia, from 2000 to 2022.

Studies	Score	Year of Publication	Region	Study area	Study population	Sample size	Sample type	Diagnosis Method	Prevalence %
Molla et al.	6	2004	Addis Ababa	Addis Ababa	FoAO	316	Milk, Meat products	Culture	5.1
Gebretsadik et al.	9	2011	Addis Ababa	Addis Ababa	FoAO	391	RtEF	Culture	5.4
Derra et al.	7	2013	Addis Ababa	Addis Ababa	FoAO	240	Milk, Meat products	Culture	4.1
Wosilla et al.	6	2013	Oromia	Jimma	FoAO	200	Milk, Milk products	Culture	4.0
Garedew et al.	7	2015	Amhara	Gondar	FoAO	384	RtEF	Culture	6.3
Seyoum et al.	6	2015	Oromia	Central Ethiopia	FoAO	443	Milk and milk products	Culture	5.6
Mulu and Pal.	5	2016	Addis Ababa	Addis Ababa	Animal	384	Sheep carcass	Culture	4.1
Fisseha.	5	2017	Addis Ababa	Addis Ababa	FoAO	340	RtEF	Culture	5.8
Girma and Abebe.	6	2018	Amhara	Debre-Birhan	FoAO	407	Raw bovine milk	Culture	8.8
Weldekidan et al.	8	2019	Tigray	Mekele	Human	141	Blood	Culture	8.5
Mereta et al.	6	2020	Oromia	Jimma Town	FoAO	100	Meat	Culture	7.0
Teshome et al.	5	2019	Oromia	Bishoftu and Dukem	FoAO	200	Milk and milk products	Culture	5.0
Gebremedhin et al.	7	2021	Oromia	Ambo and Holeta	Animal	450	Carcass and blood	Culture	4.4
Ahimed et al.	7	2022	Oromia	Haramaya	Animal	200	feces and animal feed	Culture	5.5
Borena et al.	8	2022	Oromia	Ambo, Holeta and Bako	FoAO	384	Milk and milk products	Culture	2.3
Girma et al.	8	2021	Oromia	Jimma	Human	144	Blood	Culture	5.6
Hussien et al.	7	2021	Oromia	Borena	FoAO	35	Milk and Milk products	Culture	3.2
Kidanu et al.	6	2021	Tigray	Mekele	FoAO	768	Milk and Meat	Culture	3.4

FoAO: Food of animal origin; RtEF: Ready to eat food; Env’t: Environment.

3.2. Prevalence of Listeria monocytogenes

The result of the meta-analysis from the forest plot showed that the pooled prevalence of Listeria monocytogenes in Ethiopia was 4.2% (95% CI: 2.13, 6.22), ranging from 2.3 to 8.8% (Figure 2). There was no heterogeneity observed across the included studies (I² = 0.00%; Q = 2.00; p = 1.00). However, a random effect model with a restricted maximum-likelihood method was used to estimate the pooled prevalence of Listeria monocytogenes from different sources in Ethiopia. The lowest and highest prevalence’s of Listeria monocytogenes were reported from milk products (cottage cheese and curdled milk) (2.3%) (Borena et al., 2022) and raw bovine milk (8.8%) (Girma & Abebe, 2018) respectively.

Figure 2. Forest plot of the pooled prevalence of Listeria monocytogenes in different parts of Ethiopia.

The funnel plot for publication bias showed an asymmetrical distribution of the effect estimate (Figure 3). However, Begg’s and Egger’s tests showed that there was no statistically significant publication bias in estimating the prevalence of Listeria monocytogenes from different sources (p = .06).

Figure 3. Funnel plot with 95% confidence limits of the prevalence of Listeria monocytogenes in different parts of Ethiopia.

3.2.1. Sub-group analysis

A subgroup analysis was conducted based on publication year, study region, and study population (Table 2). The highest pooled prevalence was recorded in the Amhara region at 7.1% (95% CI: 0.29–17.1), while the lowest prevalence in Oromia 3.9% (95% CI: 0.1–6.4%). The pooled prevalence of Addis Ababa 4.5% (95% CI, 0.01–9.0) and Tigray 4.1% (95% CI, 0.21–10.3) were slightly comparable. With regards to publication year, the prevalence of Listeria monocytogenes was 5.1% (95% CI −0.49 to 15.1) and 5.2% (95% CI −0.01 to 26.2) in studies that were published from 2000 to 2011 and 2012 to 2022, respectively. The results of subgroup analysis based on the study population showed that the pooled prevalence was higher in human subjects 6.4% (95% CI, 0.27–15.6) when compared to animals 4.7% (95% CI, −0.40 to 9.1) and FoAO 5.1% (95% CI, 0.42 to 10.6), but there is no statistically significant difference among subgroups.

Table 2. Subgroup estimate pooled prevalence of Listeria monocytogenes in animal, human and food of animal origin in Ethiopia.

Variables	Characteristics	Included studies	Sample size	Pooled prevalence 95% CI
Publication Year	2000–2011	1	316	5.1(−0.49 to 15.1)
	2012–2022	17	3211	5.2(−0.01 to 26.2)
Region	Addis Ababa	5	1331	4.5(0.01 to 9.0)
	Oromia	9	2496	3.9(0.13 to 6.4)
	Amhara	2	791	7.1(−0.29 to 17.1)
	Tigray	2	909	4.1(−0.21 to 10.3)
Study Population	FoAO	13	4208	5.1(0.42 to 10.6)
	Human	2	285	6.4(0.27 to 15.6)
	Animal	3	1034	4.7(−0.40 to 9.1)

3.3. Antimicrobial resistance profile of Listeria monocytogenes

To determine the antimicrobial susceptibility of Listeria monocytogenes isolates, all eligible studies used the disk diffusion technique. The isolates showed varying degrees of susceptibility to the antimicrobials tested. Over 60% of Listeria monocytogenes isolates were resistant to tetracycline, nalidixic acid, and penicillin. While more than 45% of the isolates were susceptible to gentamicin, streptomycin, and amoxicillin (Table 3).

Table 3. Antibacterial resistance rates of Listeria monocytogenes from various sources in Ethiopia, from 2000 to 2022.

Studies	Study Population	No. of Isolate	AMP	CL	T	NA	CF	P	T/S	GM	CIP	V	STR	CD	AML	OT	E
Garedew et al.	FoAO	24	_	11.6	37.5	50	_	66.7	0	0	_	0	_	_	0	_	_
Mulu and Pal.	Animal	36	11.1	8.3	60	_	19.4	_	19.4	2.8	25	5.8	11.1	5.6	0	19.4	_
Weldekidan et al.	Human	12	_	40	_	_	_	66.7	_	_	_	50	_	66.7	50	_	25
Girma and Abebe.	Animal	36	_	22.2	25	30.5	_	_	_	_	_	0	11.1	_	11.6	_	_
Fisseha	FoAO	20	10	_	15	40	10	80	10	_	30	_	0	_	_	0	_
Gebremedhin et al.	Animal	20	25	60	55	70	_	25	_	_	_	10	_	15	5	80	30
Mereta et al.	FoAO	2	_	24	59	100	_	76	_	0	_	0	_	_	0	_	_
Kidanu et al.	FoAO	26	0	_	_	96	48	11.5	_	0	0	0	15.4	_	0	_	3.9
Ahimed et al.	Animal	11	0	_	54.5	_	_	9.1	_	0	_	_	27.3	_	27.3	_	0
Borena et al.	FoAO	11	72.7	_	36.4	54.6	27.3	_	_	0	_	82.2	_	_	90.9	_	_

AMP: Ampicillin; AML: Amoxicillin; E: Erythromycin; STR: Streptomycin; T: Tetracycline; NA: Nalidixic acid; P: Penicillin; CF: Cephalothin; GM: Gentamicin; CIP: Ciprofloxacin; CL: Chloramphenicol; T/S: Trimethoprim-sulfamethoxazole; CD: Clindamycin; K: Kanamycin; OT: Oxytetracycline; V: Vancomycin; ‘_’ not tested.

The resistance rates of Listeria monocytogenes isolates to 15 antimicrobials were found to be variable, ranging from 3.9 to 100%. A single study found that all (100%) Listeria monocytogenes isolates were resistant to nalidixic acid. The isolates had significantly higher resistance rates to Tetracycline (72.7%), Nalidixic acid (63.6%), Penicillin (63.6%), and Cephalothin (54.5%). The isolates were relatively sensitive to Gentamicin (83.3%) and Amoxicillin (36.3%), but this was not statistically significant.

3.3.1. Sub-group analysis

A subgroup analysis by the study population indicated that the pooled resistance rate of Listeria monocytogenes isolates from humans showed a higher resistance rate against both penicillin and clindamycin 66.7% (95% CI: 43.18–90.22) and amoxicillin 45.80% (95% CI: 22.31, 69.29). Listeria monocytogenes from animals showed a higher resistance rate against nalidixic acid 70% (95% CI: 30.80, 109.20), oxytetracycline 57.1% (95% CI: 0.50, 114.68), tetracycline 54.9% (95% CI: 36.73, 73.32), and cephalothin 42.8% (95% CI: −4.92, 90.55). Listeria monocytogenes isolates from FoAO showed a higher resistance rate to nalidixic acid 70.2% (95% CI: 44.07, 96.44), penicillin 65.7% (95% CI: 42.24, 89.25), and tetracycline 42.7% (95% CI: 22.77, 62.60) (Table 4).

Table 4. Percentage of pooled resistance rates of antimicrobials to Listeria monocytogenes isolates from human, animal and food of animal origin in Ethiopia, from 2000 to 2022.

Antimicrobials	Pooled antimicrobial resistance rate (95% CI)
	Animal	FoAO	Human
Ampicillin	6.1 (−12.09, 24.41)	31.5 (−15.82, 78.87)	–
Cephalothin	42.8 (−4.92, 90.55)	23.9 (20.01, 27.82)	36.2 (15.91, 60.53)
Tetracycline	54.9 (36.73, 73.32)	42.7 (22.77, 62.60)	25.0 (−45.56, 95.56)
Nalidixic acid	70.0 (30.80, 109.20)	70.3 (44.07, 96.44)	30.5 (−40.06, 101.06)
Chloramphenicol	19.4 (−51.16, 89.96)	26.3 (8.56, 43.98)	–
Penicillin	12.8 (−6.10, 31.68)	65.7 (42.24, 89.25)	66.7 (43.18, 90.22)
Trimethoprim-sulfamethoxazole	19.4 (−51.16, 89.96)	5.9 (42.24, 89.25)	–
Gentamicin	0.2 (−20.38, 20.86)	0.0 (−3.83, 3.83)	–
Ciprofloxacin	25.0 (−45.56, 95.56)	18.8 (−12.22, 49.92)	–
Vancomycin	9.0 (−25.26, 43.28)	22.7 (−20.52, 65.86)	36.5 (−6.97, 80.01)
Streptomycin	25.9 (5.30, 46.54)	5.7 (−25.35, 36.80)	11.1 (−59.46, 81.66)
Clindamycin	12.8 (−21.48, 47.05)	–	66.7 (43.18, 90.22)
Amoxicillin	20.6 (2.39, 38.89)	24.7 (−22.53, 71.99)	45.8 (22.31, 69.29)
Oxytetracycline	57.1 (−0.50, 114.68)	–	–
Erythromycin	10.3 (−17.60, 38.30)	3.9 (−47.06, 54.86)	25.0 (1.48, 48.52)

4. Discussion

Listeria monocytogenes as a significant food-borne zoonotic disease has serious clinical consequences and a high case fatality rate in susceptible individuals (Shamloo et al., 2019). This is especially concerning when isolates are resistant to antimicrobials frequently used in livestock and humans. Yet no national estimates exist for prevalence and susceptibility profile in different source populations. Hence, we synthesized the prevalence and antimicrobial susceptibility profile of Listeria monocytogenes in humans, animals, and food of animal origin in Ethiopia.

According to the current meta-analysis, the pooled prevalence of Listeria monocytogenes is 4.2%. The low prevalence in the current review might be due to the apparent trend of low prevalence of Listeria monocytogenes in the general population, despite frequent isolation from various sources. The prevalence is expected to be higher in vulnerable populations, such as pregnant women. The result was slightly higher than the global prevalence in selected ready to eat foods (Churchill et al., 2019) but lower than a study conducted in south east Asia (Jibo et al., 2022), Iran (Ranjbar & Halaji, 2018) and Lebanon (Harakeh et al., 2009). The above variation could be explained by the methods of diagnosis, characteristics of the study population and higher number of studies included in this systematic review and meta-analysis.

The finding also showed a significant level of Listeria monocytogenes contamination in raw milk (8.8%). This is consistent with findings from other studies (Morobe et al., 2009; Moshoeshoe, 2013; Shourav et al., 2020). This high prevalence of Listeria monocytogenes in milk could be attributed to poor milking hygiene as well as the practices of mixing milk from different sources and adulterating it with water before selling it to the consumer, which increases the chances of contamination (Borena et al., 2022).

The Amhara region has a higher pooled prevalence of Listeria monocytogenes (7.1%) than reports from the other two regions. This could be due to the sample types (raw milk, meat, and ready-to-eat food) used in the studies from the Amhara region that are included in the current systematic review and meta-analysis. The samples were sourced from animal producers, butchers, vendors, and restaurants, all of which are prone to contamination and provide an ideal environment for Listeria monocytogenes growth and multiplication (Gebremedhin et al., 2021).

Aggregate pooled prevalence estimation revealed that humans (6.4%) had a higher prevalence of Listeria monocytogenes than animals and foods of animal origin. This might be because both human studies involved pregnant women which are vulnerable to Listeria monocytogenes infection compared to other human population. Pregnant women were reported to be 20 times more likely than the general population to develop listeriosis (Frederick and Daniel, 1996). In addition, one study was conducted on women with a history of fetal loss, reinforcing Listeria monocytogenes as a probable cause of reproductive health problems. The finding agrees with a report from Iran (Ranjbar & Halaji, 2018), in which the prevalence of Listeria monocytogenes isolates was higher in pregnant women and hospitalized patients. The estimated pooled prevalence of Listeria monocytogenes from various sources did not change within a two-decade period, from 2000 to 2010 (5.1%) and 2011 to 2022 (5.2%). This could indicate that no progress has been made in terms of implementing appropriate disease control strategies. The overall estimate of Listeria monocytogenes prevalence among animal origin was 4.7%. A higher prevalence was reported by the studies conducted in Iran 9% (Ranjbar & Halaji, 2018) and India 5.7% (Raorane et al., 2014). The observed variation could be due to the characteristics of the study population, the diagnostic technique used, and geographical differences.

In the present study, a higher pooled rate of resistance of Listeria monocytogenes isolates was recorded for tetracycline 72.7%, nalidixic acid 63.6%, penicillin 63.6%, and cephalothin 54.5%. On the other hand, Mpundu et al. (2021) reported a higher rate of resistance to penicillin (80%) and cephalosporin (47%). The difference could be due to the study population; the previous study only included isolates from foods of animal origin. Another significant finding was the presence of antimicrobials that were effective against Listeria monocytogenes isolates, such as gentamicin and erythromycin.

Listeria monocytogenes isolates from humans were resistant to penicillin, clindamycin (66.7%), and amoxicillin (45.7%). The finding was comparable to that of Khademi & Sahebkar, (2019), who reported a high resistance rate to penicillin and amoxicillin (56.8% and 29.5%, respectively). However, this result was lower than a study reported by Harakeh et al. (2009), who noted the highest resistance against amoxacillin (93.33%), followed by penicillin (90%). The widespread use of these antibiotics as first-line treatments for listeriosis, as well as the acquisition of resistance determinants through microbes originating from food of animal origin and from other bacteria may explain the high level of resistance in humans (Abdollahzadeh et al., 2016; Escolar et al., 2017; Olaimat et al., 2018). Vancomycin is also indicated for the treatment of severe listeriosis in patients who are allergic to penicillin (Abdollahzadeh et al., 2016). The prevalence of vancomycin-resistant Listeria monocytogenes was slightly high at 36.5%.

Listeria monocytogenes isolates in these studies were highly resistant to tetracycline, penicillin, cephalothin, and nalidixic acid in animals and foods of animal origin. This is consistent with the previous report by Obaidat et al. (2015), who assessed antimicrobial resistance in Listeria monocytogenes isolates from three countries viz. India, Yemen and Egypt. A study conducted on Listeria spp. isolated from cattle farm in Bangladesh (Shourav et al., 2020) reported similar resistance patterns to penicillin, ampicillin, erythromycin, and cephalothin. The reported high rate of resistance to penicillin and tetracycline may be due to the frequent, long-term, and extensive use of these antimicrobials for bacterial infection, which is mostly based on empirical therapy (Beyene et al., 2015; Gemeda et al., 2020; Kifle & Tadesse, 2014). A high rate of resistance to cephalothin might be due to resistant determinants from the use of other beta-lactam antimicrobials, such as penicillin and ampicillin.

5. Conclusion

Despite the overall pooled prevalence of Listeria monocytogenes in Ethiopia might seem low; however, a high pooled prevalence of Listeria monocytogenes was recorded in in pregnant humans. A high rate of resistance to commonly used and highly important antimicrobials for both animal and human medicine was reported in Listeria monocytogenes isolates from foods of animal origin. It also highlighted the need to understand the possible linkages and flow patterns of resistant bacteria at the animal-food-human interface to lessen the threat to public health. Therefore, emphasis shall be given to health education about the source of contamination, proper disposal of wastes, and improved food safety measures to reduce the risk of listeriosis. To reduce the occurrence and spread of resistant bacteria, antimicrobial usage should be controlled and regulated in animal husbandry and treatment of human illness. Furthermore, to tackle the threat of antimicrobial resistance, further molecular-based studies are required to recognize the transmission pathway of resistant bacteria and their genetic determinants at the animal-food-human interface.

Authors contributions

T.T. conducted the meta-analysis; T.Z. and T.E. assisted with data analysis and figures. T.T. drafted the initial manuscript, and O.G. and T.K. contributed to the text and re-visions. T.Z, O.G. and T.K. decided the criteria for article screening, screened articles, extracted data for the meta-analysis, contributed to data analysis and figures, and edited the manuscript. All authors have read and agreed to the published version of the manuscript.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Additional information

Funding

This research received no external funding