An insight into the antibiotic resistance profiles of ESKAPE pathogens isolated from humans in Africa: a systematic review and meta-analysis

Abstract

Background

The ESKAPE (Enterococcus faecium, Staphylococcus aureus, Klebsiella pneumoniae, Acinetobacter baumannii, Pseudomonas aeruginosa, and Enterobacter species) pathogens exhibited widespread resistance to multiple antibiotic classes. This study investigated the prevalence of antibiotic resistance (ABR) amongst ESKAPE pathogens in humans in Africa.

Materials and methods

The systematic review protocol was registered in the International Prospective Register of Systematic Reviews [ID no: CRD42024552173]. A systematic review of the English literature was conducted to collect and analysed data on the prevalence of antibiotic resistance (ABR) caused by ESKAPE pathogens in Africa, covering the period from January 2014 to February 2024. They were provided from three databases (PubMed, Web of Science and ScienceDirect). A total of 268 studies were retrieved and at the end of the screening, 31 full texts were eligible for inclusion in the meta-analysis.

Results

The overall pooled prevalence estimate (PPE) of ESKAPE pathogens in Africa revealed the following distribution: S. aureus (23.1%), K. pneumoniae (20.9%), E. faecium (9.8%), and Enterobacter spp. (5.3%). The prevalence of ABR in ESKAPE pathogens was reported in 12.9% (7/54) countries from various regions of Africa, and the random-effects models showed that Enterobacter spp. documented more resistance against amoxicillin-clavulanate with a pooled prevalence estimate (PPE) of 95.3% (95%CI: 79.8–99.2), E. faecium antibiotic resistance was higher against tetracycline with a PPE of 47.0% (95%CI: 2.3–97.0). Furthermore, PPE of K. pneumoniae resistance against trimethoprim-sulfamethoxazole was 40.7% (95%CI: 12.6–76.6), whilst S. aureus was mostly resistant against ceftriaxone with a PPE of 94.5% (95%CI: 82.0–98.5). Thirteen studies reported 1532 isolates with multidrug resistance to at least three antibiotic classes, yielding PPE of 64.1%. Interestingly, this meta-analysis revealed that the bla_CTX-M gene had the highest prevalence (37.6%) among the examined genes, followed by the mecA gene (31.5%), and the bla_TEM gene, which was reported in only three studies with a PPE of 13.0%.

Conclusion

There is a significant knowledge gap in published studies on ABR among ESKAPE pathogens in most African countries. This observation calls for consolidated efforts to conduct research on this subject in the continent, perhaps with support from regional organizations and the African Union.

Clinical Trial

Not applicable.

Supplementary information

The online version contains supplementary material available at 10.1186/s12879-025-12109-5.

Background

Antibiotic resistance (ABR) presents a major challenge towards achieving universal health care and impedes the accomplishment of several of the sustainable development goals (SDGs), including: (i) zero hunger, improved nutrition, food security, and sustainable agriculture (SDG 2); (ii) good health and well-being (SDG 3); and (iii) clean water and sanitation (SDG 6) [1]. To tackle the threat of ABR, the World Health Organization (WHO) developed a list of antibiotic-resistant, global priority pathogens in 2017 to aid in the research and development of new and effective antibiotic treatments [2]. Established according to multi-criteria analyses, the list was ranked into three priority tiers: medium, high, and critical [3]. Within the “Priority 1: Critical” pathogen group on the WHOs priority pathogens list are carbapenem-resistant Enterobacterales, third-generation cephalosporin-resistant Enterobacterales, and carbapenem-resistant Acinetobacter baumannii, while the high group included vancomycin-resistant Enterococcus faecium, carbapenem-resistant Pseudomonas aeruginosa, and methicillin-resistant Staphylococcus aureus [4]. These pathogens contribute significantly to the burden of disease in developed and developing nations and are frequently isolated from clinical settings where they are associated with several life-threatening, hospital-acquired (HA) infections [5].

Over the past decade, antibiotic resistance (ABR) in Africa, particularly among ESKAPE pathogens, has become a significant public health concern, with substantial increases in resistance observed for certain antibiotics [6]. Several systematic and meta-analysis studies have been carried out to investigate the prevalence of ABR in ESKAPE pathogens worldwide [7–9]. The study conducted Regassa et al. [10] in Ethiopia tested antibiotic sensitivity patterns on 840 culture isolates, whereby, Escherichia coli strains which revealed more than 57% resistance to seventeen antibiotics. Whilst Klebsiella pneumoniae showed nearly 70% resistance rates to 17 of the antibiotics used. The total detected multidrug resistance (MDR) was 64.29%; the highest MDR was reported in A. baumanni strains (84%) and K. pneumoniae (80%). A study by Arbune et al. [11] reported a concerning rise in ABR among key pathogens, including Methicillin-resistant S. aureus (86.6%), A. baumannii (36.8%), P. aeruginosa (29.1%), and K. pneumoniae (24.4%). Notably, these organisms also exhibited high levels of multidrug resistance (MDR).

It is thus well established that the ESKAPE pathogens exhibit resistance to several major classes of antibiotics, including macrolides, tetracyclines, oxazolidinones, β-lactams, lipopeptides, β-lactam-β-lactamase inhibitor combinations, as well as last-line antibiotics such as glycopeptides, carbapenems, and polymyxins [12]. One of the main drivers behind the development of ABR is the misuse and overuse of antibacterial agents [13]. Hence, the understanding of the administration and management of them can assist in curbing ABR globally [13, 14]. The aim of this study was to provide a systematic and meta-analytic review of the prevalence of antibiotic resistance patterns for ESKAPE pathogens in the African population.

Methods

Protocol registration

This study was registered in the International Prospective Register of Systematic Reviews (PROSPERO) with registration no: CRD42024552173.

Study design and systematic review protocol

As shown in Fig. 1, this systematic review and meta-analysis was carried out in accordance with the Preferred Reporting Items for Systematic Reviews and Meta-analyses (PRISMA) criteria [15], as confirmed by a checklist (Supplementary Table S1). Data extraction, screening, and analysis entailed scanning database systems for potentially relevant articles, evaluating their relevance, and determining if they were suitable for review. This review was conducted using published studies performed in Africa.

Fig. 1.

Prisma flow diagram demonstrating the search and selection process of included studies in the review

Search strategy

A comprehensive literature search was performed using the criteria outlined in Supplementary Table S1. The search spanned publications from 2014 to 2024 and covered three major databases: PubMed, ScienceDirect, and Web of Science. Duplicates were eliminated once the findings were imported into Microsoft Excel. Full-text papers were evaluated for eligibility after titles and abstracts were filtered. Two independent reviewers conducted each search and screening, and disagreements were settled by consensus.

Inclusion criteria

Following a careful analysis of the titles and abstracts, the studies were chosen for further screening. All of the articles considered in the study have to meet the following requirements: be original research articles without geographical limitations (Africa); full texts were available; the publication was in English; the geographical location of the study was clearly stated; the sample size ( > 35) (This number was chosen to guarantee adequate statistical power and reliability of studies involving antimicrobial resistance profiles, hence the cutoff of > 35 isolates was chosen); studies were not conducted in humans; and the prevalence of ESKAPE pathogens is clearly stated and research conducted after 2014.

Exclusion criteria

Reviews, meta-analyses, and case reports were omitted. Studies that did not match the given conditions were excluded. No attempts were made to get further information or unpublished studies from the authors of the original articles.

Selection of studies and data extraction

This study’s published articles were retrieved, screened, and reviewed by two authors (NGK and TR) who worked independently at each of the four stages: (i) title identification; (ii) title and abstract screening; (iii) full-text retrieval and eligibility screening; and (iv) full-text review and data extraction. Disagreements amongst the researchers were handled through conversations that resulted in consensus. The retrieved studies were managed using Microsoft Excel® (Microsoft Corporation, Redmond, WA, USA) and EndNote version 20 (1500 Spring Garden Street, Fourth Floor, Philadelphia, PA 19,130, USA). Duplicate records were deleted after compiling search titles and abstracts from three databases. After screening the titles and abstracts, the complete texts of qualifying studies were assessed using the same criteria as described above. Thereafter, data was extracted from eligible studies.

Outcome measurements

The primary findings of this study were the prevalence of ABR profiles of the ESKAPE pathogens isolated from humans in Africa. The antibiotic resistance profiles from 2014 to 2024, their antibiotic resistance genes, multidrug resistance (MDR) were studied.

Quality assessment of the studies

Two writers (NGK and TR) independently assessed the quality of the studies using the Joanna Briggs Institute’s (JBI) Critical Appraisal Tool for Prevalence Studies [16]. The studies were categorized as poor quality (less than 50%), moderate quality (50–74%), and high quality (≥75%) [17, 18]. Inconsistencies in the grading by the two reviewers were examined and rectified.

Data synthesis and data analysis

Comprehensive Meta-Analysis Software ver.4.0 program (https://www.meta-analysis.com/) was used to conduct the meta-analysis of the antibiotic resistance of ESKAPE pathogens on humans. The pooled prevalence estimate (PPE) of each isolate was calculated, and subgroup analysis was performed according to continent, country, year of publication, settings, antibiotic-resistant genes, phenotypic ABR, identification method, and samples collected. Random-effects models were used to generate forest plots displaying study-specific impact sizes with a 95% confidence interval (CI) for the PPE. The I² statistic and Chi-squared test were used to assess heterogeneity among studies. A score close to 0% implies no heterogeneity, while values near 25, 50, and 75% correspond to low, moderate, and high heterogeneity, respectively. The p-values represent the heterogeneities between studies found using a Chi-squared test of the null hypothesis that there is no heterogeneity.

Publication bias

To assess publication bias, funnel plots were used to test for symmetry, followed by the Beg and Mazumdar rank correlation test and Egger’s regression test [19, 20].

Countries from which published studies were conducted

A total of 31 studies, originating from Ethiopia [21–35] with fifteen articles, three articles from Cameroon [36–38], four articles from each of Nigeria [39–42], and Tanzania [43–46] respectively, two articles from Egypt [47, 48] and one article each from Kenya, Mali and Mozambique were included in this systematic review [49–51].

Results

Search results

A total of 268 articles were retrieved from the database search. After removing the duplicates (n = 10) and excluding studies for other reasons (Published in other languages, not conducted in Africa, titles not related to ESKAPE pathogens and some were conducted before 2014) (n = 106), 152 studies were screened based on title and abstract. Subsequently, from the full-text evaluation of the 136 studies, 10 were excluded for various reasons, including study design (only cross-sectional was selected), unclear information on the outcome of interest and a sample size of less than 35. Finally, only 31 studies were included for data extraction and analysis (Supplementary Table S2). A total of 31 studies were conducted in different countries, such as Ethiopia (n = 15), Nigeria (n = 4), Tanzania (n = 4), Cameroon (n = 3), Egypt (n = 2) and Mixed (n = 3) as shown in Fig. 2. The quality assessment score from the Joanna Briggs Institute (JBI) critical appraisal ranges from 1 to 9. The lowest score was found only on 5 studies (Supplementary Table S3).

Fig. 2.

A map showing the number of studies included in the study per country that investigated ESKAPE pathogens in humans from Africa [https://www.mapchart.net/world.html (accessed on 26 April 2024)]. A comprehensive summary of studies published between 2014 and 2024 was conducted

Characteristics of eligible studies

For the purpose of this study, the sample size per study ranged from 254 to 5982, and all studies were published between 01, January 2014 to early 2024. Furthermore, our species subgroup analysis showed that S. aureus was the most studied ESKAPE pathogen with 17 studies, 5982 sample size and 1445 positive isolate, followed by K. pneumoniae with 9 studies, 3332 sample sizes, 523 positive isolates and E. faecium with 3 studies, 982 samples and 109 isolates. Whilst, Enterobacter spp., P. aeruginosa, and A. baumanii were the least studied pathogens, as shown in Fig. 3. Our subgroup analysis further revealed that more studies were conducted extensively between 2014 and 2020 with 17 studies while between 2021 and 2024, only 14 studies were conducted. Majority of the studies employed the culturing method (n = 19) for identification of ESKAPE pathogens, followed by PCR (n = 8), two studies used whole genome sequencing (WGS) and VITEK-MS, respectively, and MALDI-TOF MS and PCR (n = 1). Finally, the disk diffusion method was the preliminary method used for antibiotic resistance testing in all the studies included in this review.

Fig. 3.

Proportion of ESKAPE pathogens isolates included in this study

Pooled prevalence estimates

An overall pooled prevalence estimate (PPE) of ESKAPE pathogens in Africa was observed in S. aureus with PPE of 23.1% (95% CI: 16.2–31.9), a significant difference between study heterogeneity was observed (Q = 528.759, p < 0.0001) from the 17 eligible studies with 1445 isolates. Followed by K. pneumoniae with PPE of 20.9% (95% CI: 0.113–0.353, Q = 303.680, p < 0.0001), from the nine studies, 3331 samples, with 523 isolates. Then, E. faecium with a PPE of 9.8% (95% CI: 0.013–0.475, Q = 148.769, p < 0.001), determined from three studies with 109 isolates. Lastly, Enterobacter spp. with PPE of 5.3% (95% CI: 0.024–0.113, Q = 66.606, p < 0.0001), from six studies, with 93 isolates. While A. baumannii, P. aeruginosa and E. faecium were not included in the meta-analysis due to the low number of studies conducted. The heterogeneity estimates of ESKAPE pathogens are shown in Table 1.

Table 1.

Subgroup analysis of ESKAPE pathogens in humans

Risk factors	Number of studies	Pooled estimates			Measure of heterogeneity			Publication bias
		Sample size	Isolates	I2 (95%CI)	Q Value	I2	Q	P-value
Overall
E. faecium	3	982	109	9.8% (1.3–47.5)	148.769	98.656	< 0.001	0.058
S. aureus	17	5982	1445	23.1% (16.2–31.9)	528.759	97.163	< 0.001	0.500
K. pneumoniae	9	3332	523	20.9% (11.3–35.3)	303.680	97.366	< 0.001	0.265
A. baumannii	1	254	16	0.0	0.0	0.0	0.0	0.0
P. aeruginosa	2	254	193	0.0	0.0	0.0	0.0	0.0
Enterobacter spp.	6	2435	93	5.3% (2.4–11.3)	66.606	92.493	< 0.001	0.286
Study year
2014–2020	17	7672	1558	24.6% (17.7–33.1)	549.886	97.090	< 0.001	0.080
2021–2024	14	4839	2021	50.4% (34.6–66.2)	703.601	98.152	< 0.001	0.478
Methods
PCR	8	2899	1130	54.4% (30.7–76.2)	580.031	98.793	< 0.001	0.355
Culturing	19	7381	2022	29.9% (21.2–40.3)	650.488	97.233	< 0.001	0.231
WGS	2	1991	337	0.0	0.0	0.0	0.0	0.0
VITEK- MS	2	1342	404	0.0	0.0	0.0	0.0	0.0
MALDI-TOF MS, & PCR	1	200	67	0.0	0.0	0.0	0.0	0.0
Countries
Ethiopia	15	6707	1783	24.9% (17.5–34.1)	523.731	97.327	< 0.001	0.402
Nigeria	4	685	614	98.3% (48.8–99.9)	65.869	95.445	< 0.001	0.500
Tanzania	4	2162	309	16.1% (8.5–28.3)	91.911	96.736	< 0.001	0.500
Cameroon	3	713	359	40.1% (14.3–72.9)	114.168	98.248	< 0.001	0.500
Egypt	2	1753	345	0.0	0.0	0.0	0.0	0.0
Antibiotic resistance methods
DDA	31	12511	3579	34.8% (26.8–43.8)	1456.575	97.940	< 0.001	0.084

DDA= disk diffusion assay, PCR = polymerase chain reaction, WGS = whole genome sequencing, I² = I-squared, Q = Cochran‘s Q

DDA = disk diffusion assay, PCR = polymerase chain reaction, WGS = whole genome sequencing, I² = I-squared, Q = Cochran’s Q.

Prevalence by diagnostic methods

Five diagnostic techniques were used to understand the antibiotic-resistant profiles of ESKAPE pathogens in Africa (Table 1). Most studies (n = 19) used traditional microbiological culturing, however, their PPE of 29.9% (95% CI: 21.2–40.3, Q = 580.031, p < 0.0001) was not greater than that of PCR techniques, even though there were minimal studies at 54.4% (95% CI: 30.7–76.2, Q = 580.031, p < 0.0001).

Prevalence by country

The highest pooled prevalence estimate of antibiotic-resistant pathogens was found in Nigeria with 98.3% (95% CI: 48.8–99.9, Q = 65.869, p < 0.0001), followed by a number of countries mixed, such as Mozambique, Kenya, and Mali with 41.2% (95% CI: 19.1–67.5, Q = 52.191, p < 0.0001), Cameroon with 40.1% (95% CI: 14.3–72.9, Q = 114.168, p < 0.0001), while the least number of countries where antibiotic resistant profiles from ESKAPE pathogens were found included Ethiopia with 24.9% (95% CI: 17.5–34.1, Q = 523.731, p < 0.0001) and Tanzania with 16.1% (95% CI: 8.5–28.3, Q = 91.911, p < 0.0001), respectively.

Prevalence by years of study

A total of 14 studies at a PPE of 50.4% (95% CI: 34.6–66.2) were conducted between the years 2021–2024 (Fig. 4A), while between the years 2014 and 2020, the PPE was found to be 24.6% (95% CI: 17.7–33.1) with 17 studies (Fig. 4B).

Fig. 4.

Forest plot of studies included in a random-effects meta-analysis for prevalence of abr in ESKAPE pathogens, (A) studies from 2021 to 2024, (B) studies from 2014 to 2020. The diamond at the base indicates the pooled estimates from the overall studies

Meta-analysis for the prevalence of phenotypic antibiotic resistance on ESKAPE pathogens in Africa

The PPE of antibiotic resistance among ESKAPE pathogens is shown in Table 2. A total of 444 isolates of Enterobacter spp. were screened for ABR and had antibiotic resistance PPE of 95.3% (95% CI: 79.8–99.2); 77.5% (95% CI: 39.0–94.9); 45.1% (95%CI: 26.4–67.4) and 36.7% (95% CI: 14.7–66.0) against amoxicillin-clavulanate, gentamicin, chloramphenicol and ciprofloxacin respectively. Our analysis showed that E. faecium was more resistant to tetracycline with PPE of 47.0% (95% CI: 2.3–97.0)], followed by erythromycin with 24.9% (95%CI: 3.1–77.6) and vancomycin 19.0% (95% CI: 4.9–51.7).

Table 2.

Pooled prevalence estimates and 95% ci of antibiotic resistance of ESKAPE pathogens isolates from this study

Antibiotic agents	Number of studies	Number of isolates	% Prevalence	I2 (95%CI)	P-value
Enterobacter spp.
Amoxicillin-clavulanate	3	100	95.3	(79.8–99.2)	0.300
Chloramphenicol	4	139	45.1	(26.4–67.4)	0.500
Ciprofloxacin	4	120	36.7	(14.7–66.0)	0.248
Gentamicin	3	85	77.5	(39.0–94.9)	0.058
E. faecium
Erythromycin	3	21	24.9	(3.1–77.6)	0.300
Tetracycline	3	29	47.0	(2.3–97.0)	0.300
Vancomycin	3	15	19.0	(4.9–51.7)	0.058
K. pneumoniae
Amoxicillin-clavulanate	6	201	28.7	(10.5–58.0)	0.425
Cefepime	5	134	26.3	(8.0–59.2)	0.312
Cefotaxime	4	125	22.4	(3.7–68.1)	0.087
Cefoxitin	4	22	13.9	(3.7–40.7)	0.248
Ceftazidime	5	49	14.6	(4.6–37.7)	0.163
Ceftriaxone	4	47	8.6	(1.9–31.4)	0.500
Chloramphenicol	5	194	32.0	(13.8–58.0)	0.312
Ciprofloxacin	8	257	17.9	(6.7–39.7)	0.228
Gentamicin	8	236	30.3	(12.1–57.8)	0.228
Tetracycline	5	101	16.9	(8.6–30.4)	0.025*
Trimethoprim-sulfamethoxazole	4	142	40.7	(12.6–76.6)	0.248
S. aureus
Amikacin	6	79	12.9	(5.9–26.2)	0.246
Amoxicillin	3	112	74.5	(47.0–90.6)	0.058
Amoxicillin-clavulanate	5	112	43.0	(15.7–75.4)	0.312
Ampicillin	7	345	57.3	(27.0–83.0)	0.326
Azithromycin	3	70	13.8	(5.9–27.1)	0.058
Cefoxitin	7	268	24.0	(8.7–51.1)	0.226
Ceftazidime	3	244	94.5	(82.0–98.5)	0.300
Ceftriaxone	7	273	32.9	(17.7–52.7)	0.440
Cefuroxime Axetil	3	187	53.0	(22.5–81.4)	0.300
Chloramphenicol	6	110	19.5	(13.8–26.9)	0.286
Ciprofloxacin	4	110	22.1	(11.4–38.5)	0.500
Clindamycin	6	115	18.0	(11.4–27.2)	0.425
Cloxacillin	3	251	90.6	(78.3–96.2)	0.058
Doxycycline	5	143	17.5	(7.2–36.7)	0.025*
Erythromycin	13	466	38.3	(28.9–48.7)	0.403
Gentamicin	9	286	26.3	(14.5–42.9)	0.417
Kanamycin	3	76	38.1	(16.6–65.4)	0.300
Ofloxacin	4	128	26.9	(11.5–51.1)	0.248
Oxacillin	3	16	32.1	(5.3–79.8)	0.058
Penicillin	8	599	91.1	(84.3–95.2)	0.161
Tetracycline	9	273	33.8	(25.3–43.5)	0.202
Vancomycin	8	72	15.7	(5.9–35.5)	0.068
MDR	13	1532	64.1	(51.3–75.1)	0.043*

MDR = multidrug resistance, *Statistically significant (p value < 0.05)

Moreover, the PPE of K. pneumoniae resistance to antibiotics was 40.7% (95% CI: 12.6–76.6) against trimethoprim-sulfamethoxazole, followed by chloramphenicol at 32.0% (95% CI: 13.8–58.0), and gentamicin at 30.3% (95% CI: 12.1–57.8), while this bacterium was least resistant to tetracycline, ceftazidime and ceftriaxone at 16.9% (95% CI: 8.6–30.4), 14% (95%CI: 4.6–37.7), and 8.6% (95% CI: 1.9–31.4), respectively. The S. aureus isolates were mostly resistant to ceftriaxone followed by penicillin, cloxacillin and amoxicillin with PPE of 94.5% (95% CI 82.0–98.5), 91.1 (95%CI 84.3–95.2), 90.6% (95%CI: 78.3–96.2) and 74.5% (95%CI: 47.0–90.6), respectively. On the other hand, S. aureus isolates were less resistant to doxycycline [17.5% (95%CI: 7.2–36.7)], vancomycin [15.7% (95% CI: 5.9–35.5)], azithromycin [13.8% (95% CI: 5.9–27.1)], and amikacin [12.9% (95% CI: 5.9–26.2)], respectively. A total of thirteen (n = 13) studies classified S. aureus isolates as multidrug resistant (MDR), which is defined as resistance to three or more drugs with a PPE of 64.1% (95% CI: 51.3–75.1) (Fig. 5).

Fig. 5.

Forest plot showing mdr prevalence in ESKAPE pathogens in Africa between 2014 and 2024. Random effects model: tau = 0.888; tau² = 0.789; Q = 191.848; p = 0.0001. The diamond at the base indicates the pooled estimates from the overall studies

Meta-analysis for the prevalence of genotypic antibiotic resistance genes on ESKAPE pathogens in Africa

Based on the findings presented in Table 3, our meta-analysis also revealed that the majority of research studies in Africa were conducted on the staphylococcal mecA gene, which codes for methicillin resistance, with 11 studies accounting for PPE of 31.5% (95% CI 17.0–50.8). Five studies detected bla_CTX-M gene which encodes for extended-spectrum β-lactamases with a PPE of 37.6% (95% CI: 9.1–78.4), whilst only 3 studies detected bla_TEM gene with a PPE of 13.0% (95%CI: 1.7–55.8).

Table 3.

Pooled prevalence estimates and 95% ci of antibiotic resistance genes of ESKAPE isolates

Antibiotic agents	Number of studies	Number of isolates	% Prevalence	I2 (95%CI)	P-value
blaCTX-M	5	182	37.6	(9.1–78.4)	0.163
blaTEM	3	131	13.0	(1.7–55.8)	0.300
mecA	11	308	31.5	(17.0–50.8)	0.121

Several of the studies in this review have reported the presence of the following genes linked to antibiotic resistance: bla_SHV [36, 42], bla_CMY, bla_DHA, bla_FOX and bla_MOX [49], mecC [50] bla_NDM-1 and bla_OXA-48 [51, 52], bla_CTX-M, bla_SHV, bla_CTX-M and bla_SHV [42], bla_SPM and bla_IMP [48]. Due to the limited number of studies, they were not included in the meta-analysis.

Publication bias

The Begg and Mazumdar rank correlation test demonstrated no significant publishing bias for practically all parameters except for two antibiotics, tetracycline (p = 0.025) doxycycline (p = 0.025), and MDR (p = 0.043) where both asymmetry of the funnel plots and p-values of indicated considerable bias as shown in Supplementary file S1-3, respectively.

Discussion

One of the most urgent issues facing global health is antibiotic resistance (ABR), which jeopardizes the effectiveness of currently available medicines and undermines decades of advancements in the treatment of infectious diseases [13, 53]. ABR might significantly jeopardize attempts to lower the mortality and morbidity linked to bacterial infections if it is not tackled immediately. The provision of regular, research-based pathogen susceptibility data, which guides focused treatments and policy choices, is essential to addressing this epidemic. The antibiotic susceptibility of ESKAPE pathogens—Enterococcus faecium, Staphylococcus aureus, Klebsiella pneumoniae, Acinetobacter baumannii, Pseudomonas aeruginosa, and Enterobacter spp.—isolated from human samples in Africa is the main focus of this systematic review, which gathers data from studies carried out between 2014 and 2024.

S. aureus had a pooled prevalence estimate (PPE) of 23.1% in Africa among the 1445 ESKAPE isolates from 31 studies, which is close to the prevalence among African bacteremia patients reported by Haindongo et al. [54] between 2008 and 2019. The current analysis’s methicillin-resistant S. aureus (MRSA) PPE was 24.0%, which is much less than the 48.4% PPE for hospital-acquired MRSA infections that was discovered in Germany [55]. This fluctuation is a reflection of larger global trends. MRSA prevalence in the Asia-Pacific region varied from 0 to 98.4% between 2000 and 2016 [56], while rates in Western Europe ranged from 1% to over 20% between 2000 and 2010 [57]. In the meantime, MRSA resistance decreased from 19% in 2015 to 15.5% in 2019, according to the European Centre for Disease Prevention and Control [58]. Interestingly, some of the studies in our analysis did not distinguish between ambient and clinical isolates, which made comparisons more difficult.

Nine studies yielded 523 isolates from 3331 samples, resulting in a PPE of 20.9% for Klebsiella pneumoniae. In comparison, Okafor and Nwodo [59] reported an 86% prevalence in South Africa, while Mapipa et al. [60] found a 78.8% rate in hospital wastewater. Conversely, research from South Africa and Ireland found lower prevalence rates of 29 and 14%, respectively [61, 62]. As reported by Mbelle et al. [63] and Kaapu et al. [64] in South African clinical settings, the current investigation found that K. pneumoniae had an alarmingly high resistance to trimethoprim-sulfamethoxazole. Chloramphenicol resistance was also found, even though its use is limited since it is linked to aplastic anemia [65]. The reported 32% resistance is consistent with Bangladesh’s Rabbani et al. [66]. Given their significance in clinical therapy, the fact that over half of the K. pneumoniae isolates in this research were resistant to cephalosporins such as ceftazidime (14%) and ceftriaxone (8.6%) is alarming. There is a significant therapeutic conundrum due to the rising prevalence of multidrug-resistant (MDR) K. pneumoniae strains globally [67]. The constitutive production of chromosomal class A beta-lactamase enzymes may be one factor contributing to the high resistance [68]. Though careful and sensible administration is still essential, the comparatively low resistance rates for cefoxitin and colistin ( < 30%) indicate that some therapeutic value may still be there.

Three studies produced 109 isolates of E. fecium and a PPE of 9.8%. At 47.0%, tetracycline resistance was the most common, followed by vancomycin (19.0%) and erythromycin (24.9%). Georges et al. [69] discovered that Enterococcus spp. were rare pathogens in Kenya, accounting for fewer than 2% of clinical isolates, which is comparable to the 9.8% prevalence reported in our review. This is consistent with data from Ethiopia that indicates a prevalence of 2.7% as opposed to 13.6% in Zambia [70]. More resistance to vancomycin, erythromycin, and tetracycline was shown by E. faecium than by E. faecalis. On the other hand, Mwikuma et al. [70] found that all isolates were resistant to tetracycline. Nevertheless, studies conducted in the United States that show resistance to tetracycline, penicillin, and ciprofloxacin and erythromycin, nitrofurantoin, and tetracycline also corroborate the findings [71]. Global relevance is suggested by the significant tetracycline resistance that is consistent across locations [72].

Six studies reported Enterobacter species, and 93 isolates had a PPE of 5.3%. High PPEs of 95.3% for amoxicillin-clavulanate, 77.5% for gentamicin, 45.1% for chloramphenicol, and 36.7% for ciprofloxacin were found in 444 isolates that underwent antibiotic susceptibility testing. The discovered Enterobacter spp. are known nosocomial pathogens, mainly E. aerogenes and E. cloacae [73]. These species can acquire mobile genetic elements that confer significant fitness and survival advantages, and they act as reservoirs for resistance genes [74]. In keeping with their known inherent resistance to ampicillin, amoxicillin-clavulanic acid, and cefoxitin, all of the Enterobacter species in this investigation showed resistance to β-lactams, cephems, tetracyclines, and aminoglycosides [75].

Only 16 isolates of Acinetobacter baumannii were found between 2014 and 2024, making it the least studied ESKAPE organism in the current study. In hot and humid places like tropical Asia and Australia, where it has been connected to community-acquired pneumonia, it is frequently found [76]. In stark contrast to the low number of investigations conducted in Africa, MDR A. baumannii rates surpassing 90% have been reported in Greece and Turkey [77]. A major threat to public health is the bacterium’s quick development of resistance, particularly to β-lactams and carbapenems [78]. A. baumannii may exacerbate the global resistance dilemma in the absence of improved pharmaceutical therapies and epidemiological surveillance [79].

Multidrug resistance to at least three antibiotic classes was found in 1532 isolates across 13 studies, accounting for 64.1% PPE. In gram-negative isolates such as A. baumannii, P.aeruginosa, and K. pneumoniae, MDR was especially noticeable. This emphasizes how important it is to employ antimicrobial susceptibility testing to direct clinical actions, especially in view of hospitals’ overuse of antibiotics and the rising incidence of resistant strains. Notably, P. aeruginosa from burn patients in hospitals has demonstrated a rise in MDR characteristics. Given the significance of imipenem in treating MDR infections, one study found that 79.2% of isolates were resistant to multiple antibiotics [80]. Ceftazidime (57.5%), ciprofloxacin (65%), gentamycin (67.5%), piperacillin (87.5%), amikacin (90%), and imipenem (97.5%) were among the antibiotics with the highest resistance rates, according to a 2013 Iranian study [80]. In Greece, a 2018 study by Karakonstantis et al. [81] discovered that 84% of A. baumannii were MDR, and 48% were extensively drug-resistant (XDR). An Austrian study that demonstrated 80.7% carbapenem resistance [82] further confirmed the concerning trend that 50% to 80% of A. baumannii isolates exhibited imipenem resistance, as described by Karakonstantis et al. [80].

Resistance genes were additionally investigated in our meta-analysis. The mecA gene was found in staphylococci with a PPE of 31.5% in eleven investigations. While Khasapane et al. [83] in South Africa reported a detection rate of 16%, which is in line with our findings, Samutela et al. [84] obtained a 100% detection rate in 32 isolates from Zambia, which is significantly higher than our findings. With a PPE of 13.0%, the bla_TEM gene was only found in three studies. This stands in sharp contrast to research conducted in Senegal by Ngom et al. [85], which found a prevalence of 78.1%. However, our results are consistent with those of Mbyemeire et al. [86], who recently reported 3.8% in Uganda. Because these genes are commonly found on mobile plasmids, horizontal gene transfer between bacteria is made easier [87]. Due to its extensive distribution and environmental sources, the bla_CTX-M enzyme group has become the most prevalent extended-spectrum beta-lactamase (ESBL) [88].

The antibiotic resistance of ESKAPE infections isolated from humans in Africa has been documented by this meta-analysis. This review provides an objective assessment of the prevalence of ABR throughout the continent by incorporating peer-reviewed papers. Geographical differences were noteworthy; in ESKAPE resistance investigations, many African nations were either completely absent or underrepresented. Studies published between 2014 and 2020 were more numerous (17 articles) than those published between 2021 and 2024 (14 articles); however, the PPE for the later period was substantially higher at 50.4% as opposed to 24.6% for the former. These results demonstrate the increasing prevalence of ABR throughout Africa and the pressing need for cross-border cooperation, strategic antimicrobial management, and regular surveillance to lessen the threat presented by resistant organisms.

Limitations

This systematic review and meta-analysis have several limitations, such as the restriction of the literature search to English-language publications, which may have resulted in the omission of relevant studies published in other languages, followed by limited or absent data from certain countries which may have affected the representativeness of the findings at the continental level. Moreover, there was an unequal distribution of research output across countries, with some contributing substantially more studies than others. Lastly, heterogeneity in the focus of included studies was noted, with varying emphasis placed on individual ESKAPE pathogens.

Conclusion

Overall, these findings highlight a concerning burden of antibiotic resistance among ESKAPE pathogens across multiple African regions, with notably high resistance rates to commonly used antibiotics. The widespread prevalence of multidrug resistance, particularly among Enterobacter spp. and S. aureus, underscores the urgent need for coordinated surveillance and stewardship interventions. Moreover, the detection of key resistance genes such as bla_CTX-M, mecA, and bla_TEM points to the ongoing dissemination of critical resistance mechanisms, further complicating treatment options and public health control efforts on the continent.

Electronic supplementary material

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Abbreviations

ABR

Antibiotic resistance

CI

Confidence interval

ESBL

Extended spectrum beta-lactamase producing

ESKAPE

Enterococcus faecium, Staphylococcus aureus, Klebsiella pneumoniae, Acinetobacter baumannii, Pseudomonas aeruginosa, and Enterobacter

JBI

Joanna Briggs Institute’s

MDR

Multidrug resistant

MRSA

Methicillin-resistant Staphylococcus aureus

PPE

Pooled prevalence estimate

PRISMA

Preferred Reporting Items for Systematic Reviews and Meta-analyses

PROSPERO

International Prospective Register of Systematic Reviews

SDGs

Sustainable development goals

WHO

World Health Organisation

Author contributions

NGK: Writing - original Draft, Methodology, Screening and Review of included studies, Data curation. TR: - Data Screening, Supervision. and Review of included studies, Data curation and analysis, Visualisation, Review and Editing. OT: Writing – Review & Editing. SJN: Writing – Review & Editing, LK: Writing – Review & Editing.

Funding

This study was supported financially by the National Research Foundation (NRF) grant number: NFSG23042496860.

Data availability

All relevant data is contained within the article.

Declarations

Ethics approval and consent

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.