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Frontiers in Microbiology ·

Volume 17 - 2026 | https://doi.org/10.3389/fmicb.2026.1908867

Diverse Staphylococcus aureus lineages in a tertiary hospital in North Central Nigeria: emergence of CC1-ST772-MRSA, CC8-ST789-MRSA, and ST152-MRSA

  • Rasaki Adewole Raheem1,2*corresponding author
  • Charles Nwabuisi3
  • Abayomi Fadeyi3
  • Bashirat Ayobola Olanipekun2
  • Ademola Ibraheem Hamzat2
  • Tomiwa Olumide Adesoji4
  • Taofiq Adewale Sulayman4
  • Alexander Mellmann5
  • Frieder Schaumburg1*corresponding author
  • Adebayo Osagie Shittu1,4
  1. 1Institute of Medical Microbiology, University of Münster, Münster, Germany
  2. 2Department of Medical Microbiology and Parasitology, University of Ilorin Teaching Hospital, Ilorin, Nigeria
  3. 3Department of Medical Microbiology and Parasitology, University of Ilorin, Ilorin, Nigeria
  4. 4Department of Microbiology, Obafemi Awolowo University, Ile-Ife, Nigeria
  5. 5Institute for Hygiene, University of Münster, Münster, Germany
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Abstract

Staphylococcus aureus is a human pathogen associated with both hospital- and community-acquired infections. Data on its molecular epidemiology in North Central Nigeria are currently unavailable. This study investigated the antibiotic resistance, virulence genes, and the population structure of S. aureus in a tertiary hospital in North Central Nigeria. S. aureus strains from various clinical specimens collected between July 2017 and July 2021 were characterized based on antibiotic susceptibility testing and PCR detection of nuc , mecA , PVL ( lukS -PV/ lukF -PV), and immune evasion ( scn , sak , chp ) genes. Genotyping of the strains was performed by spa typing and whole-genome sequencing (WGS) of representative strains. Of the 169 S. aureus strains, 52% ( n = 88) were recovered from wound infections. The resistance rates were highest for penicillin ( n = 162; 96%), followed by trimethoprim-sulfamethoxazole ( n = 128; 76%), tetracycline ( n = 66; 39%), gentamicin ( n = 54; 32%), ciprofloxacin ( n = 53; 31%), erythromycin ( n = 31; 18%), and clindamycin ( n = 3; 2%). Overall, 90 (53%) were mecA -positive (MRSA), and 81 strains (48%) were multidrug-resistant (MDR). Genotyping revealed a diverse S. aureus population, comprising 37 spa types and 19 sequence types (STs) in nine clonal complexes (CC1, CC5, CC8, CC15, CC22, CC30, CC45, CC88, CC121) and two singletons (ST152 and ST7572). The predominant MRSA lineages comprised CC1-ST772-MRSA-V-t657, CC8-ST789-MRSA-V-t091, and ST152-MRSA-Vc-t4690, while the common methicillin-susceptible S. aureus (MSSA) lineages were ST152-MSSA-t355, CC15-ST15-MSSA-t084, and CC5-ST5-MSSA-t311. The dfrG gene was detected across lineages, and 65% of all strains (MSSA: 68%; MRSA: 62%) were PVL-positive. Phylogenetic analysis revealed strain diversity, suggesting the dissemination of different lineages across various wards within the hospital. The S. aureus population at a tertiary hospital in North-Central Nigeria is highly diverse. The detection of PVL-positive ST152-MRSA-Vc and MDR CC1-ST722-MRSA-V is of significant public health concern. Genomic surveillance of S. aureus , combined with clinical data, is essential for effective infection prevention and control strategies.

Keywords

1 Introduction

Staphylococcus aureus is a major human pathogen responsible for various infections, ranging from mild skin and soft tissue infections (SSTIs) to severe illnesses, e.g., sepsis, pneumonia, osteomyelitis, and food poisoning (Tong et al., 2015). These infections occur in hospitals and communities, leading to significant health and economic burdens (Noskin et al., 2007). S. aureus acquires antibiotic resistance through chromosomal mutations or via mobile genetic elements (Mlynarczyk-Bonikowska et al., 2022) and its pathogenicity is further enhanced by numerous virulence factors (Cheung et al., 2021). S. aureus infections represent a global public health concern, with a high burden in sub-Saharan Africa (Naghavi et al., 2024). A major factor contributing to this burden is the high prevalence (>70%) of Panton-Valentine Leukocidin (PVL)-positive S. aureus, particularly methicillin-susceptible S. aureus (MSSA), in Africa (Schaumburg et al., 2014). In contrast, 25% of S. aureus strains in Europe are PVL-positive (Bouchiat et al., 2017). PVL-positive S. aureus strains are associated with severe SSTIs, necrotizing pneumonia, life-threatening infections in children, and prolonged hospital stays (Garbo et al., 2024; Da Qu et al., 2022).

Methicillin-resistant Staphylococcus aureus (MRSA) is a key antimicrobial-resistant pathogen identified by the World Health Organization as a major antimicrobial resistance threat, particularly in relation to the Sustainable Development Goals (SDGs) on health (SDG 3) (Gajdács et al., 2021). MRSA is characterized by resistance to β-lactam agents, except the fifth-generation cephalosporins (ceftaroline and ceftobiprole), and often possesses additional resistance genes to other classes of antibiotics (Lakhundi and Zhang, 2018). The prevalence of MRSA varies geographically, ranging from 24 to 50% across Africa (Falagas et al., 2013; Lakhundi and Zhang, 2018). In Nigeria, MRSA rates vary by region: 42% in the South–South (Obasuyi et al., 2020), <60% in the South-West (Adeyanju et al., 2022; Olalekan et al., 2025) and 31% in the North-East (Bilyaminu et al., 2025).

The population structure of S. aureus is influenced by recombination, genetic mutation, and horizontal gene transfer. These phenomena result in diverse clones with varying antibiotic resistance and virulence profiles, capable of adapting and spreading in hospital and community settings (Souza et al., 2024). Studies indicate that the S. aureus population varies between and within regions and can change over time (Chen et al., 2021; Wang et al., 2022). The predominant African MRSA lineages include clonal complexes (CC)1, CC5, CC8, CC30, and CC88 (Lawal et al., 2022). In Nigeria, the dominant S. aureus lineages include CC5-MRSA, CC8-MRSA, CC15-MSSA, CC88-MRSA, CC121-MSSA, and ST152-MSSA (Shittu et al., 2011; Obasuyi et al., 2020; Adeyanju et al., 2022; Lawal et al., 2022).

Despite several regional studies, data on the molecular epidemiology of S. aureus in North Central Nigeria remain scarce. Therefore, the objectives of this study were to investigate the antibiotic resistance and virulence gene determinants, as well as the molecular epidemiology of S. aureus strains at the University of Ilorin Teaching Hospital (UITH).

2 Materials and methods

This study was conducted at UITH, a 640-bed tertiary referral centre in North Central Nigeria, with an average of ~12,000 inpatients and 126,000 outpatients annually. The inclusion criterion was non-duplicate S. aureus strains from diverse clinical specimens submitted to the Medical Microbiology Laboratory between July 2017 and July 2021. S. aureus strains from samples without a clinical diagnosis or from colonized patients in surveillance investigations were excluded. Relevant socio-demographic and clinical data were retrieved from laboratory records.

2.1 Identification and antibiotic susceptibility testing of the Staphylococcus aureus strains

Strains were presumptively identified using standard microbiological methods, including Gram staining, catalase, coagulase, DNase, mannitol fermentation, and lysostaphin susceptibility tests (Mast Group, UK). S. aureus strains were confirmed by MALDI-TOF MS (Sirius One, Bruker Daltonics, Bremen, Germany). Antimicrobial susceptibility testing was performed using the VITEK 2 automated system (bioMérieux, France), and clinical breakpoints were interpreted according to EUCAST (v12) clinical guidelines. Multidrug resistance (MDR) was defined as resistance to ≥3 antibiotic classes (Magiorakos et al., 2012).

2.2 PCR detection of nuc, mecA, non-ribosomal peptide synthetase (NRPS), lukS-PV/lukF-PV, chp, sak, and scn genes

Genomic DNA was extracted using the QIAamp tissue kit (QIAGEN, GmbH, Hilden, Germany), with lysostaphin added during the lysis step. Species identification as S. aureus and the methicillin resistance phenotype, i.e., MRSA, were determined by PCR detection of nuc and mecA, respectively (Brakstad et al., 1992; Murakami et al., 1991). PCR detection of the non-ribosomal peptide synthetase (NRPS) gene was performed to identify members of the S. aureus complex (Zhang et al., 2016). All strains were screened for the PVL toxin (lukS-PV/lukF-PV) gene (Lina et al., 1999) and immune evasion cluster (scn, sak, chp) genes (Van Wamel et al., 2006).

2.3 Molecular typing of Staphylococcus aureus strains

Spa typing (Harmsen et al., 2003) was done as previously described (Mellmann et al., 2006), and data were analyzed using Ridom SeqSphere software (version 7, Ridom GmbH, Münster, Germany). Representative strains (one strain per spa type) were selected for whole-genome sequencing (WGS). After DNA isolation (NEB Monarch Genomic Purification Kit, New England Biolabs, Ipswich, MA, USA), WGS was performed on a PacBio® Sequel IIe system (Pacific Biosciences, Menlo Park, CA, USA) using the SMRTbell® Express Template Prep Kit 2.0 (Pacific Biosciences Inc.). The sequencing data were assembled de novo using the SMRT® Link software suite v10 with default parameters and annotated using Prokka (1.14.6) on the Galaxy platform (Seemann, 2014). Using default parameters, antimicrobial resistance and virulence genes, with sequence types (STs), were predicted in silico with SeqSphere+ (v9).

2.4 SCCmec typing and phylogenetic analysis

The staphylococcal cassette chromosome mec (SCCmec) types (and subtypes) of the strains were determined using the Centre for Genomic Epidemiology tools, SCCmecFinder 1.21. A pan-genome was constructed using Roary (v. 3.13.0) (Page et al., 2015) to identify core genes shared across all strains. Core gene alignment (present in 99% of strains) was generated using default parameters, including a minimum percentage identity of 95% for clustering homologous genes. Core gene sequences were also aligned using MAFFT (7.526) with the auto-selected strategy (Katoh and Standley, 2013). A maximum-likelihood phylogeny was inferred from the untrimmed alignment using IQ-Tree (v. 2.4.0) (Nguyen et al., 2014) under the general time-reversible substitution model with 1,000 ultrafast bootstrap replicates for branch and node support. The visualization and annotation of the phylogenetic tree were performed using iTOL (v6.7.4) (Letunic and Bork, 2021). All analyses were conducted on the public Galaxy server2. Genome sequences of the representative strains were deposited on the NCBI website under Bioproject accession number PRJNA1463733.

2.5 Data analysis

The Chi-Square test and Student’s t-test were used to compare antibiotic resistance rates and PVL prevalence between MRSA and MSSA. Strains with the category ‘susceptible, increased exposure’ were grouped as ‘susceptible’ when comparing resistance rates between groups. A p-value <0.05 was considered statistically significant.

3 Results

3.1 Distribution of Staphylococcus aureus associated with clinical infections

A total of 169 S. aureus strains were obtained from inpatients and outpatients (Table 1). The cohort comprised 87 male and 82 female patients, with mean ages of 24 ± 21.9 and 29.4 ± 20.9 years, respectively. Strains were predominantly recovered from wound infections (n = 88; 52%) and bloodstream infections (n = 32; 19%), followed by upper respiratory tract and urogenital infections (n = 13; 8% each), eye infections (n = 11; 7%), lower respiratory tract infections (n = 7; 4%), and septic arthritis (n = 5; 3%).

Table 1. Demographic and clinical characteristics of S. aureus strains from UITH, Nigeria.

CharacteristicsS. aureus (n = 169)
MRSA: n = 90 (%)MSSA: n = 79 (%)
Age stratification
≤ 1426 (29)37 (47)
15–2813 (14)12 (15)
29–4327 (30)12 (15)
44–5817 (19)10 (13)
> 587 (8)8 (10)
Sex
Male42 (47)45 (57)
Female48 (53)34 (43)
Location
In-patient62 (69)55 (70)
Out-patient28 (31)24 (30)
Ward/Clinic
Accident & Emergency11 (12)11 (14)
Ear, Nose, and Throat3 (3)6 (8)
Emergency pediatric7 (8)17 (22)
Female medical8 (9)3 (4)
Female surgical9 (10)2 (2)
General outpatient15 (17)11 (14)
Male Medical3 (3)4 (5)
Male surgical6 (7)3 (4)
Neonatal intensive care8 (9)11 (14)
National health insurance scheme1 (1)3 (4)
Obstetrics & gynecology8 (9)2 (2)
Orthopedics2 (2)0 (0)
Pediatric surgical5 (6)2 (2)
Surgical outpatient4 (4)3 (4)
Sickle cell0 (0)1 (1)
Clinical diagnosis
Blood stream infectionsa12 (13)20 (25)
Eye infectionsb5 (6)6 (8)
LRTIsc4 (4)3 (4)
URTIsd6 (7)7 (9)
Septic arthritis2 (2)3 (4)
Urogenital infectionse9 (10)4 (5)
Wound infectionsf52 (58)36 (45)
Specimen
Aspirate2 (2)3 (4)
Blood12 (13)20 (25)
Eye discharge5 (6)6 (8)
LRTI sampleg4 (4)3 (4)
URTI samplesh6 (7)7 (9)
Urogenital samplei9 (10)4 (5)
Wound samplej52 (58)36 (45)

Endocarditis, septicaemia, neonatal sepsis, meningitis.

Ophthalmia neonatorum, conjunctivitis.

Pleuritis, parapneumonic infection, community-acquired pneumonia, hospital-acquired pneumonia.

Upper respiratory tract infections (otitis media, rhinosinusitis, sinusitis, and pharyngotonsillitis).

Urethritis, puerperal sepsis, vaginitis, pelvic inflammatory disease, and urinary tract infections.

Abscess, catheter line infection, wound ulcer, burn infection, surgical site infection, mastitis, pyomyositis, osteomyelitis, diabetes mellitus foot syndrome, implant infections, skin and soft tissue infections (necrotizing fasciitis, cellulitis, folliculitis, abscess, paronychia).

Sputum, pleural fluid.

Ear discharge, nasal discharge, and pharngotonsillar swab. iUrine, urethral swab, high vaginal swab, endocervical swab.

Wound biopsy, pus, exudates, deep wound swab, wound discharge.

3.2 Antibiotic susceptibility of Staphylococcus aureus strains

All the strains were susceptible to daptomycin, fosfomycin, fusidic acid, linezolid, mupirocin, rifampicin, glycopeptides, and tigecycline. High resistance rates were recorded for penicillin (n = 162; 96%) and trimethoprim-sulfamethoxazole (n = 128; 76%, Table 2). Overall, 53% (n = 90) of strains were mecA-positive, including one phenotypically susceptible strain to cefoxitin. MRSA strains demonstrated significantly higher rates than MSSA strains for gentamicin (59% vs. 1%), fluoroquinolones (53% vs. 6%), and tetracycline (50% vs. 27%). Multidrug resistance was observed in 48% of strains (n = 81), predominantly among MRSA (74% vs. 18% in MSSA). The inducible clindamycin resistance rate was low (2%).

Table 2. Antibiotic susceptibility testing of S. aureus strains from clinical samples at UITH, Nigeria.

AntibioticsMRSA (n = 90)MSSA (n = 79)p-value
Resistance (%)Susceptible (%)Resistance (%)Susceptible (%)
Cefoxitin89 (99)1 (1)0 (0)79 (100)-
Penicillin90 (100)0 (0)72 (91)7 (9)0.001
Co-amoxiclav89 (99)1 (1)4 (5)75 (95)0.001
Gentamicin53 (59)37 (41)1 (1)78 (99)0.001
Levofloxacin48 (53)42 (47)5 (6)74 (94)0.001
Ciprofloxacin48 (53)42 (47)5 (6)74 (94)0.001
Moxifloxacin48 (53)42 (47)5 (6)74 (94)0.001
Azithromycin28 (31)62 (69)3 (4)76 (96)0.001
Clarithromycin28 (31)62 (69)3 (4)76 (96)0.001
Erythromycin28 (31)62 (69)3 (4)76 (96)0.001
Clindamycin3 (3)87 (97)0 (0)79 (100)-
Tetracycline45 (50)45 (50)21 (27)58 (73)0.001
Trimethoprim-Sulfamethoxazole74 (82)16 (18)54 (68)25 (32)0.026
Linezolid0 (0)90 (100)0 (0)79 (100)-
Daptomycin0 (0)90 (100)0 (0)79 (100)-
Teicoplanin0 (0)90 (100)0 (0)79 (100)-
Vancomycin0 (0)90 (100)0 (0)79 (100)-
Tigecycline0 (0)90 (100)0 (0)79 (100)-
Fosfomycin0 (0)90 (100)0 (0)79 (100)-
Fusidic acid0 (0)90 (100)0 (0)79 (100)-
Mupirocin0 (0)90 (100)0 (0)79 (100)-
Rifampicin0 (0)90 (100)0 (0)79 (100)-

Bold values represent statistically significant p-values for resistance between MRSA and MSSA to the corresponding antibiotics.

3.3 PCR detection of the immune evasion cluster and the bi-component (lukF-PV/lukS-PV) genes

The prevalence of immune evasion cluster genes (scn, sak, and chp) was 94, 66, and 25%, respectively. The PVL gene was present in 110 strains (65%), with MSSA and MRSA at 68 and 62%, respectively (Supplementary Table 1), with no statistically significant difference (p = 0.4).

3.4 Molecular typing of Staphylococcus aureus strains by spa typing

The spa typing identified 37 genotypes, including one new spa type (t20210). The most common were t355 (23%), t091, and t657 (11% each, Table 3). Among the MRSA strains, the dominant types were t657 (20%), t4690 (18%), and t091 (17%). In MSSA, t355 was most common (44%), followed by t084 (13%) and t311 (8%) (Table 3).

Table 3. Characterization of MRSA and MSSA strains from UITH, Nigeria, based on spa typing and MLST.

Clonal complex (n)Sequence types from WGS data (n)spa types (n)MRSAn (%)MSSAn (%)
CC1 (28)ST1 (7)t114 (1), t1931 (2), t1931 (1), t5557 (2), t20210* (1)6 (86)1 (14)
ST772 (21)t657 (18), t657 (1), t9180 (1), t13180 (1)20 (95)1 (5)
CC5 (9)ST5 (8)t311 (1), t311 (6), t450 (1)1 (14)7 (86)
ST6 (1)t304 (1)0 (0)1 (100)
CC8 (32)ST8 (12)t008 (4), t008 (1), t064 (3), t1476 (3), t11148 (1)11 (92)1 (8)
ST789 (20)t091 (15), t091 (4), t2616 (1)16 (80)4 (20)
CC15 (13)ST15 (11)t084 (10), t5126 (1)0 (0)11 (100)
ST3712 (2)t326 (2)0 (0)2 (100)
CC22 (1)ST22 (1)t2933 (1)1 (100)0 (0)
CC30 (5)ST30 (3)t13518 (3)0 (0)3 (100)
ST243 (2)t021 (2)0 (0)2 (100)
CC45 (2)ST508 (1)t1156 (1)0 (0)1 (100)
ST2498 (1)t861 (1)0 (0)1 (100)
CC88 (7)ST88 (7)t2393 (1), t1244 (2), t7558 (2), t13249 (2)7 (100)0 (0)
CC121 (13)ST121 (11)t314 (5), t314 (5), t1991 (1)6 (55)5 (45)
ST7570** (1)t159 (1)0 (0)1 (100)
ST7571** (1)t159 (1)0 (0)1 (100)
ST152 (58)t355 (34), t355 (4), t1172 (1), t1299 (1), t4687 (1),t4690 (16), t11375 (1)22 (38)36 (62)
ST7572** (1)t355 (1)0 (0)1 (100)

MRSA identified with spa types in bold; *, new spa type; **, new sequence types.

3.5 Identification of Staphylococcus aureus clonal lineages based on MLST

WGS was performed on randomly chosen strains representing the 37 spa types. These S. aureus strains comprised 23 MRSA and 14 MSSA. We identified 19 STs, including three new types: ST7570, ST7571, and ST7572 (Table 3). The most frequently occurring STs were ST152 (34%), ST772 (12%), ST789 (12%), ST8, ST15, and ST121 (7% each), and ST5 (5%). ST1, ST30, ST88, ST243 and ST3712 occurred at lower frequencies (≤4%), and ST6, ST22, ST508, ST2498, ST7570, ST7571, ST7572 were represented by a single strain (<1%, Table 3). The strains were grouped into nine CCs, with CC8 (n = 32), CC1 (n = 28), CC15, and CC121 (n = 13 each) being the most common. Others include CC5 (n = 9), CC88 (n = 7), CC30 (n = 5), CC45 (n = 2), CC22 (n = 1), and two singletons: ST152 (n = 58) and ST7572 (n = 1). Diverse S. aureus lineages (>4 CCs) were observed in some clinical presentations, particularly bloodstream, upper respiratory tract, urogenital, and wound infections. S. aureus strains assigned to CC1 and ST152 were identified in all categories of clinical presentations, whereas those grouped with CC8 were observed in all infection groups except eye infections (Table 4).

Table 4. Prevalence of S. aureus clonal lineages according to clinical diagnosis.

Clinical diagnosisCCSTFrequency (%)
Bloodstream infectiona (n = 32)CC1ST1 (3), ST772 (1)4 (13)
CC5ST5 (1)1 (3)
CC8ST8 (1), ST789 (4)5 (16)
CC15ST15 (3), ST3712 (1)4 (13)
CC30ST30 (2), ST243 (2)4 (13)
CC88ST88 (2)2 (6)
CC121ST121 (3)3 (9)
ST152 (9)9 (28)
Eye infectionb (n = 11)CC1ST1 (2), ST772 (1)3 (27)
CC121ST121 (2)2 (18)
ST152 (6)6 (55)
LRTIsc (n = 7)CC1ST772 (2)2 (29)
CC8ST8 (2)2 (29)
CC15ST15 (1)1 (14)
ST152 (2)2 (29)
URTIsd (n = 13)CC1ST1 (1)1 (8)
CC5ST5 (1), ST6 (1)2 (15)
CC8ST8 (1)1 (8)
CC15ST3712 (1)1 (8)
CC88ST88 (1)1 (8)
CC121ST121 (1)1 (8)
ST152 (5)ST7572 (1)5 (38)1 (8)
Septic arthritis (n = 5)CC1ST772 (1)1 (20)
CC8ST789 (1)1 (20)
CC121ST7571 (1)1 (20)
ST152 (2)2 (40)
Urogenital infectione (n = 13)CC1ST1 (1), ST772 (3)4 (31)
CC5ST5 (1)1 (8)
CC8ST789 (2)2 (15)
CC15ST15 (1)1 (8)
CC22ST22 (1)1 (8)
CC45ST45 (1)1 (8)
ST152 (3)3 (23)
Wound infectionf (n = 88)CC1ST772 (13)13 (15)
CC5ST5 (5)5 (6)
CC8ST8 (9), ST789 (13)22 (25)
CC15ST15 (6)6 (7)
CC30ST30 (1)1 (1)
CC45ST508 (1)1 (1)
CC88ST88 (4)4 (5)
CC121ST121 (5), ST7570 (1)6 (7)
ST152 (30)30 (34)

Sequence Types in which MRSA strains were identified are in bold format.

Endocarditis, septicaemia, neonatal sepsis, meningitis.

Ophthalmia neonatorum, conjunctivitis.

Pleuritis, parapneumonic infection, community-acquired pneumonia, hospital-acquired pneumonia.

Upper respiratory tract infections (otitis media, rhinosinusitis, sinusitis, and pharyngotonsillitis).

Urethritis, puerperal sepsis, vaginitis, pelvic inflammatory disease, and urinary tract infections.

Abscess, catheter line infection, wound ulcer, burn infection, surgical site infection, mastitis, pyomyositis, osteomyelitis, diabetes mellitus foot syndrome, implant infections, skin and soft tissue infections (necrotizing fasciitis, cellulitis, folliculitis, abscess, paronychia).

MRSA was predominant in CC1, CC8, and CC88, whereas MSSA were mainly associated with CC15, CC30, and CC45 (Table 3). Both MRSA and MSSA were mainly identified in CC121 and ST152. Of the 23 MRSA strains selected for WGS, the following SCCmec types were identified: Vc (48%), V (22%), IVa (26%), and XIII (4%). SCCmec elements were distributed across the CCs, notably IV/IVa in CC8, CC22, CC88, and CC121; V in CC1-ST772 and CC8-ST789; and Vc in CC1-ST1, CC8, CC88, and ST152. Moreover, one ST152 strain possessed the SCCmec XIII element (Table 5).

Table 5. Characterization of the S. aureus strains from UITH, Nigeria, based on clonal lineages, SCCmec typing, and detection of antibiotic resistance and virulence genes.

Strain IDCCSTSCCmecspaGENERYQUNTETSXTLEUEXFTSTENTHLBADH
SW3401811Vct114---tet(K)-lukD, lukS-PV/lukF-PV--seh-fnbA, cna, clfA, clfB
BC0511911Vct1931---tet(K)-lukD, lukS-PV/lukF-PV--seh-fnbA, cna, clfA
SW49511Vct557---tet(K)-lukD, lukS-PV/lukF-PV--seh-fnbA, cna, clfA, clfB
BC6152011Vct20210---tet(K)-lukD, lukS-PV/lukF-PV--seh-fnbA, cna, clfB
SW9751772Vt657aac(6′)-Ie/aph(2″)-Iamph(C)/msr(A)gyrA_S84L/parC_S80F-dfrGlukS-PV/lukF-PV--sea, sec-clfA
SW041211772Vt9180aac(6′)-Ie/aph(2″)-Iamph(C)/msr(A)gyrA_S84L/parC_S80F-dfrGlukS-PV/lukF-PV--sea, sec-clfA
SP375181772Vt1318aac(6′)-Ie/aph(2″)-Iamph(C)/msr(A)gyrA_S84L/parC_S80F-dfrGlukS-PV/lukF-PV--sea, sec-clfA
SW6922055-t311-----lukD, lukS-PV/lukF-PV-----
SW0452155-t450----dfrGlukD--sec-fnbB
SW11501756-t304---tet(M)-lukD--sea--
SW1411888Vct008aac(6′)-Ie/aph(2″)-Ia-gyrA_S84L/parC_S80Ftet(K)dfrGlukD--sebhlbfnbA
SP1121888Vct064--gyrA_S84L/parC_S80Ftet(K)dfrGlukD--sea, seb-fnbA
SWI502088IVt1476aac(6′)-Ie/aph(2″)-Iaerm(C)gyrA_S84L/parC_S80Ftet(K)dfrC/dfrGlukD-tst-1--fnbA
SW1002188IVat11148aac(6′)-Ie/aph(2″)-Ia-gyrA_S84L/parC_S80Ftet(K)dfrC/dfrGlukD-tst-1--fnbA
BC961198789Vt091aac(6′)-Ie/aph(2″)-Ia-gyrA_S84L/parC_S80F-dfrGlukD---hlbclfB
SW9348789Vt2616aac(6′)-Ie/aph(2″)-Ia-gyrA_S84L/parC_S80Ftet(K)dfrGlukD---hlbclfB
BC833181515-t084----dfrGlukD----clfA, clfB
SW101211515-t5126----dfrGlukDeta----
SW973153712-t326----dfrGlukDeta, etb---clfB
SW2862222IVat2933----dfrC--tst-1sea-fnbA, cna
SW503193030-t13518----dfrGlukS-PV/lukF-PV----cna
BC5051930243-t021-----lukS-PV/lukF-PV---hlbcna
SW29645508-t1156-------tst-1sec-cna
UR1844452498-t861-------tst-1seb, sec-clfB
BC089198888Vct2393---tet(K)-lukD, lukS-PV/lukF-PV--sec--
SW729208888IVat7558----dfrClukD----clfA
BC042198888Vct12444----dfrGlukD, lukS-PV/lukF-PV--sec--
SW178198888IVat13249----dfrClukD----clfA
SW10221121121IVat1991---tet(K)dfrGlukD, lukS-PV/lukF-PV--seb-cna
SW78320121121-t314-----lukD, lukS-PV/lukF-PV--seb-cna
SW533201217571-t159----dfrGlukD, lukS-PV/lukF-PV--seb-cna
SW08821-152XIIIt355aac(6′)-Ie/aph(2″)-Ia----lukD, lukS-PV/lukF-PV---hlb-
SW923-152-t1299----dfrGlukD, lukS-PV/lukF-PV---hlbfnbB, cna
SW14218-152-t4687----dfrGlukD, lukS-PV/lukF-PV---hlbfnbB, cna
BC62020-152Vct4690---tet(K)dfrGlukD, lukS-PV/lukF-PV---hlb-
SW857-152Vct1172---tet(K)dfrGlukD, lukS-PV/lukF-PV---hlbfnbB, cna
SW93917-152Vct11375---tet(K)dfrGlukD, lukS-PV/lukF-PV---hlb-

ST, Sequence Type; CC, Clonal Complex; SCCmec, Staphylococcal Cassette Chromosome mec; GEN, Gentamicin; ERY, Erythromycin, QUN, Quinolones (Ciprofloxacin; Levofloxacin; Moxifloxacin); TET, Tetracycline; SXT, Trimethoprim-Sulfamethoxazole; LEU, Leukocidin genes (lukD, leukocidin D; lukF/S-PV, Panton-Valentine leukocidin subunit F; lukS-PV, Panton-Valentine leukocidin subunit S); EXF, Exfoliative toxin genes (eta, exfoliative toxin A; etb, exfoliative toxin B); TST, Toxic shock syndrome toxin (tst-1); ENT, Enterotoxins (sea, enterotoxin A; seb, enterotoxin B; sec, enterotoxin C; seh, enterotoxin H); HLB, β-haemolysin; ADH, Adhesion genes (clfA, clumping factor A; clfB, clumping factor B; cna, collagen adhesin; fnbA, fibronectin-binding protein A; fnbB, fibronectin-binding protein B); antibiotic resistance genes, [variants of SCCmec, IVa, Vc, and XIII; resistance to aminoglycosides, aac(6′)-Ie/aph(2″)-Ia; a bi-functional aminoglycoside acetyltransferase and phosphotransferase;mph(C)/msr(A), macrolide phosphotransferase/efflux pump; erm(C), macrolide, lincosamide, and type B streptogramin ribosomal site modification; lnu(A), lincosamide nucleotidyltransferase; gyrA_S84L/parC_S80F, fluoroquinolone point-mutated DNA gyrase and topoisomerase IV; tet(38)/tet(K), tetracycline efflux pump; dfrC/drfG, dihydrofolate reductase enzyme].

3.6 Characterization of the Staphylococcus aureus clonal lineages based on some antibiotic resistance and virulence genes

Some STs possessed diverse AMR and virulence genes, and some genes were associated with specific STs (Table 5). Within CC1, SCCmec typing differentiated ST1 (SCCmecVc) from ST772 (SCCmecV). The ST772 strains possessed resistance genes for erythromycin (mph(C)/msr(A)), gentamicin (aac(6′)-Ie-aph(2″)-Ia), trimethoprim (dfrG), and fluoroquinolones (gyrA S84L, parC S80F), with the enterotoxins (sea, sec). These genes were absent in the ST1 lineage, which instead harbored tetK and some virulence genes (cna, fnbA, seh, lukD). CC8, comprising ST8 and ST789, harbored several antibiotic resistance genes and was lukD-positive; ST8 was fnbA-positive, whereas ST789 was clfB-positive. All CC30 strains were PVL- and cna-positive, while the CC45 strains were tst-positive. All the CC88 strains were MRSA. Moreover, CC88-MRSA-IVa strains harbored dfrC, clfA, and lukD, whereas CC88-MRSA-Vc strains were positive for PVL, lukD, and sec genes. All CC121 strains harbored PVL, lukD, seb, and cna, while ST152 strains were positive for PVL, lukD, and hlb (Table 5).

3.7 Genomic epidemiology of Staphylococcus aureus strains

Phylogenetic analysis of S. aureus revealed a genetically diverse population comprising various CCs and SCCmec elements (Figure 1). The ST152 lineage was the most heterogeneous, encompassing both MSSA (e.g., t1299, t4687) and MRSA (e.g., t355, t1172, t4690, t1375) associated with SCCmecVc and XIII. Three major MRSA lineages were identified. The first, CC8 (ST8-MRSA), included strains with different spa types (t008, t064, t1476, t11148) and SCCmec IV and Vc. The second, CC88 (ST88), comprised strains with spa types t12444, t2393, t7558, and t13249, with SCCmecIVa and Vc. CC1-ST1-MRSA-Vc strains formed a distinct cluster linked to spa types t114, t5557, t20210, and t1931. Other clusters included CC1-ST772-MRSA-V and CC8-ST789-MRSA-V. The distribution of various CCs across clinical wards indicates a diverse S. aureus population within the hospital. Specifically, PVL-positive MRSA strains assigned to CC1, CC88, and ST152-MRSA were identified in the NICU.

Maximum-likelihood phylogenetic tree among clinical *Staphylococcus aureus* strains recovered between 2017 and 2021. The tree was constructed from whole-genome sequence data and visualized using Interactive Tree of Life (iTOL). Strains are annotated with strain ID, year of isolation, hospital ward, clinical diagnosis, clonal complex (CC), sequence type (ST), *SCCmec* type, and *spa* type, NA: Not Applicable. A&E, Accident & Emergency; ENT, Ear, Nose, and Throat; EPU, Emergency Pediatric Unit; FSW, Female Surgical Ward; FMW, Female Medical Ward; GOPD, General Outpatient Department; MSW, Male Surgical Ward; NHIS, National Health Insurance Scheme; NICU, Neonatal Intensive Care Unit; O&G, Obstetrics & Gynecology; ORTHO, Orthopedic Ward; PSW, Pediatric Surgical Ward; PMW, Pediatric Medical Ward; SCC, Sickle Cell Clinic.
Figure 1. Maximum-likelihood phylogenetic tree among clinical Staphylococcus aureus strains recovered between 2017 and 2021. The tree was constructed from whole-genome sequence data and visualized using Interactive Tree of Life (iTOL). Strains are annotated with strain ID, year of isolation, hospital ward, clinical diagnosis, clonal complex (CC), sequence type (ST), SCCmec type, and spa type, NA: Not Applicable. A&E, Accident & Emergency; ENT, Ear, Nose, and Throat; EPU, Emergency Pediatric Unit; FSW, Female Surgical Ward; FMW, Female Medical Ward; GOPD, General Outpatient Department; MSW, Male Surgical Ward; NHIS, National Health Insurance Scheme; NICU, Neonatal Intensive Care Unit; O&G, Obstetrics & Gynecology; ORTHO, Orthopedic Ward; PSW, Pediatric Surgical Ward; PMW, Pediatric Medical Ward; SCC, Sickle Cell Clinic.

4 Discussion

Based on phenotypic and molecular methods, we investigated the antimicrobial resistance and virulence genes, as well as the population dynamics of S. aureus from clinical samples in North Central Nigeria. The most frequent clinical presentations were wound infections, and 58% of strains from this source were MRSA, which is similar to reports from other African settings (Monk et al., 2025; Wangai et al., 2019). All strains were susceptible to daptomycin, fosfomycin, fusidic acid, linezolid, mupirocin, rifampicin, glycopeptides, and tigecycline, corroborating previous Nigerian studies (Adeyanju et al., 2022; Shittu et al., 2011). Previous studies also reported that some of these antibiotics, such as fusidic acid, fosfomycin, linezolid, mupirocin, rifampicin, and tigecycline, are effective against S. aureus with low resistance rates (<3%) across various regions in Africa, including Ghana (Egyir et al., 2014), Nigeria (Adeyanju et al., 2022), Mozambique (Garrine et al., 2023), and Ethiopia (Verdú-Expósito et al., 2020). The low S. aureus resistance rates to these antibiotics may indicate their limited use due to high cost and lack of availability (Abubakar and Salman, 2024; Kallberg et al., 2018; Pauwels et al., 2021). Penicillins, cephalosporins, aminoglycosides, fluoroquinolones, sulfonamides, macrolides, and tetracyclines are the most common antibiotics prescribed in Nigeria (Abubakar and Salman, 2024; Egwuenu et al., 2024). This study documented a moderate S. aureus resistance rate (>30%) to tetracycline, gentamicin, the fluoroquinolones, and a high resistance rate (>90%) to penicillin and trimethoprim-sulfamethoxazole (>70%), which is comparable with regional data (Adeyanju et al., 2022; Garrine et al., 2023; Perovic et al., 2015; Shittu et al., 2011).

PVL-positive S. aureus strains are associated with SSTIs, necrotizing pneumonia, and severe sepsis, often leading to poor clinical outcomes, particularly in children (Garbo et al., 2024; Da Qu et al., 2022). PVL-positive S. aureus is endemic in Africa (Schaumburg et al., 2014). In this study, more than 60% of strains were PVL-positive, which is similar to reports from Southwest Nigeria (70%) (Olalekan et al., 2025) and The Gambia (61%) (Darboe et al., 2019). The prevalence of PVL-positive S. aureus varies across regions in Nigeria, including South–South (13–52%) (Ide et al., 2025; Obasuyi et al., 2020), South-West (13–82%) (Adeyanju et al., 2022; Ayepola et al., 2015), North Central (31%) (Essien et al., 2021), and North East Nigeria (10.9%) (Onanuga et al., 2021). Although PVL is typically more prevalent among MSSA in Africa (Olalekan et al., 2025; Schaumburg et al., 2014), this study found no significant difference (68% vs. 62%; p < 0.40). The high prevalence of PVL-positive S. aureus in North Central Nigeria reinforces its endemicity in Africa and underscores its clinical importance. Although PVL-positive S. aureus strains were detected in various clinical presentations (Supplementary File 1), the primary clinical diagnosis in this study was wound infections (including SSTIs), accounting for 52% of cases. PVL-positive S. aureus has been associated with SSTIs in Africa (Schaumburg et al., 2014) and may explain the high prevalence observed in this study. Host, pathogen, or environmental factors may contribute to the spread of PVL-positive S. aureus in Africa. A recent study indicated that the high prevalence of PVL-positive S. aureus in Africa could be attributed to the susceptibility of polymorphonuclear (PMN) cells in the African population to PVL and an increased inflammatory response (Grebe et al., 2025). This could lead to excessive PMN infiltration and lysis, enhanced tissue destruction, and necrotizing infections.

The dominant S. aureus lineages (CC1, CC8, and ST152) were identified in various clinical samples, which is similar to recent reports in Ghana and Nigeria (Egyir et al., 2024; Olalekan et al., 2025). CC1-ST772-MRSA (Bengal Bay clone) emerged in India, spreading locally in hospitals and communities before rapidly spreading worldwide through medical tourism (Steinig et al., 2019). In this study, MDR CC1-ST772-MRSA-V-t657 was the predominant MRSA lineage, consistent with recent reports on human nasal samples (Ogundipe et al., 2020) and clinical samples (Olalekan et al., 2025) in South-West Nigeria. It has been associated with necrotizing fasciitis (Sabat et al., 2022) and outbreaks at the NICU (Brennan et al., 2012) as well as SSTIs (Blomfeldt et al., 2017). Our study provides evidence that the prevalence of the MDR CC1-ST772-MRSA-V clone is increasing in Nigeria (O’Malley et al., 2015; Obasuyi et al., 2020; Ogundipe et al., 2020; Olalekan et al., 2025; Essien et al., 2021) after the first documented case over a decade ago (Raji et al., 2013). The MDR CC8-ST789-MRSA-V was also one of the common MRSA clones in this study. This lineage has been reported in Africa (Ogundipe et al., 2020; Olalekan et al., 2025; Schaumburg et al., 2022) including colonized individuals (Laurence Yehouenou et al., 2023) and patients with SSTIs (Schaumburg et al., 2022). It has also been linked with zoonotic transmission potential (Ogundipe et al., 2020). The emergence of CC8-ST789-MRSA-V in Nigeria, with its MDR phenotype and reported cases in both human and animal hosts, highlights the need for strengthened One Health surveillance to understand its transmission dynamics and public health significance.

The PVL-positive ST152 was the most common lineage (35%), including both MSSA and MRSA (Figure 1; Table 3). This clone has consistently been reported as among the dominant lineages in Africa, particularly in Central and West Africa (Lawal et al., 2022). The high proportion of MRSA, particularly ST152-MRSA-Vc-t4690, is noteworthy (Tables 3, 5). This observation is similar to recent findings in Nigeria (Olalekan et al., 2025) but differs from the predominant ST152-MRSA-Va-t355 identified in Ghana (Egyir et al., 2024) and Kenya (Nyasinga et al., 2024). Our study also identified an ST152-MRSA-XIII-t355 strain from a patient with an eye infection at the NICU, and likely the first report in North Central Nigeria. These observations suggest that ST152-MRSA may have emerged through multiple independent acquisitions of SCCmec elements rather than clonal expansion. Previous genomic studies have demonstrated that MRSA frequently emerged through the horizontal acquisition of SCCmec by MSSA progenitors, followed by clonal diversification under antimicrobial selection pressure (Deurenberg et al., 2007). The coexistence of MSSA and MRSA strains within the ST152 lineage supports the hypothesis of independent SCCmec acquisition events within an established MSSA background, a phenomenon previously documented in African S. aureus populations (Baig et al., 2020).

In this study, representative PVL-positive ST152 strains retained an intact haemolysin (hlb) gene (Table 5). While many human-adapted strains carry φSa3-like prophages that integrate into the hlb locus and introduce immune evasion cluster genes, not all PVL-positive S. aureus strains experience hlb disruption (Rohmer and Wolz, 2021). Some community-associated and livestock-adapted strains retain an intact hlb (Egyir et al., 2024; Lebughe et al., 2017; Shittu et al., 2021). The co-occurrence of PVL and β-hemolysin may enhance pathogenicity, as Hlb-sphingomyelinase activity can synergize with PVL-mediated leukocyte cytotoxicity, potentially promoting tissue colonization, destruction, and immune evasion (Di Bella et al., 2025).

Our study found diverse S. aureus lineages in some clinical presentations (Table 4). We observed diverse S. aureus lineages (>4 CCs) in bloodstream, upper respiratory tract, urogenital, and wound samples. S. aureus strains assigned to CC1 and ST152 were identified in all categories of clinical presentations, whereas those grouped with CC8 were observed in all infection groups except eye infections. Moreover, phylogenetic analysis revealed strain diversity across both inpatient and outpatient units (Figure 1), suggesting overlapping transmission dynamics among lineages, particularly classical community-associated MRSA (CA-MRSA) clones. SCCmec types IV and V are classically linked to CA-MRSA (Lakhundi and Zhang, 2018). The substantial genetic heterogeneity suggests possible endemic circulation of different lineages in the healthcare institution. The emergence of PVL-positive clones (e.g., ST152-MRSA-V and CC1-ST772-MRSA-V) across different wards, particularly in the NICU, raises the possibility of localized nosocomial transmission. These findings underscore the importance of molecular surveillance, improved infection prevention and control strategies, and integrating genomic data with clinical information to mitigate MRSA spread in hospital settings.

This study has some limitations. The retrospective, single-centre design carries inherent selection bias, and the disproportionate representation of wound infection strains (52%) might limit the generalization of the findings to broader clinical and community settings. Nevertheless, this study provides a comprehensive genomic study of S. aureus in North Central Nigeria. It highlights the emergence of MDR and hypervirulent S. aureus clones in the health-care facility. Although the number of strains analyzed is insufficient to generalize the findings, identifying hypervirulent and MDR S. aureus clones in the hospital underscores the need for effective infection prevention and control strategies, antimicrobial stewardship, and genomic surveillance.

5 Conclusion

This study describes a diverse S. aureus clonal population and high prevalence of MRSA and MDR S. aureus in a tertiary hospital in North Central Nigeria. The emergence of hypervirulent MRSA lineages, particularly CC1-ST772 and ST152, poses significant challenges for clinical management and infection control. These findings underscore the need for genomic surveillance integrated with infection prevention and control and antimicrobial stewardship programs to limit the spread of these high-risk clones.

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Supplementary material

The Supplementary material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fmicb.2026.1908867/full#supplementary-material

Supplementary material Supplementary material at the source

Supplementary material Supplementary material at the source

Supplementary material Supplementary material at the source

Footnotes

Edited by: Kunyan Zhang, University of Calgary, Canada

Reviewed by: Remous Ocloo, TASK Applied Science, South Africa

Muammer Çelik, Dokuz Eylul University, Türkiye

Footnotes

https://cge.cbs.dtu.dk/services/SCC*mec*Finder/

https://usegalaxy.org

Footnotes

CC, Clonal Complex; CA-MRSA, Community-acquired Methicillin-resistant Staphylococcus aureus; DNA, Deoxyribonucleic acid; EUCAST, European Committee on Antimicrobial Susceptibility Testing; iTOL, Interactive Tree of Life; MALDI-TOF MS, Matrix-Assisted Laser Desorption/Ionization Time-of-Flight Mass Spectrometry; MAFFT, Multiple-sequence alignment Fast Fourier Transform; MLST, Multilocus Sequence Typing; MSSA, Methicillin-susceptible Staphylococcus aureus; NCBI, National Center for Biotechnology Information; NEB, New England Biolabs; NRPS, nonribosomal peptide synthetase; PCR, Polymerase Chain Reaction; S. aureus, Staphylococcus aureus; SCCmec, Staphylococcal Cassette Chromosome mec; ST, Sequence Type; SMRT, Single Molecule Real Time; WGS, Whole-Genome Sequencing.

Statements

Conflict of interest

The author(s) declared that this work was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Funding

The author(s) declared that financial support was received for this work and/or its publication. The Deutsche Forschungsgemeinschaft (German Research Foundation; grant 404893180) supported RR, and TA is a postdoctoral fellow sponsored by the AMIR Fund. The Alexander von Humboldt Foundation (Georg Forster-Forschungsstipendium -NGA 1203003 -GF-E) supported AS. We acknowledge the support from the Open Access Publication Fund of the University of Münster.

Data availability

The datasets presented in this study can be found in online repositories. The names of the repository/repositories and accession number(s) can be found in the article/Supplementary material.

Ethics approval

Ethics approval was obtained from the University of Ilorin Teaching Hospital Ethics Review Board (ERC PAN/2017/07/1698). The studies were conducted in accordance with the local legislation and institutional requirements. The human samples used in this study were acquired from a by- product of routine care or industry. Written informed consent for participation was not required from the participants or the participants’ legal guardians/next of kin in accordance with the national legislation and institutional requirements.

Author contributions

RR: Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Validation, Writing – original draft, Writing – review & editing. CN: Conceptualization, Methodology, Writing – review & editing. AF: Supervision, Writing – review & editing, Conceptualization. BO: Data curation, Writing – review & editing. AH: Data curation, Investigation, Writing – review & editing. TA: Data curation, Formal analysis, Visualization, Writing – review & editing. TS: Data curation, Formal analysis, Visualization, Writing – review & editing. AM: Data curation, Formal analysis, Methodology, Visualization, Writing – review & editing. FS: Funding acquisition, Methodology, Project administration, Resources, Validation, Writing – review & editing, Conceptualization, Data curation, Visualization. AS: Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Supervision, Validation, Writing – review & editing, Visualization.

Acknowledgements

The authors thank the Medical Microbiology Diagnostic Laboratory at the University of Ilorin Teaching Hospital in Nigeria for facilitating the phenotypic identification of Staphylococcus aureus and the Institute of Medical Microbiology at the University Hospital Münster in Germany for their support in the molecular characterization.

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Citation

Raheem, R. A., et al. (2026). Diverse Staphylococcus aureus lineages in a tertiary hospital in North Central Nigeria: emergence of CC1-ST772-MRSA, CC8-ST789-MRSA, and ST152-MRSA. Frontiers in Microbiology, Volume 17. https://doi.org/
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17 - 2026

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Copyright © 2026 Raheem, Nwabuisi, Fadeyi, Olanipekun, Hamzat, Adesoji, Sulayman, Mellmann, Schaumburg and Shittu.

License: https://creativecommons.org/licenses/by/4.0/

*Correspondence: Rasaki Adewole Raheem; Frieder Schaumburg

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