Methicillin-resistant Staphylococcus aureus colonization and associated factors in clinical isolates among patients attending a tertiary medical centre in Nigeria

Abstract

Background

The burden of methicillin-resistant Staphylococcus aureus (MRSA) constitutes a major public health issue globally. However, there is a paucity of information concerning the prevalence and trends in antibiotic resistance of MRSA in clinical samples in the study area. This study aimed to determine the prevalence and associated risk factors of MRSA in clinical isolates from patients at the Federal Medical Centre (FMC), Azare, Nigeria.

Methods

A cross-sectional study was performed in a hospital from January to May 2024. A total of 210 clinical samples were collected from the study participants. Data concerning sociodemographic variables and associated risk factors were gathered using structured questionnaires. Clinical samples were obtained aseptically, and S. aureus was identified using standard microbiological methods. MRSA was detected using cefoxitin discs, and the antimicrobial Susceptibility profiles to different antibiotics were performed using the Kirby-Bauer disk diffusion method. Multivariate logistic regression tests were conducted, with a significance level set at P < 0.05.

Results

Of the 210 blood, urine, and wound swab samples analyzed, the overall prevalence of S. aureus and MRSA was 13.8% (29/210; 95% CI: 9.40–19.20) and 4.2% (9/210; 95% CI: 2.0–8.0), respectively. The multivariate analysis indicates that female (AOR) (95% CI): 10.023 (1.033–97.228)], wound swab specimen (AOR) (95% CI): 12.860 (1.236-133.833)] and history of hospitalization (AOR) (95% CI): 10.223 (1.712–61.044) were associated with MRSA infection. All 9 MRSA isolates showed resistance to penicillin, oxacillin, and cefoxitin, while others exhibited varying levels of resistance, with azithromycin showing the lowest resistance (66.7%). All the isolates showed multidrug resistance.

Conclusion

Based on the findings, the clinical samples showed a reduced incidence of MRSA compared to other studies conducted in Nigeria. The alarming factor is the presence of MDR in all MRSA isolates, emphasizing the need for regular testing to prevent endogenous infections.

Supplementary Information

The online version contains supplementary material available at 10.1186/s12879-025-12166-w.

Introduction

Staphylococcus aureus (S. aureus) is a Gram-positive coccus bacterium that colonizes the human body and is responsible for a range of substantial clinical diseases globally, including endocarditis, osteomyelitis, and skin and soft tissue infections [1, 2]. Its pathogenicity is complex, including resistance to antimicrobial agents [1]. S. aureus isolates were initially responsive to beta-lactam antibiotics, but eventually became resistant to these drugs. The synthesis of the beta-lactamase enzyme and the integration of a mecA gene into its chromosome at a designated locus confer resistance [3, 4].

Some strains of S. aureus are identified as methicillin-resistant Staphylococcus aureus (MRSA) due to their resistance to methicillin. Methicillin was introduced in the 1960s to address certain infections caused by penicillin-resistant S. aureus [5]. However, the evolution of the MRSA shortly after compounded the issue by exhibiting cross-resistance to all beta-lactam (𝛽-lactam) antibiotics. The residual S. aureus strains exhibit susceptibility to methicillin and are commonly referred to as methicillin-susceptible Staphylococcus aureus (MSSA) [6].

MRSA strains are predominantly linked with significant nosocomial infections, designated as healthcare-associated MRSA (HA-MRSA) [6]. In addition to HA-MRSA strains, community-acquired MRSA (CA-MRSA) infection has also been documented in various studies [6, 7]. The CA-MRSA may result from livestock-associated MRSA (LA-MRSA), which are mostly linked to animals (such as chickens and cattle) and have distinct genotypic characteristics compared to HA-MRSA and CA-MRSA [8].

MRSA are the most often documented multidrug-resistant bacteria globally. Despite ongoing advancements in innovative medication, proactive monitoring programs, and enhancements in the prevention of infection, the swiftly escalating prevalence of HA-MRSA presents significant contributors to public health, clinical, and economic challenges [9, 10]. These challenges have resulted in an increased morbidity and mortality in hospitals globally over recent decades [9].

MRSA remains a significant pathogen in hospital-acquired infections in developing nations [11]. The presence of antimicrobial-resistant strains such as MRSA significantly increases an individual’s susceptibility to infection [12]. The expected incidence of disease following MRSA acquisition is approximately 30% [12].

The carriage rates of MRSA significantly differ across countries, healthcare facilities within the same country, and the specific population under investigation. Some studies indicate that the incidence of MRSA infection upon hospitalization varies between 2.6% and 8%, with elevated rates observed in older individuals [5, 13]. Similarly, WHO indicates that MRSA prevalence levels surpass 20% in all areas, with certain nations documenting rates as high as 80%, and roughly 80–95% of MRSA carriers are asymptomatic [9, 12]. In Nigeria, the prevalence rates of MRSA vary among geographical locations, with an increase from 18.3% in 2019 to 48.9% in 2021 [14].

Notwithstanding the importance of MRSA infections for public health, data regarding MRSA carriage rates in the present study area are scarce. This study aimed to determine the prevalence of MRSA, identify associated risk factors, and assess the antimicrobial susceptibility profile and multidrug resistance (MDR) to commonly used antibiotics among patients at the Federal Medical Centre (FMC), Azare, northeast Nigeria.

Materials and methods

Study design and study population

The study is a cross-sectional investigation conducted at FMC from January to May 2024. The FMC, a tertiary medical institution with approximately 350 beds for patient care, is situated in Azare, Katagum Local Government Area, Bauchi State, Northeastern Nigeria. All patients admitted to FMC during the study period who met the inclusion criteria constituted the study population.

Inclusion and exclusion criteria

The study included patients who were admitted to FMC during the data collection period for treatment and had signed the informed consent form (ICF). For participants who are minors, informed consent was obtained from their parents or legally authorized representatives (LARs). Exclusion criteria were implemented for those in the study who were not admitted to FMC Azare, who had taken antibiotics within the past two (2) weeks, as this could potentially impact the study’s findings by underrepresenting the prevalence of antibiotic-resistant bacteria in the population, and study participants who refused to sign the informed consent form.

Sample size determination and sampling techniques

The sample size for this study was determined using the single population method, predicated on the prevalence of MRSA from clinical isolates in tertiary hospitals in northeastern Nigeria, which was 12.5% [15]. The margin of error was established at 5%, with a 95% confidence interval (alpha = 0.05).

In this context, n denotes the sample size, p represents the prevalence of MRSA among clinical isolates (12.5%), q is defined as (1-p), z equals 1.96, and d represents the accuracy.

A minimum sample size of 168.07 was established. Nonetheless, the determined sample size was adjusted to 210, establishing it as the foundational sample size for our study, thus mitigating any skew in the selection of participants.

A simple random sampling method, using the lottery method, was employed to recruit study participants who met the inclusion criteria after assigning them a unique identification number. The numbers were written on slip papers, thoroughly mixed in a container, and then randomly picked without replacement until the target sample size of 210 was achieved.

Ethical issue

The Federal Medical Center’s (FMC) Ethical Research and Review Committee (ERRC), Bauchi State, Nigeria, approved the study on January 12, 2024, prior to its commencement, with reference ID FMCA/COM/35/V1. All obtained information was regarded as very confidential.

Data collection

After obtaining informed written consent, a structured questionnaire was distributed to participants to gather their sociodemographic characteristics. The questionnaire was developed based on a previous literature study and used as a research instrument. An expert in the field validated the content validity, corroborated by a recent study [3, 4, 9, 16]. The questionnaire collected data on risk factors, including a history of hospitalizations, skin infections, and prior antibiotic treatment for MRSA infections, as well as sociodemographic characteristics.

Sample collection and examination

Standard microbiological procedures were used to collect various clinical samples from patients. Sterilized containers and swabs were used to collect blood, urine, and wound swabs. To prevent any potential contamination, all specimens were delivered right away to the Microbiology laboratory of the Department of Microbiology. Clinical specimens were inoculated onto sheep blood agar (Oxoid, Basingstoke, Hampshire, England) and mannitol salt agar (MSA) (Oxoid, Basingstoke, Hampshire, England) and aerobically incubated for 24 h at 37 °C. Yellow colonies on MSA, colony features on blood agar, and catalase and coagulase tests were used to identify presumed S. aureus. Gram-positive cocci that showed a yellow appearance on mannitol salt agar and tested positive for both coagulase and catalase were regarded as S. aureus colonies.

Antimicrobial susceptibility testing

According to the standards established by the Clinical and Laboratory Standards Institute [17], the Kirby-Bauer disc diffusion technique was used to determine the antimicrobial susceptibility profile. The CLSI guidelines were also adhered to for the identification of MRSA isolates using a cefoxitin disk (30 µg) [17]. The zone of inhibition surrounding each antimicrobial disk was measured and analyzed using the CLSI interpretation chart to ascertain the antimicrobial resistance pattern of the S. aureus isolate. Isolates exhibiting a zone of inhibition ≤ 21 mm surrounding the cefoxitin disk were classified as MRSA isolates [18].

Multidrug resistance (MDR)

Isolates were classified as multidrug-resistant (MDR) if they exhibited resistance to a minimum of three classes of antimicrobial drugs [19].

Data quality control

Standard operating procedures (SOPs) were meticulously adhered to for every laboratory activity. To verify the questionnaire’s validity, 10% of the sample size was pre-tested from a given population. The sterility of the culture media was verified by incubating 5% of it at 37 °C for 24 h without inoculation. Furthermore, standard positive control strains of S. aureus (ATCC 25923) were employed to assess the quality of the culture media and antimicrobial disks [17].

Data analysis and interpretation

Data were entered, cleaned, and analyzed using Statistical Package for Social Sciences (SPSS) software version 25. Descriptive statistics were presented as frequencies and percentages, while inferential statistics, including bivariate and multivariate logistic regression analyses, were used to assess the relationship between independent and dependent categorical variables. All independent variables with a p-value of 0.05 or lower in the bivariate analysis were included in the subsequent multivariate logistic regression model to identify variables that were independently associated. A p-value < 0.05 was deemed statistically significant, and adjusted odds ratio (AOR) and 95% confidence interval (CI) were employed to assess the strength of the relationship between factors.

Results

Sociodemographic characteristics

Out of 210 samples analysed, 51.4% (108/210; 95% CI: 44.5–58.4) were male, with the majority in the 19–30 age group, at 37.1% (78/210; 95% CI: 30.6–44.1). Among the participants in the present study, 58.1% (122/210; 95% CI: 51.1–64.8) were single, 63.3% (133/210; 95% CI: 56.4–69.9) resided in urban residences, 39.5% (83/210; 95% CI: 32.9–46.5) had a tertiary educational level, and most of them were students, 48.1% (101/210; 95% CI: 41.2–55.1). The majority of the study participants were Hausa by tribe, comprising 86.2% (181/210; 95% CI: 80.8–90.6), with the majority having a family size of less than 3, 45.2% (95/210; 95% CI: 38.4–52.2). Additionally, the majority had a monthly income of less than ₦30,000, 44.8% (94/210; 95% CI: 37.9–51.8) as shown in Table 1.

Table 1.

Sociodemographic characteristics of patients attending FMC, Azare, Bauchi, Nigeria

Characteristics	n (%)	Percentage
Gender
Male	108	51.4
Female	102	48.6
Age group
< 10 years	32	15.2
11–18 years	55	26.2
19–30 years	78	37.1
31–45 years	42	20.0
> 46 years	3	1.4
Residence
Urban	133	63.3
Rural	77	36.7
Marital status
Single	122	58.1
Married	83	39.5
Divorced	2	1.0
Widow	3	1.4
Occupation
Housewife	43	20.5
Farmer	26	12.4
Civil servant	18	8.6
Students	101	48.1
Business	22	10.5
Ethnicity
Hausa	181	86.2
Fulani	19	9.0
Yoruba	8	3.8
Igbo	2	1.0
Family Size
< 3	95	45.2
3–5	52	23.8
> 5	63	30.0
Monthly income
Less than 30 K	94	44.8
₦30–49 K	50	23.8
₦50–99 K	48	22.9
>₦100 K	18	8.6

Clinical-related characteristics

Of the 210 study participants, 34.8% (73/210; 95% CI: 28.3–41.6) of the specimen collected was from wound swab, 19.5% (41/210; 95% CI: 14.4–25.5) reported antibiotic use in the preceding 3 months, 30.0% (63/210; 95% CI: 23.9–36.7) had been hospitalized in the last 3 months, and 17.1% (36/210; 95% CI: 12.3–22.9) had skin infections as shown in Table 2.

Table 2.

Clinical-related characteristics of patients attending FMC, Azare, Bauchi, Nigeria

Characteristics	n (%)	Percentage
Specimen type
Urine	67	31.9
Wound swab	73	34.8
Blood	70	33.3
Antibiotic use in the last three (3) Months
Yes	41	19.5
No	169	80.5
History of hospitalization
Yes	63	30.0
No	147	70.0
History of skin infection
Yes	36	17.1
No	174	82.9

Prevalence of Staphylococcus aureus

Among the total of 210 clinical samples, S. aureus was isolated from 13.8% (29/210; 95% CI: 9.40–19.20). The rate was relatively high among females, at 18.6% (19/102; 95% CI: 11.6–27.6), compared to 9.3% (10/108; 95% CI: 4.5–16.4) among males. The prevalence was highest among members of the age group between 31 and 45 years 19.0% (8/42; 95% CI: 8.6–31.4), followed by those between the age group of 19–30 years 15.4% (12/78; 95% CI: 8.2–25.3), while there was no colonization among aged 46 and above (0%). The prevalence of S. aureus was highest among wound swab specimens 22.2% (16/72; 95% CI: 13.3–33.6), followed by urine samples which was 11.8% (8/68; 95% CI: 5.2–21.9), while the lowest was recorded among blood specimens which was 7.1% (5/70; 95% CI: 2.4–15.9) (Table 3).

Table 3.

Prevalence of S. aureus and MRSA among clinical samples at FMC Azare, Nigeria

Characteristics	S. aureus		MRSA
	Positive (n = 29) (%)	Negative (n = 181) (%)	Positive (n = 9) (%)	Negative (n = 20) (%)
Gender
Male	10 (9.3)	98 (90.7)	1 (8.3)	11 (91.7)
Female	19 (18.6)	83 (81.4)	8 (47.1)	9 (52.9)
Age group
< 10 years	3 (9.4)	29 (90.6)	1 (33.3)	2 (66.7)
11–18 years	6 (10.9)	49 (89.1)	0 (0.0)	6 (100.0)
19–30 years	12 (15.4)	66 (84.6)	4 (33.3)	8 (66.7)
31–45 years	8 (19.0)	34 (81.0)	4 (50.0)	4 (50.0)
> 46 years	0 (0.0)	3 (100.0)	0 (0.0)	0 (0.0)
Specimen type
Urine	8 (11.8)	60 (88.2)	1 (12.5)	7 (87.5)
Wound swab	16 (22.2)	56 (77.8)	8 (50.0)	8 (50.0)
Blood	5 (7.1)	65 (92.9)	0 (0.0)	5 (100.0)

Prevalence of MRSA

Of the 29 S. aureus isolates, nine (9) were identified as MRSA, resulting in an incidence of 31.0% (9/29; 95% CI: 15.3–50.8) within S. aureus-positive individuals. The overall prevalence of MRSA was 4.3% (9/210; 95% CI: 2.0–8.0); females accounted for the highest proportion, 47.1% (8/17; 95% CI: 23.0-72.2), compared to males, 8.3% (1/12; 95% CI: 0.2–38.5). In terms of age, the total MRSA carriage was highest in the 31–45 age group, 50% (4/8; 95% CI: 15.7–84.3), followed by those in the 19–30 age group, while those in the 46 years and above age group recorded the lowest percentage (0.00%). The prevalence was highest in wound swabs, at 50.0% (8/16; 95% CI: 24.7–75.3), followed by urine specimens, at 12.5% (1/8; 95% CI: 0.3–52.7), while the no colonization was observed in blood specimens (0.00%) (Table 3).

Factors associated with the prevalence of MRSA

Table 4 demonstrates that most associated factors, including age, monthly income, occupation, marital status, residence, history of skin infection, educational level, ethnicity, and family size, as determined by univariate and multivariate logistic regression analyses, were not significantly associated with MRSA colonization.

Table 4.

Bivariate and multivariate analysis of characteristics correlated with MRSA in hospitalized patients at FMC Azare, Nigeria

Characteristics	MRSA, n (%)		Univariate analysis		Multivariate analysis
	Positive	Negative	COR (95% CI)	p-value	AOR (95% CI)	p-value
Sex
Male	1 (0.9)	109 (99.1)	1	1	1
Female	8 (8.0)	92 (92.0)	9.48 (1.16–77.19)	0.036*	10.02 (1.03–97.23) *	0.047
Age
1–10	1 (3.1)	31 (96.9)	1	1
11–18	0 (0.0)	55 (100.0)	0.0 (0.0)	0.997
19–30	4 (5.1)	74 (94.9)	1.68 (0.18–15.60)	0.650
31–45	4 (9.5)	38 (90.5)	3. 26 (0.35–30.72)	0.301
> 45	0 (0.0)	3 (100.0)	0.0 (0.0)	0.999
Marital status
Singled	4 (3.3)	118 (96.7)	1	1
Married	5 (6.0)	78 (94.0)	1.89 (0.50–7.26)	0.353
Divorced	0 (0.0)	2 (100.0)	0.0 (0.0)	0.999
Widowed	0 (0.0)	3 (100.0)	0.0 (0.0)	0.999
Residence
Urban	6 (4.5)	127 (95.5)	1.17 (0.28–4.80	0.832
Rural	3 (3.9)	74 (96.1)	1	1
Educational Level
Cannot read	2 (5.4)	35 (94.6)	1.52 (0.24–9.53)	0.652
Primary	0 (0.0)	29 (100.0)	0.0 (0.0)	0.998
Secondary	4 (6.6)	57 (93.4)	1.871 (0.40–8.69)	0.424
Tertiary	3 (3.6)	80 (96.4)	1	1
Occupation
Housewife	2 (4.7)	41 (95.3)	1.02 (0.09–11.96)	0.985
Farmer	0 (0.0)	26 (100.0)	0.0 (0.0)	0.998
Civil servant	0 (0.0)	18 (100.0)	0.0 (0.0)	0.998
Student	6 (5.9)	95 (94.1)	1.33 (0.15–11.61)	0.799
Businessman	1 (4.5)	21 (95.5)	1	1
Ethnicity
Hausa	8 (4.4)	173 (95.6)	1	1
Fulani	1 (5.3)	18 (94.7)	1.20 (0.14–10.16)	0.866
Yoruba	0 (0.0)	8 (100.0)	0.0 (0.0)	0.999
Igbo	0 (0.0)	2 (100.0)	0.0 (0.0)	0.999
Family size
< 3	3 (3.2)	92 (96.8)	1	1
3–5	2 (3.8)	50 (96.2)	1.23 (0.20–7.59)	0.826
> 5	4 (6.3)	59 (93.7)	2.08 (0.45–9.62)	0.349
Monthly Income
< 30k	3 (3.2)	91 (96.8)	1	1
30-50k	4 (8.0)	46 (92.0)	2.64 (0.57–12.28)	0.217
50-100k	1 (2.1)	47 (97.9)	0.645 (0.07–6.38)	0.708
100k above	1 (5.6)	17 (94.4)	1.78 (0.18–18.19)	0.625
Specimen type
Urine	1 (1.5)	67 (98.5)	1	1
Wound swap	8 (11.1)	64 (88.9)	8.38 (1.02–68.87)	0.048*	12.86 (1.24-133.83) *	0.033
Blood	0 (0.0)	70 (100.0)	0.0 (0.0)	0.997	0.0 (0.0)	0.997
History of antibiotics used
Yes	5 (12.5)	36 (87.8)	5.73 (1.47–22.40)	0.012*	4. 71 (0.90-24.78)	0.067
No	4 (2.4)	165 (97.6)	1	1	1
History of hospitalization
Yes	7 (11.1)	56 (88.8)	9.06 (1.83–44.95)	0.007*	10.22 (1.71–61.04) *	0.011
No	2 (1.4)	145 (98.6)	1	1
History of skin infection
Yes	1 (2.8)	35 (97.2)	0.59 (0.07–4.89)	0.627
No	8 (4.6)	166 (95.4)	1	1

* Statistically significant

However, the univariate analysis revealed that the factors correlated with MRSA among the study participant included female gender [COR (95% CI): 9.478 (1.164–77.192] (p = 0.036), wound swab specimen [COR (95% CI): 8.375 (1.019–68.865)] (p = 0.048), history of taking antibiotics [COR (95% CI): 5.729 (1.466–22.396)] (p = 0.012) and history of hospitalization [COR (95% CI): 9.062 (1.827–44.951)] (p = 0.07) (Fig. 1).

Fig. 1.

Forest plot illustrating the Crude Odds Ratio (COR) of the factors associated with the prevalence of MRSA in clinical specimens at FMC, Azare, Northeast Nigeria

Nevertheless, after controlling for the confounding effects of these variables through multivariate regression, only three (3) variables were identified as statistically significant with MRSA among the study participants. The multivariate analysis shows that the likelihood of MRSA occurrence was approximately 10.02 times higher among females [AOR (95% CI): 10.02 (1.03–97.23), p = 0.047] compared to males. Similarly, the results show that the likelihood of MRSA occurrence was approximately 12.86 times higher in wound swab specimens [AOR (95% CI): 12.86 (1.24-133.83), p = 0.033] compared to urine specimens. Finally, the multivariate analysis also shows that the relative risk of MRSA occurrence was approximately 10.22 times higher among patients with a history of hospitalization [AOR (95% CI): 10.22 (1.71–61.04), p = 0.011] compared to those without one, as shown in Fig. 2.

Fig. 2.

Forest plot illustrating the adjusted odds ratio (AOR) of the factors associated with the prevalence of MRSA in clinical specimens at FMC, Azare, Northeast Nigeria

Antimicrobial susceptibility patterns

An antimicrobial susceptibility test was conducted on 29 S. aureus isolates. Among 29 isolates of S. aureus, 31.0% (9/29; 95% CI: 15.3–50.8) were identified as MRSA, while the rest, 69.0% (20/29; 95% CI: 49.2–84.7) were identified as MSSA. Of the total S. aureus isolates (n = 29), 100% were resistant to penicillin and oxacillin. In contrast, susceptibility rates were 69.0% (20/29; 95% CI: 49.2–84.7) for cefoxitin, 65.5% (19/29; 95% CI: 45.7–82.1) for azithromycin, 55.2% (16/29; 95% CI: 35.7–73.6) for tetracycline, and 51.7% (15/29; 95% CI: 32.5–70.6) for vancomycin. Among the 9 MRSA isolates, three (3) were 100% resistant to penicillin, oxacillin, and cefoxitin. Seventy-seven point eight per cent, 77.8% (7/9; 95% CI: 40.0.5–97.2) were resistant to tetracycline and vancomycin, while 66.7% (6/9; 95% CI: 29.9–92.5) were also resistant to azithromycin. For MSSA isolates, 70% (14/20; 95% CI: 45.7–88.1), 65% (13/20; 95% CI: 40.8–84.6), and 80% (16/20; 95% CI: 56.3–94.3) exhibited susceptibility to tetracycline, vancomycin, and azithromycin, respectively, as indicated in Table 5.

Table 5.

Antibiotic susceptibility profile of MRSA isolated from patients attending FMC Azare

Antibiotics	S. aureus isolates (n = 29)	S. aureus isolates (n = 29)		p-value
		MRSA (n = 9) (31.0%;95% CI: 15.3 to 50.8)	MSSA (n = 20) (69.0%;95% CI: 49.2 to 84.7)
Penicillin
Susceptible	0 (0.0)	0 (0.0)	0 (0.0)	0.001
Resistant	29 (100)	9 (100.0)	20 (100.0)
Oxacillin
Susceptible	0 (0.0)	0 (0.0)	0 (0.0)	0.001
Resistant	29 (100)	9 (100.0)	20 (100.0)
Tetracycline
Susceptible	16 (55.17)	2 (22.2)	14 (70.0)	0.017
Resistant	13 (44.83)	7 (77.8)	6 (30.0)
Vancomycin
Susceptible	15 (51.72)	2 (22.2)	13 (65.0)	0.033
Resistant	14 (48.38)	7 (77.8)	7 (35.0)
Azithromycin
Susceptible	19 (65.52)	3 (33.3)	16 (80.0)	0.014
Resistant	10 (34.48)	6 (66.7)	4 (20.0)
Cefoxitin
Susceptible	20 (68.97)	0 (0.0)	20 (100)	0.001
Resistant	9 (31.03)	9 (100.0)	0 (0.0)

Multidrug resistance of Staphylococcus aureus isolates

Among the isolates, 23 (79.31%) were multidrug resistant. Table 6 shows that fourteen isolates (66.7%) were resistant to three or more antimicrobial classes, while two (9.5%) were resistant to all six antimicrobial classes.

Table 6.

Multidrug-resistant pattern of S. aureus isolates among patients attending FMC, Azare

S. aureus (n = 29)	Resistance patterns
	R0	R1	R2	R3	R4	>R5	MDR (%)
MRSA (n = 9)	-	-	-	1 (11.1)	5 (55.6%)	3 (33.3%)	9 (100.0%)
MSSA (n = 20)	-	-	6 (30.0%)	8 (40.0%)	5 (25.0%)	1 (5.0%)	14 (70.0%)
Total (n = 29)	-	-	6 (20.7%)	9 (31.0%)	10 (34.5%)	4 (13.8%)	29 (100.0%)

MSSA refers to methicillin-susceptible Staphylococcus aureus, while MRSA denotes methicillin-resistant Staphylococcus aureus. R0: no resistance; R1: resistant to one antibiotic; R2: resistant to two antibiotics; R3: resistant to three antibiotics; R4: resistant to four antibiotics; R5: resistant to five or more antibiotics

Discussion

MRSA isolates are significant pathogens that cause infections worldwide, resulting in the creation and spread of increasingly virulent and multidrug-resistant strains that cause both nosocomial and community-acquired infections. The swift and accurate identification of MRSA is essential for providing appropriate antibiotic therapy and for reducing the nosocomial spread of MRSA strains. The current study indicates that the prevalence of S. aureus within participants is 13.8% (29/210; 95% CI: 9.40–19.20). This value is lower than those recorded in some part of Nigeria such as Abuja (26.9%) [20], Enugu (18.4%) [21], Kogi (82.7%) [14], and other parts of the world such as Tanzania (34.5%) [22], Ethiopia (23.2%) [10] and Nepal (14.4%) [23]. These inconsistencies might be attributed to differences in the laboratory methods employed to screen MRSA, the study’s duration, the number of samples used, as well as variations in the situations existing in different countries and hospital settings, including measures to prevent infections and standard precautions implemented.

Furthermore, the study revealed that 9 (4.2%) of the isolates were methicillin-resistant. The outcome was comparable to the 5.2% MRSA prevalence in various clinical samples from the Peshawar district in Pakistan (24). However, the figure exceeded the prevalence of MRSA documented in high-income nations, including the Netherlands (0.13%) [24], Germany (2.1%) [25], and Ireland (2.7%) [26]. In contrast, the findings are lower than those reported by Mofolorunsho [14], Adetayo [27] in Nigeria, Gebremeskel [3] in Ethiopia, and Breves [28] in Brazil, who found prevalences of 22.6%, 30.4%, 9.3%, and 31.4%, respectively.

The discrepancies in incidence among various studies may stem from differences in personal hygiene and lifestyle characteristics, the sharing of personal items, densely populated living conditions, direct skin-to-skin contact, study duration, hospitalization, antimicrobial policies, and variations in perceptions and awareness of the study participants regarding the epidemiology of MRSA.

The prevalence of MRSA carriage was higher among female compared to male participants in our study, with a statistically significant difference (p = 0.047). The multivariate analysis reveals that females are tenfold more likely to be MRSA carriers than their male counterparts (AOR: 10.223; 95% CI: 1.033–97.228). The findings align with those of Gebreyesus [29] in Ethiopia, who reported that females are 1.41 times more likely to be MRSA carriers, with a statistically significant difference (p = 0.044). Comparable findings were also documented by Adeiza [30] in Sokoto, Nigeria, and Sharma and Mall [31] in India, who showed that females have a greater incidence of MRSA than males. The high prevalence of MRSA observed in females in this study may be ascribed to increased healthcare-seeking behaviour and hospital visits among female patients. However, the outcome contradicts the findings of Onelum [32] in Nigeria, Joachim [12] in Tanzania, and Adhikari [9] in Nepal, which indicated that gender was not a risk factor for MRSA infection.

The current study revealed a greater incidence of MRSA carriage in two age groups: 31–45 years (9.5%) and 19–30 years (5.1%), however, the difference was not statistically significant (p >0.05). This outcome aligns with previous findings of Ike [33] in Nigeria and Gebremeskel [3] in Ethiopia. The findings indicate that age was not a significant determinant in the acquisition of MRSA infections. However, the results contradict those of Worku [2] in Ethiopia, which indicate that the likelihood of MRSA occurrence was approximately 3.7 times higher among study participants aged 61 years compared to those aged less than 60. Similar findings have been reported by Almeida [34] in Brazil and Shahi [23] in Nepal. The increased susceptibility of this age group can be attributed to their diminished immune system.

In the present study, the occurrence of MRSA was significantly correlated with the type of specimen. Wound swabs yielded the highest proportion of MRSA when compared to urine or blood. The results of multivariate analysis show that the likelihood of MRSA occurrence was 12.86 times higher in wound swabs compared to urine. These findings agree with previous studies reported in Nigeria [32, 35, 36] and other regions of the world, such as Pakistan [37, 38] and Saudi Arabia [39].

Several studies across many populations have demonstrated that sociodemographic features and additional risk factors significantly influence the incidence of MRSA. The multivariate logistic regression analysis indicates that patients with a history of hospitalization are tenfold more likely to acquire MRSA than those without such a history (AOR: 10.223; 95% CI: 1.712–61.044). This finding aligns with comparable results from studies conducted in Nigeria [40] and other regions, including Somalia [16], Ethiopia [41], Saudi Arabia [42], and Brazil [13], which have documented a higher prevalence of MRSA among individuals with a history of hospitalization. This is linked to infectious microorganisms, which may result from frequent hospital visits, especially those involving drug-resistant diseases, and inadequate personal hygiene. Another possible explanation could be attributed to the rapidity with which S. aureus develops resistance to methicillin, a comparable approach for isolating MRSA, and the quick colonization of MRSA.

The emergence of drug-resistant MRSA poses a significant problem in the management and prevention of staphylococcal infections. Consequently, the swift identification of MRSA and clarification of its susceptibility profile are crucial for effective therapy, particularly given the limited therapeutic options available. Literature on the antibiotic susceptibility characteristics of MRSA in clinical isolates from Nigeria’s northeast region is limited.

This study reports that MRSA isolates exhibit resistance to the most frequently utilized antibiotics. Antimicrobial susceptibility profiles were identified in all MRSA isolates, albeit to differing degrees. Resistance was notably observed against the antibiotics, specifically penicillin and oxacillin, both of which are β-Lactam antibiotics, with cefoxitin, exhibiting 100.0% resistance. This was followed by tetracycline and vancomycin, both of which displayed 77.8% resistance, and lastly, azithromycin, which showed 66.7% resistance. The production of β-lactamase and the existence of the mecA gene, which decrease the effectiveness of β-lactam antibiotics, are the reasons why MRSA isolates are highly resistant to penicillin and oxacillin (16).

The complete resistance shown to penicillin aligned with several investigations performed in various geographical areas of Nigeria. For instance, Ariom [36] in Abakaliki, Ebonyi State, reported complete resistance to penicillin among MRSA isolates. In a related study in Zaria, Kaduna State, AbdulAziz [43] documented a 100% resistance rate, whilst Mohammed [44] noted a similar resistance trend in their study at Aminu Kano Teaching Hospital (AKTH) in Kano. The higher resistance of MRSA isolates against penicillin is not unique to Nigeria; comparable resistance trends have been reported in other countries. A meta-analysis conducted by Eshetie [45] revealed 99.1% resistance to penicillin among MRSA strains in multiple regions of Ethiopia. Furthermore, the elevated resistance rate of penicillin identified in the present study aligns with findings from Abie [10] in Ethiopia and Adhikari [9] in Nepal, who also found MRSA isolates resistant to penicillin. More recently, Weldegebreal [18] in Ethiopia and Hassan [16] in Somalia also confirmed near-total resistance to penicillin among MRSA isolates.

These findings strongly suggest that penicillin is no longer effective in treating MRSA infections across several regions in Nigeria and elsewhere in the world. These consistent reports of absolute resistance to penicillin, both locally and internationally, indicate a widespread and well-established trend of resistance in MRSA. These resistances may arise from improper prescriptions stemming from the absence of standardized treatment guidelines [46]. In underdeveloped nations, patients do not adhere to prescribed regimens, and some individuals engage in self-medication [46].

The present study revealed a significant antimicrobial susceptibility pattern, including the complete resistance of MRSA isolates to oxacillin antibiotics. The result aligns with the findings of Oginni [40] in southwest Nigeria, who observed that the MRSA isolates are 96.9% resistant to oxacillin. Moreover, comparable findings have been documented in several regions globally, including Pakistan [37].

The resistance of MRSA isolates to Tetracycline and Erythromycin in the present study exceeded that observed in a study conducted at Nepal’s National Medical College Teaching Hospital, while resistance to Ampicillin was lower [47]. This disparity in the susceptibility profile of MRSA to other antibiotics may be attributed to the differing utilization of these agents for patient treatment across various geographic regions.

Multiple investigations conducted globally indicate that the resistance of MRSA isolates to vancomycin varies substantially depending on the study location [9]. The variation occurs from none (0.0%) in Somalia [16], Nepal [4, 48, 49], Pakistan [37], Saudi Arabia [50], to as high as 0.33% in India [51]. The absence of resistance noted in their investigation prompted the recommendation that vancomycin be utilized as the preferred antibiotic for treating MRSA and MDR in the studied regions. In contrast, the present study found a high resistance rate (77.8%) of MRSA isolates to vancomycin. This finding aligns well with the study by Olowe [52] in southwest Nigeria, which reported 62.5% resistance to vancomycin. These findings are worrisome as this necessary antibiotic cannot be used as the preferred treatment for MRSA in the research location.

A notable disparity was observed in the resistance of MRSA and MSSA to all six antibiotics used in the present study. The result aligns with studies conducted in Nepal, which have noted a substantial disparity in the resistance of MRSA and MSSA isolates to penicillin and tetracycline. Similarly, a study in Egypt by Mohamed [53] revealed a notable disparity in antibiotic resistance between MRSA and MSSA concerning cefoxitin and oxacillin.

The multidrug resistance exhibited by MRSA is presently seen as a global threat [46]. In this study, multidrug resistance was defined as resistance to three or more classes of the tested antimicrobial agents. In the current study, all MRSA isolates (100%, 9/9) were multidrug-resistant, whereas 70.0% (14/20) of MSSA isolates were also multidrug-resistant. This is comparable to 92.9% multidrug resistance observed in clinical samples in Sokoto, Northwest Nigeria [54]. However, the MDR identified in our study exceeded that reported in certain regions of Nigeria, such as Enugu state (72.0%) [21], Ogun state (71.6%) [55], Abuja (68.0%) [20], as well as in other countries such as Ethiopia (88.5%) [3] and Iran (80.5%) [56]. The elevated levels of antibiotic resistance identified in our study may be attributed to the widespread usage of these antibiotics in the study area for treating S. aureus infections without proper prescription. Other factors that may contribute to this issue include self-medication and the accessibility of over-the-counter medications, which are often provided without an antibiotic susceptibility test or a prescription. Moreover, factors such as the excessive consumption rate of antibiotics, the sale of counterfeit or substandard medications, and the unregulated use of antimicrobials in livestock, including poultry and fisheries, may also be linked to antibiotic resistance.

Furthermore, the current study demonstrated that age, marital status, ethnicity, residence, and educational level did not serve as predictors for MRSA prevalence, aligning with findings from studies conducted in the East Wallaga zone, Ethiopia [57], and Douala, Cameroon [58]. Moreover, monthly income was not statistically associated with MRSA, contrasting with the findings of Gebremeskel [3] in Hawassa, Ethiopia, which indicated a substantial correlation. Nonetheless, sociodemographic characteristics, including marital status and ethnicity, were included in the study to provide a comprehensive overview of the study population’s sociodemographic characteristics. These variables denote the demographic characteristics of the local community, which are predominantly Hausa and young, and were not intended or designed to suggest any direct causal association with MRSA colonization or infection.

Conclusion

Our study demonstrates that MRSA poses a considerable public health concern in Nigerian tertiary medical institutions. The alarming multidrug resistance, which renders most antibiotics ineffective, underscores the need to formulate, implement, and enforce suitable control measures in hospital environments. Health education, mandatory antibiotic susceptibility testing before antibiotic prescription, and prudent use of antimicrobial agents are crucial in mitigating the rise in MRSA incidence and antibiotic resistance.

Supplementary Information

Below is the link to the electronic supplementary material.

Abbreviations

MRSA

Methicillin resistant Staphylococcus aureus

MSSA

Methicillin susceptible Staphylococcus aureus

HA-MRSA

Healthcare-Associated Methicillin-resistant Staphylococcus aureus

CA-MRSA

Community-acquired Methicillin-resistant Staphylococcus aureus

LA-MRSA

Livestock-associated Methicillin-resistant Staphylococcus aureus

MDR

Multidrug resistance

MSA

Mannitol salt agar

CLSI

Clinical and Laboratory Standards Institute

SOPs

Standard Operating Procedures

SPSS

Statistical Package for Social Sciences

β-LactamA

Beta-Lactam

WHO

World Health Organization

FMC

Federal Medical Centre

COR

Crude Odd Ratio

AOR

Adjusted Odds Ratio

CI95%

95% Confidence Interval

Author contributions

The work was designed and conceptualized by UB and BMA. UB did the laboratory analysis and data gathering. BMA and IMM oversaw the laboratory analysis and data gathering. BMA and AMS analyzed the data. The first draft of the publication was developed and written by BMA, UB, IMM, and AMS, with corrections and contributions from all authors. The final draft of the manuscript has been authorized for publication by all authors.

Funding

No funding.

Data availability

All materials are within the manuscript; any additional data will be available upon reasonable request from the corresponding author.

Declarations

Ethics approval and consent to participate

The study protocol was approved by Ethical Research and Review Committee (ERRC) of the Federal Medical Center’s (FMC), Bauchi State, Nigeria. Good Clinical Practice (GCP) and the principles outlined in the Declaration of Helsinki were adhered to in the conduct and development of the study’s protocol.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.