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Burden of rifampicin resistance in methicillin-resistant Staphylococcus aureus among apparently healthy students at the University of Jos, Jos, Nigeria
Corresponding author: Ocheme Julius Okojokwu, Department of Microbiology, Faculty of Natural Sciences, University of Jos, Jos, Plateau State, Nigeria. okojokwuoj@gmail.com; okojokwuo@unijos.edu.ng
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Received: ,
Accepted: ,
How to cite this article: Okojokwu OJ, Mawak JD, Lawrence N, Cirfat NA, Shaibu AM, Ndubuisi JC, et al. Burden of rifampicin resistance in methicillin-resistant Staphylococcus aureus among apparently healthy students at the University of Jos, Jos, Nigeria. J Health Sci Res 2023;8:51–56.
Abstract
Objectives
As a broad-spectrum antibiotic, rifampicin is used to treat staphylococcal infections. Due to its chemical makeup, it can easily get into tissues and abscesses, which majority of the other antibiotics (anti-staphylococcal drugs) have trouble doing. To treat these infections, methicillin-resistant Staphylococcus aureus (MRSA) isolates exhibit rapid evolution of rifampicin resistance, necessitating use of costly medicines. This study, therefore, assessed the burden of rifampicin resistance rate among MRSA in Jos, Nigeria.
Material and Methods
A total of 92 samples were collected from students at the University of Jos. S. aureus was isolated and identified by conventional methods. Susceptibility test was conducted to determine MRSA. After that, the MRSA was challenged with 30 µg of rifampicin using the Kirby–Bauer disk diffusion method.
Results
Out of the 92 samples that were isolated, 45 (48.91%) were from female students, while 47 (51.09%) were from male students. 57 (61.96%) samples were positive for S. aureus. Of the 57 (61.96%) S. aureus isolates recovered, 32 (56.14%) were found to be MRSA. These were subjected to rifampicin, and 18 (56.25%) showed resistance. The susceptibility patterns of S. aureus against antibiotics tested showed a susceptibility of 94.74, 77.19, 75.44, 73.68, 71.93, 64.91, 52.63, 43.86, and 31.58% to ofloxacin, clindamycin, chloramphenicol, ciprofloxacin, gentamycin, erythromycin, trimethoprim/sulfamethoxazole, cefoxitin, and tetracycline, respectively.
Conclusion
It was concluded that MRSA were present in the study population, and a substantial number (56.25%) of these were rifampicin resistant.
Keywords
antibiotics
MRSA
resistance
rifampicin
Staphylococcus aureus
INTRODUCTION
Gram-positive bacteria, known as Staphylococci, typically form sporadic clusters of cocci. Although they are mostly located on the skin, skin glands, and mucous membranes of mammals and birds, they are widely distributed in nature and, in some situations, can cause infections. Compared to the other frequent members of the genus (Staphylococcus epidermidis, Staphylococcus saprophyticus, Staphylococcus haemolyticus, and Staphylococcus hominis), Staphylococcus aureus is more detrimental and causes diseases more easily. It is a significant human pathogen responsible for a variety of clinical illnesses. It is the most common cause of osteoarticular, skin and soft tissue, pleuropulmonary, device-related infections, bacteremia, and infective endocarditis. The major cause of mortality and morbidity in hospitals, S. aureus has mostly been a nosocomial pathogen; nevertheless, community-associated Infections with these pathogens are increasing and are now a growing risk.[1] Antimicrobial resistance has grown due to the increase in use of antibiotics and its abusive use in treatment of staphylococcal infections, putting patients at risk for more severe infections.[2]
Methicillin-resistant S. aureus (MRSA) poses a significant public health challenge worldwide because it can cause a wide range of infections with limited treatment options. Rifampicin is one of the antibiotics used to treat MRSA infections; however, its efficacy is reduced when the bacteria become resistant. The burden of rifampicin resistance in MRSA among apparently healthy individuals is poorly reported in Nigeria, where the prevalence of MRSA is high. According to a previous study, the prevalence of MRSA among apparently healthy individuals in Nigeria ranges from 5 to 31.6%.[3] This prevalence is alarming, because MRSA is associated with increased morbidity, mortality, and healthcare costs.[4] Furthermore, the emergence of rifampicin-resistant MRSA strains complicates the treatment of infections, leading to treatment failures, longer hospital stays, and increased healthcare costs.
Though primarily used for treating tuberculosis, Rifampicin is a component of active combination therapy against MRSA and biofilms formed by these organisms.[5] Although MRSA strains are susceptible to rifampicin in vitro, the isolates rapidly develop resistance.[6]
This study was therefore conducted with the aim to determine the burden of rifampicin resistance in MRSA among apparently healthy students at the University of Jos, Nigeria.
MATERIALS AND METHODS
Study area
This study was conducted at the University of Jos, Jos North Local Government Area, Plateau State, North-Central Region of Nigeria. Jos has a population of about 900,000 residents based on the 2006 census.[7] It is about 1238 m or 4,062 feet above sea level. It has a latitude of 9°56’N and longitude of 8°53’E with monthly mean temperature of 21–25°C and 179 km (111 miles) from Abuja, the Nation’s Federal Capital Territory.[8]
Inclusion and exclusion criteria
The inclusion criteria for the study were healthy students of the University of Jos, aged ≥16 years with no history of hospital admission in the past 6 months, no history of use of antibiotics in the past 2 weeks, and who provided a written informed consent. Students who had a history of antibiotics usage within the last 2 weeks, those who had received any form of immunosuppressive therapy in the past 6 months, with a history of chronic diseases, and those who declined to provide informed consent were excluded from the study. These criteria were set to ensure that the study population was representative of apparently healthy individuals without any confounding factors that could affect the study results.
Ethical approval
This study was approved by the Health Research Ethics Committee (HREC) at Plateau State Specialist Hospital, Jos via a notice of approval with reference number PSSH/ADM/ETH.CO/2019/005. Participant information was confidential throughout the study, and all data were collected and analyzed anonymously.
Determination of sample size
The sample size was determined to be 92 using the OpenEpi statistical software (version 3.01). The expected prevalence of rifampicin resistance among MRSA was estimated to be 6.4% based on the previous studies,[9] and the desired level of precision was set at 5%.
Sample collection
The nasal swab samples were collected from the anterior nares of the participants using sterile cotton swabs, and the swabs were transported to the microbiology laboratory of the Department of Microbiology, University of Jos, for processing.
Isolation and identification of Staphylococcus aureus
Within 1–2 h of sample collection, the swab sticks containing different samples were inoculated into mannitol salt agar (MSA) plates and incubated aerobically at 37°C for 24 h. Isolated colonies that seemed to be S. aureus after incubation were allowed to expand on nutrient agar plates before being identified biochemically and under a microscope.[10,11] A pure colony was chosen and gram stained for microscopic examination. Under a light microscope with a magnification of 100X, the form, organization, and gram responses of the isolates were examined.[12] Following established protocols, necessary confirmatory physiological and biochemical tests, such as catalase, coagulase, hemolytic test, and triple sugar iron agar tests, were carried out to determine probable S. aureus.[12]
Antibiotics susceptibility test
Disk agar diffusion test
In accordance with the recommendations of the Clinical and Laboratory Standards Institute (CLSI), the Kirby–Bauer disk diffusion technique was used to ascertain the antibiotic resistance profile of the isolates. Mueller–Hinton agar in 20 mL sterile aliquots was placed on to sterile petri dishes and allowed to set. Mueller–Hinton agar plates were flooded with overnight cultures of the isolates diluted in normal saline to 0.5 McFarland turbidity standard (1.5 × 108 cfu/mL). With sterile forceps, the different antibiotics disks: ofloxacin (5 µg), chloramphenicol (30 µg), clindamycin (2 µg), gentamicin (10 µg), erythromycin (15 µg), penicillin (10 units), tetracycline (30 µg), cefoxitin (30 µg), ciprofloxacin (30 µg), and trimethoprim/sulfamethoxazole (co-trimoxazole) (1.25/23.75 µg) were aseptically placed on the inoculated agar plate and incubated at 37°C for 24 h. After 24 h of incubation, zones of inhibition were measured to the nearest millimeter, and interpreted accordingly as sensitive, intermediate, or resistant based on the CLSI zone diameter interpretative standards.[13] Isolates resistant to cefoxitin were considered to be resistant to methicillin.[13] Isolates resistant to at least two classes of antibiotics were reported as multidrug-resistant (MDR). To determine the multiple antibiotic resistance (MAR) indexes for each isolate, we used a formula that involved two variables, a and b. Variable “a” represents the number of antibiotics the isolate resisted, while variable “b” represents the total number of antibiotics tested to evaluate the susceptibility of the isolate. The formula we used to calculate the MAR index was MAR = a/b, where a is divided by b. This helped us to determine the degree of resistance of each isolate to multiple antibiotics. The higher the MAR index, the more resistant was the isolate to antibiotics.[14]
Rifampicin resistance
MRSA isolates identified by an agar diffusion test were emulsified in normal saline. The turbidity was corrected to 0.5 McFarland standard as per the CLSI guidelines.[13] MRSA was streaked onto the surface of Mueller–Hinton agar with a sterile swab stick in three different directions, with the plate being rotated by about 60 degrees to ensure even dispersion. The antibiotic disk (Rifampicin 30 g) was then aseptically placed on the agar surface after the plates had dried for 10 min. After another 30 min of drying, the samples were incubated at 35°C for 24 h. Following the measurement and recording of the diameter of the zone of inhibition to the nearest millimeter, isolates were categorized as resistant, intermediate, or sensitive as per the CLSI guidelines.[13]
Statistical data analysis
The data collected from this study were entered into a Microsoft Excel spreadsheet and analyzed using SPSS version 23.0 software. The prevalence of rifampicin-resistant MRSA was determined by calculating the proportion of MRSA isolates resistant to rifampicin. Descriptive statistics, such as percentages, were used to summarize the data. The chi-square test determined the association between rifampicin resistance and categorical variable, for example, sex. P < 0.05 was considered statistically significant.
RESULTS
Fifty-seven (62.0%) S. aureus was isolated in this study; 33 (70.2%) were obtained from male students, and 24 (53.3%) were acquired from female students [Table 1]. [Table 2] presents the results obtained from the antibiotic susceptibility test of all 57 confirmed S. aureus. According to the result of susceptibility test using the cefoxitin disk, 32 (56.1%) of the S. aureus isolates were resistant to cefoxitin and therefore considered methicillin-resistant. In comparison, all the isolates were resistant (100%) to penicillin. The resistance to other antibiotics was as follows: 19.3% to chloramphenicol, 22.8% to clindamycin, 28.1% to gentamicin, 31.6% to erythromycin, 49.1% to tetracycline, 21.0% to ciprofloxacin, and 38.6% to trimethoprim/sulfamethoxazole.
| Source of isolates | Number of samples (%) | Positive on mannitol salt agar (%) | Negative on mannitol salt agar (%) |
|---|---|---|---|
| Female | 45 (48.9) | 24 (53.3) | 21 (46.7) |
| Male | 47 (51.1) | 33 (70.2) | 14 (29.8) |
| Total | 92 | 57 (62.0) | 35 (38.0) |
| Class of antibiotics | Antibiotics (concentration) | Sensitive (%) | Intermediate (%) | Resistant (%) |
|---|---|---|---|---|
| Fluoroquinolones | Ofloxacin (5 µg) | 54 (94.7) | 3 (5.3) | 0 (0.0) |
| Fluoroquinolones | Ciprofloxacin (5 µg) | 42 (73.7) | 3 (5.3) | 12 (21.0) |
| Phenicols | Chloramphenicol (30 µg) | 43 (75.4) | 3 (5.3) | 11 (19.3) |
| Lincosamides | Clindamycin (2 µg) | 44 (77.2) | 0 (0.0) | 13 (22.8) |
| Aminoglycosides | Gentamicin (5 µg) | 41 (71.9) | 0 (0.0) | 16 (28.1) |
| Macrolides | Erythromycin (15 µg) | 37 (64.9) | 2 (3.5) | 18 (31.6) |
| β-Lactams | Penicillin (10 units) | 0 (0.0) | 0 (0.0) | 100 (100.0) |
| Tetracyclines | Tetracycline (30 µg) | 18 (31.6) | 11 (19.3) | 28 (49.1) |
| Cephalosporins | Cefoxitin (30 µg) | 25 (43.9) | 0 (0.0) | 32 (56.1) |
| Antifolates/Sulphonamides | Trimethoprim/Sulfamethoxazole (1.25/23.75 µg) | 30 (52.6) | 5 (8.8) | 22 (38.6) |
The MDR pattern observed in the study was the three-antibiotic patterns of cefoxitin, penicillin, and tetracycline, which was seen in 7 out of 27 (25.9%) of the MDR S. aureus isolates. The subsequent most common patterns were the three-antibiotic pattern of penicillin, tetracycline, and trimethoprim/sulfamethoxazole, and the four-antibiotic pattern of chloramphenicol, clindamycin, gentamicin, and tetracycline, each of which was seen in 5 out of 27 (18.5%) of the MDR S. aureus isolates [Table 3]. Several MDR patterns involving five or more antibiotics were seen. The least common was the 7-antibiotic pattern of cefoxitin, chloramphenicol, clindamycin, erythromycin, penicillin, tetracycline, and trimethoprim/sulfamethoxazole, which was seen in 1 out of 27 (3.7%) of the MDR S. aureus isolates. Twenty-seven (27) isolates (47.4%) had an MAR index ≥ 0.3, indicating resistance to at least 30% of the antibiotics tested. The most common MAR index was 0.3, which was observed in 12 isolates (44.44%).
| Number of antibiotics | MDR pattern | No. of antibiotics classes | Number of MDR S. aureus (%) | MAR Index |
|---|---|---|---|---|
| 3 | CFX, PEN, TET | 3 | 7 (25.9) | 0.3 |
| 3 | PEN, TET, TMP/SMX | 3 | 5 (18.5) | 0.3 |
| 4 | CHL, CLI, GEN, TET | 4 | 5 (18.5) | 0.4 |
| 5 | CFX, CLI, GEN, PEN, TMP/SMX | 5 | 3 (11.1) | 0.5 |
| 6 | CFX, CIP, GEN, PEN, TET, TMP/SMX | 6 | 4 (14.8) | 0.6 |
| 7 | CFX, CHL, CIP, ERY, GEN, TET, TMP/SMX | 7 | 1 (3.7) | 0.7 |
| 7 | CFX, CHL, CLI, ERY, PEN, TET, TMP/SMX | 7 | 2 (7.4) | 0.7 |
| Total | 27 (47.4) |
CFX: cefoxitin, CHL: chloramphenicol, CIP: ciprofloxacin, CLI: clindamycin, ERY: erythromycin, GEN: gentamicin, PEN: penicillin, TMP/SMX: trimethoprim/sulfamethoxazole, TET: tetracycline, MDR: Multidrug resistance, MAR: Multiple antibiotic resistance.
[Table 4] provides the proportion of rifampicin resistance among methicillin-sensitive S. aureus (MSSA) and MRSA. The prevalence of rifampicin resistance in MSSA was 8.0%, all occurring among males (2 [13.3%]). There was a statistically significant association (ꭓ2 = 11.458, P = 0.001) between the resistances of S. aureus to methicillin and rifampicin. Of the 32 (56.1%) MRSA samples obtained, 18 (56.3%) were resistant to rifampicin. Five (35.7%) MRSA samples isolated from female subjects were rifampicin-resistant, and the remaining 13 (72.2%) rifampicin-resistant isolates were obtained from male students, resulting in 18 (56.3%) rifampicin-resistant S. aureus. There was no statistically significant association (P > 0.05) between the sex of the students and the resistance of S. aureus to rifampicin and methicillin [Table 5].
| Sex | Cefoxitin | RIF-S (%) | RIF-R (%) | Total | χ2 | P |
|---|---|---|---|---|---|---|
| Overall | MSSA | 23 (92.0) | 2 (8.0) | 25 | 11.458 | 0.001** |
| MRSA | 16 (50.0) | 16 (50.0) | 32 | 0.001*† | ||
| Total | 39 (68.4) | 18 (31.6) | 57 | |||
| Female | MSSA | 10 (100.0) | 0 (0.0) | 10 | 4.511 | 0.034* |
| MRSA | 9 (64.3) | 5 (35.7) | 14 | 0.053*† | ||
| Total | 19 (79.2) | 5 (20.8) | 24 | |||
| Male | MSSA | 13 (86.7) | 2 (13.3) | 15 | 7.823 | 0.005** |
| MRSA | 7 (38.9) | 11 (61.1) | 18 | 0.011*† | ||
| Total | 20 (60.6) | 13 (39.4) | 33 |
| Source of samples | Total number of samples (%) | Resistant to cefoxitin (%) | Resistant to rifampicin (%) |
|---|---|---|---|
| Female | 24 (42) | 14 (58.3) | 5 (35.7) |
| Male | 33 (58) | 18 (54.5) | 13 (72.2) |
| Total | 57 (100) | 32 (56.1) | 18 (56.3) |
| ꭓ2 | 0.081 | 2.215 | |
| P | 0.776 | 0.137 |
ꭓ2 : Chi-square.
DISCUSSION
This study was designed to determine the burden of rifampicin resistance in MRSA among apparently healthy undergraduate students at the University of Jos, Nigeria. Because of this, 62.0% of the study subjects were discovered to have nasal carriage of S. aureus. This implies that the students with nasal colonization could suffer opportunistic and possibly life-threatening infections, including but not limited to surgical-site infection, otitis media, or other infections that increase morbidity as well as mortality.[14]
The relatively high prevalence of S. aureus found in the study was consistent with the results of the study conducted by Nsofor et al.[15] in Rivers State, Nigeria, which found that 62.9% of learners in Elele had a nasal carriage. However, the results contrasted with the 16% found in a study conducted at the Federal University of Birnin Kebbi in Nigeria and published by Aliyu et al.[16] Additionally, S. aureus nasal colonization rates of 33.3% in healthy Amassoma residents in the Niger Delta region of Nigeria and 14.0% among medical students in Lagos, Nigeria, were reported by Onanuga and Temedie[17] and Adesida et al.,[18] respectively.
The prevalence of MRSA obtained in this study contrasts with the findings of the studies carried out by Osinupebi et al.[19] in Abeokuta and Udobi et al.[20] in Zaria, Nigeria, where prevalence rates of 41 and 85.25%, respectively, were recorded. This study showed a lower prevalence than the study by Jean-Marie et al.,[21] who recorded a prevalence of 63.5% on surgical site infection in Kinshasa. However, Barkin et al.[22] reported a prevalence of 53.4%, which was congruent with the report of this study. The difference in sample size, study sites, and geographical variations may be the cause of this variation.
One unexpected finding was the extent to which the S. aureus isolates were resistant to penicillin (100%). It suggests that S. aureus circulating in the student population cannot be treated with penicillin if the organism causes a disease. In addition, the organism was found to be resistant in varying degrees to commonly used antibiotics such as cefoxitin, chloramphenicol, tetracycline, gentamicin, ciprofloxacin, and trimethoprim/sulfamethoxazole (co-trimoxazole). A possible explanation for this might be the indiscriminate use of antibiotics abuse where patients fail to complete the entire course of the prescribed dosage of antibiotics. It could also be due to the problematic practice of self-medication prevalent in the student community.[9,23] These results agree with the findings of other studies, in which all S. aureus isolated were resistant to penicillin.[24]
The results showed that 47.4% of the isolates had a MAR index of 0.3 or higher, indicating a high level of antibiotic resistance. The high levels of antibiotic resistance would make it difficult to treat infections with common antibiotics. The MAR index can also help identify the source of antibiotic resistance, possibly due to the indiscriminate use of antibiotics in clinical settings, agriculture, and animal husbandry. These findings highlight the need for more responsible use of antibiotics to reduce the emergence of antibiotic-resistant bacterial strains. Additionally, there is a need for the development of new antibiotics to combat antibiotic-resistant bacteria.
The higher prevalence of rifampicin resistance in male students than in females in this study was consistent with that of the previous studies that reported higher rates of MRSA and antimicrobial resistance in male individuals.[25,26] The reasons for this gender difference are unclear, but they may be related to differences in behavior, lifestyle, or biological factors.
In contrast to previously reported findings where rifampicin resistance in MRSA varied between 3.26 and 46.4%,[27,28] 50.0% prevalence of rifampicin in MRSA was recorded in this study. The high prevalence of rifampicin resistance among MRSA is most likely a result of the frequent use of the drug to treat tuberculosis in this setting.[9] In developing countries such as Nigeria, many people rely on self-medication, which is also associated with an incomplete dosing regimen of antibiotics and failure to comply with treatment. This renders the antibiotic completely ineffective in treatment. The findings confirm the association between rifampicin and methicillin resistance. This suggests that intrinsic factors in the organism could be responsible for the resistance and not the gender of the study subjects.
CONCLUSION
It was concluded that the prevalence of S. aureus among the students at University of Jos, Nigeria was found to be 62%. In addition, MRSA was present in this study population with a prevalence of 56.1%, and a substantial number (56.3%) of these were rifampicin resistant. This study provides important insights into the burden of rifampicin resistance in MRSA among apparently healthy students at the University of Jos, Jos, Nigeria. The high prevalence of MRSA and rifampicin resistance underscore Nigeria’s urgent need for infection prevention and control measures and antimicrobial stewardship programs. Further studies are needed to identify the risk factors for MRSA and antimicrobial resistance in Nigeria and to develop effective strategies for their prevention and control.
Acknowledgments
None to declare.
Declaration of patients consent
The authors certify that they have obtained all appropriate patient consent.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
REFERENCES
- Rapid detection of mecA-positive and mecA-negative staphylococci by an anti-penicillin binding protein 2a slide latex agglutination test. J Clin Microbiol. 2005;38:2051-4.
- [Google Scholar]
- Absence of mecA gene in methicillin-resistant Staphylococcus aureus isolates. Afr J Infect Dis. 2009;3:49-56.
- [Google Scholar]
- The emergence of community-associated methicillin-resistant Staphylococcus aureus at a London teaching hospital, 2000–2006. Clin Microbiol Infect. 2010;16:1141-7.
- [Google Scholar]
- Antimicrobial susceptibility of methicillin-resistant Staphylococcus aureus isolates from South Africa. SAMJ. 2009;99:170-3.
- [PubMed] [Google Scholar]
- In vitro efficacy of antimicrobial agents against high-inoculum or biofilm-embedded methicillin-resistant Staphylococcus aureus. Int J Antimicrob Agents. 2011;38:46-51.
- [CrossRef] [PubMed] [Google Scholar]
- National Population Commission (NPC) (2006). Federal Republic of Nigeria official gazette. Legal notice on publication of 2006 census final results. Retrieved: 19th November 2021 from population.gov.ng/index.php/plateau-state.
- Abuja Geographic Information System (AGIS) (2010). Geographical location of Jos, Plateau State. www.agis.fcta.gov.ng [Last accessed on 2022 Jun 10].
- Detection of rifampicin resistance rate among methicillin-resistant Staphylococcus aureus (MRSA) isolates in Kano, Nigeria. BJMLS. 2016;1:26-33.
- [Google Scholar]
- Antimicrobial resistant bacteria among healthcare workers in intensive care units at Ain Shams University Hospitals. J Egypt Soc Parasitol. 2010;40:71-83.
- [PubMed] [Google Scholar]
- Epidemiology and risk factors for hospital-acquired methicillin-resistant Staphylococcus aureus among burn patients. J Burn Care Res. 2011;32:429-34.
- [CrossRef] [PubMed] [Google Scholar]
- Microbiology: A laboratory manual (10th edition). New York: Pearson publishers; 2014.
- Performance standards for antimicrobial susceptibility testing (32nd ed). CLSI informational supplement M100. CLSI Wayne, P.A.; 2022.
- Staphylococcus aureus nasal colonization: An update on mechanisms, epidemiology, risk factors, and subsequent infections. Frontiers in Microbiol.. 2018;9:2419.
- [Google Scholar]
- Nasal carriage of multidrug-resistant S. aureus among apparently healthy school children in Elele, Nigeria. Adv Med Biol Sci Res. 2013;3:29-35.
- [Google Scholar]
- Prevalence of methicillin-resistant Staphylococcus aureus isolated from skin and nasal cavity of Microbiology students of Federal University Birnin Kebbi. Savannah J Basic Appl Sci. 2019;1:51-5.
- [Google Scholar]
- Nasal carriage of multi-drug resistant S. aureus in healthy inhabitants of Amassoma in Niger delta region of Nigeria. Afr Health Sci. 2011;11:176-81.
- [PubMed] [PubMed Central] [Google Scholar]
- Associated risk factors and pulsed field gel electrophoresis of nasal isolates of Staphylococcus aureus from medical students in a tertiary hospital in Lagos, Nigeria. Brazilian J Infect Dis. 2007;11:63-69.
- [Google Scholar]
- Prevalence of methicillin-resistant S. aureus in Abeokuta, Nigeria. S Asian J Res Microbiol. 2018;1:1-8.
- [Google Scholar]
- Prevalence and antibiotic resistance pattern of MRSA from an Orthopedic Hospital in Nigeria. Int J Biomed Res. 2013;10:1155.
- [Google Scholar]
- High prevalence of methicillin resistant Staphylococci strains isolated from surgical site infections in Kinshasa. Pan Afr Med. 2014;10:1160.
- [Google Scholar]
- Prevalence of methicillin-resistant S. aureus in upper extremity soft tissue infections at Jackson memorial hospital, Miami-dade County, Florida. Iowa Orthoped J. 2009;29:67-73.
- [Google Scholar]
- Antimicrobial drug use and MRSA. Emerg Infect Dis. 2001;7:1.
- [CrossRef] [PubMed] [PubMed Central] [Google Scholar]
- Difference in epidemiology and antibiotic susceptibility to methicillin-resistant and methicillin-susceptible Staphylococcus aureus isolates. Iranian J Clin Infect Dis. 2009;4:219-23.
- [Google Scholar]
- Prevalence of Staphylococcus aureus nasal colonization in the United States, 2001–2002. J Infect Dis. 2006;193:172-9.
- [CrossRef] [PubMed] [Google Scholar]
- Invasive methicillin-resistant Staphylococcus aureus infections in the United States. JAMA. 2007;298:1763-71.
- [CrossRef] [PubMed] [Google Scholar]
- Epidemiological and molecular aspects of rifampicin-resistant Staphylococcus aureus isolated from wounds, blood, and respiratory samples. J Antimicrob Chemother. 2011;10:1093-7.
- [Google Scholar]
- Genetic basis of rifampicin resistance in methicillin-resistant Staphylococcus aureus suggests clonal expression in hospitals in Cape Town, South Africa. Biomed Centr Microbiol. 2012;12:46.
- [Google Scholar]
