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*Corresponding Author: Seyi Samson Enitan, 2Department of Medical Laboratory Science, Babcock University Ilishan-Remo, Ogun state 121103, Nigeria.
Citation: Terry Alli OA, Hannah B. Sonde, Seyi S. Enitan, Michael O. Dada and Effiong J. Effiong, (2024), Prevalence of Methicillin Resistant Staphylococcus aureus strains among Medical Undergraduate Students in South-West Nigeria, J. Biomedical Research and Clinical Reviews. 9(3); DOI:10.31579/2692-9406/186
Copyright: © 2024, Adamu Tizazu Yadeta, this is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Received: 18 April 2024 | Accepted: 25 April 2024 | Published: 30 April 2024
Keywords: methicillin; nasal carriage; prevalence; resistance; staphylococcus aureus
Background: Staphylococcus aureus (S. aureus) infections pose significant challenges in healthcare settings due to the emergence of methicillin-resistant strains (MRSA). This study aimed to evaluate the prevalence of nasal carriage of S. aureus (including MRSA) and antibiotic sensitivity pattern, among medical undergraduate students at Babcock University, Nigeria, and assess antibiotic resistance patterns. Methods: Nasal swabs were obtained from 200 consenting participants, cultured on enriched and selective media (blood agar, mannitol salt agar, and Baird-Parker agar) and incubated at 37°C for 18-24 hours. Isolates were identified using standard biochemical tests, and antibiotic sensitivity testing was performed. MRSA detection utilized the Cefoxitin disk diffusion test and a latex agglutination kit. Results: Among participants, 34% harbored S. aureus in their nasal passages, with MRSA carriage observed in 61.8%. Notably, medicine and surgery students exhibited the highest MRSA carriage (30%), particularly fifth-year students (66.6%). Antibiotic resistance analysis revealed vancomycin and cefoxitin resistance rates of 47.1% and 61.8%, respectively, while clindamycin and erythromycin showed the highest sensitivity (70.6%). Conclusion: This study underscores a concerning prevalence of MRSA among medical undergraduate students, highlighting the urgent need for effective strategies to mitigate its spread. Implementation of stringent antibiotic prescription regulations and MRSA control measures is imperative in addressing this growing public health threat and combating antibiotic resistance effectively.
The human nose acts as a habitat and a means of transmission for various disease-causing microorganisms. Staphylococcus aureus, a pathogenic bacterium, is known to be carried in the nasal passages of both individuals in hospitals and community settings, especially among food handlers [1,2]. S. aureus can also be found in other body sites like the skin, rectum, throat, and more, but it is commonly present in the anterior nares of 50-70% of healthy individuals.
The Staphylococcus genus belongs to the Micrococcaceae family, which includes a wide range of bacteria capable of causing various diseases such as impetigo, boils, wound infections, toxic food poisoning, and more [3]. S. aureus is a Gram-positive bacterium that produces several virulence factors, making it harmful to both healthy individuals and those with weakened immune systems [3,4]. Staphylococci are normally harmless commensals that colonize around one-third of the human population, causing no harm unless they enter the body through cuts or injuries. However, the majority of recent clinical isolates of staphylococci have become resistant to penicillin, and multiple drug resistance is now common, particularly among MRSA strains. MRSA strains are resistant to common medications used to treat staphylococcal infections, and some have even developed resistance to the last-resort antibiotic, vancomycin. This has led to increased concern over MRSA's involvement in both community-acquired and hospital-acquired infections. Efforts are underway to find new antibiotics and vaccines effective against MRSA strains [4-8].
The presence of S. aureus in the nasal passages plays a significant role in the development of infections among patients in the intensive care unit (ICU) [9], those undergoing dialysis [9,1], and individuals after surgery [2,12]. To cause infection and colonize the human nares, S. aureus must effectively interact with human nasal epithelial cells and evade the host's immune system. However, various circumstances can prevent S. aureus colonization, while specific host characteristics and environmental factors can promote it. Nasal colonization by S. aureus can lead to the emergence of opportunistic and potentially fatal infections in both non-surgical and surgical patients, particularly at surgical sites, giving rise to surgical site infections and other types of infections. This, in turn, results in increased healthcare costs, disease burden, and even fatalities [13].
Apart from using culture media like Baird-Parker agar to isolate MRSA, there are various identification kits available for the definite diagnosis of MRSA. Some of these kits include the Electronic RapIDTM Staph Plus Diagnostic Code Compendium Panel System (ERIC®), Dryspot Staphytect Plus (DR0100), and Penicillin Binding Protein (PBP2') Plus (DR0900). These kits can identify particular proteins and enzymes specific to MRSA, and they are generally more cost-effective compared to Polymerase Chain Reaction (PCR) methods.
Staphylococcal infections, especially MRSA, have been primarily associated with hospital-acquired infections, presenting a significant concern due to its resistance to antibiotics. Consequently, the role of medical undergraduates in transmitting nosocomial infections, such as S. aureus infections, to patients is of utmost importance. These healthcare workers can serve as a source of infection and reservoir for transmitting the pathogenic organism to hospitalized patients. Nasal colonization by the pathogen can lead to infections and reinfections among the patients in the hospital setting. Additionally, MRSA nasal colonization among healthcare workers poses a substantial public health threat to in-patients as these workers can potentially transmit the multidrug-resistant bacteria strain within the hospital environment [14,15]. Notably, there is currently no available data on the nasal carriage of Staphylococcus aureus, particularly the MRSA strain, among undergraduate students at Babcock University. Due to this lack of data, conducting this research is essential. The primary objective of this study is to evaluate the nasal carriage of S. aureus and the prevalence of antibiotic resistance among medical undergraduate students at Babcock University, Ilishan-Remo, Ogun state, Nigeria.
Study Design
This cross-sectional study was carried out among undergraduate medical students at Babcock University, Ilishan-Remo, in the Ikenne Local Government Area of Ogun State, Nigeria. Babcock University is a prominent Seventh-day Adventist institution of higher education located in the South-Western region of Nigeria, with coordinates 70 29'00''N, 20 55'00''E. The university consists of nine schools and has a total student population of approximately twelve thousand (12,000), offering various academic and professional courses at both the undergraduate and postgraduate levels. The selection of undergraduate medical students as study participants was based on their regular and continuous interaction with patients who could potentially carry S. aureus, making them susceptible to staphylococcal infections. The geographical location was chosen due to its close proximity to the laboratory, ensuring minimal loss of viable organisms of interest and easy accessibility for study subjects to participate.
Duration of Study
The research work lasted for 2 months (May to June, 2022).
The sample size for this study was calculated using the formula as described by Sharma et al [16].
N= (z1-a/2)2* (p) (q) d2
A simple random sampling technique was used to select two hundred (200) subjects into the study and this comprised of: 68 Medical Laboratory Science, 70 Medicine and Surgery students and 62 Nursing Sciences students.
Eligibility of Subjects
Inclusion Criteria
Consenting medical undergraduate students of Babcock University were recruited for the study.
Exclusion Criteria
Non-medical undergraduate students were excluded from the study.
Informed Consent:
Before collecting samples, each participant was provided with a comprehensive explanation of the study's purpose and methodology. They were then given a consent form to voluntarily complete and sign, indicating their willingness to take part in the research. The participants were assured of the confidentiality of their study results.
Data Collection:
Upon obtaining ethical approval from BUHREC and informed consent from willing participants, a well-structured standardized questionnaire was used to collect data from the study subjects before specimen collection. Each questionnaire contained a unique participant identification number and other relevant personal information to distinguish the three departments from one another. The data collection process spanned approximately 14 days, during which the questionnaires were distributed and collected, study participants were selected, and samples were obtained from each department.
Sample Collection and Transportation:
Sterile swab sticks were used to collect nasal samples from the nostrils of study participants. These samples were promptly transported to the laboratory for analysis. In the laboratory, the samples were appropriately sorted and labeled. Media were prepared and stored in the refrigerator following the manufacturer's instructions. Before culturing, the agar plates were briefly dried in a hot air oven to eliminate surface moisture.
Culture and Identification:
Nasal swabs were streaked on mannitol salt agar, blood agar, and Baird-Parker agar, followed by incubation at 37°C for 24 hours. S. aureus identification relied on colonial characteristics and standard biochemical tests including catalase and tube coagulase tests [3].
Antibiotic Sensitivity Testing:
Two methods were used: Kirby Bauer disc diffusion and agar dilution.
Kirby Bauer Method: Pure colonies were emulsified, inoculated onto Mueller Hinton agar, and incubated with antibiotic discs (Clindamycin, Gentamycin, Ciprofloxacin, Erythromycin, Cefoxitin). Zones of inhibition were measured and interpreted.
Agar Dilution Method: Mueller Hinton Agar plates with vancomycin were prepared. MRSA isolates were inoculated, and MIC was determined after incubation [18,19,20,21].
MRSA Detection:
Latex agglutination test using a penicillin binding protein (pbp2') test kit supplied by Oxoid, UK was utilized [22]. S. aureus colonies were suspended, heated, and centrifuged. Test latex was added, and agglutination was observed for MRSA detection.
Interpretation:
Antibiotic susceptibility was categorized as resistant, intermediate, or susceptible based on CLSI guidelines. MRSA detection was confirmed by agglutination within three minutes.
Data Analysis
Microsoft Excel was used to enter the raw data. Results were presented using frequency distribution tables and charts. Statistical Package for Social Sciences (SPSS) version 26.0 was used for data analysis. Chi-square test was used to determine association between prevalence of nasal carriage of Staphylococcus aureus and socio-demographic variables. P-values less than or equal to 0.05 were considered statistically significant at a 95% confidence interval.
This present study assessed the nasal prevalence of S. aureus and its antibiotic susceptibility amongst medical undergraduate students at a private university in Ogun state. S. aureus colonisation according to the socio-demographic characteristics of the study participants is presented in Table 1. A total of 200 students (81 males and 119 females) between the ages of 16 and 25 years were recruited for the study. 68 (34%) S. aureus isolates were recovered from the 200 nasal swabs examined. The female participants (57.4%) were more colonised than their male counterparts (42.6%); however, the difference was not statistically significant (Chi square = 17.42; p = 0.872). Based on age, S. aureus colonisation was higher among those aged 21-25 years (54.4%) than among those aged16-20 years (45.6%). However, the difference was not statistically significant (Chi square= 24.28; p = 0.432). Nasal colonisation of S. aureus was found to be significantly higher among students of Medicine (38.2%), as well as Nursing (38.2%), but lower among students of the Medical Laboratory Science Department (23.5%) (Chi-squared=10.47; p=0.012). Based on their year of study, nasal colonisation of S aureus was found to be statistically significant (Chi squared = 12.52; p = 0.005) higher among students in the fifth year of study.
The prevalence of MSSA and MRSA according to the socio-demographic characteristics of the study participants is presented in Table 2. From the 68 isolates recovered from the nasal swabs examined, MSSA had a prevalence of 38.2% (26 out of 68), while MRSA had a prevalence of 61.8% (42 out of 68). The prevalence of MRSA is not significantly associated with the gender and age of the study participants (X2 = 2.01; 4.02; and 14.07; p>0.05). The prevalence of MRSA was statistically significant (X2= 10.47; p=0.012) higher among students of Medicine and Surgery (50%), followed by students of Nursing (31%) and then Medical Laboratory Science (19%). Based on their year of study, MRSA prevalence was significantly higher among students in the fifth year of study (66.6%) (X2=34.28; p = 0.000).
Regarding nose hygiene among the participants, a correlation was found between their beliefs about nose hygiene and their actual nose hygiene practices across the three departments. The questionnaire results indicated that the belief in nose hygiene was lowest among medicine students (50 or 71.4%), followed by medical laboratory science students (54 or 79.4%), and highest among nursing science students (58 or 93.5%) (X2= 6.81; p=0.000). However, the practice of nose hygiene was most commonly observed among medical laboratory science students (60 or 88.2%), followed by medicine students (54 or 77.1%), and least among nursing science students (46 or 74.2%) (X2 = 14.20; p=0.017), as shown in Table 3.
In terms of the frequent use of antibiotics, medicine students had the highest occurrence with 35 (45.7%) reporting frequent use, followed by nursing science students with 25 (40.3%), and medical laboratory science students with 11 (16.2%). There was a significant association between the frequency of antibiotic use and the departments (X2 = 10.02; p = 0.000) as seen in Table 4. As for wound infection, it was not recorded among medical laboratory science students (0 or 0%), and the least occurrence was among nursing science students with 8 (12.9%), while medicine students had the highest occurrence with 12 (17.1%) among the three departments. There was no statistical relationship observed among the study departments concerning wound infection.
Where χ2 = Chi-square; * = Significant at p < 0>
Table 1: S. aureus colonisation according to the socio-demographic characteristics of the study participants
Keys: MSSA = Methicillin Sensitive Staphylococcus aureus, MRSA = Methicillin-resistant Staphylococcus aureus. * p-value <0>
Table 2: The prevalence of MSSA and MRSA was determined according to the socio-demographic characteristics of the study participants
Table 3: Nose hygiene practices among study participants
Where χ2 = Chi-square; * = Significant at p < 0>
The results of the antibiotic susceptibility test for S. aureus isolates, categorized by the participants' department, are presented in Table 5 and Figure 1. Among all the antibiotics used, there were no intermediate susceptibility results recorded; isolates were either classified as resistant or sensitive. A range of susceptibility levels to antibiotics was observed, with the highest resistance seen for cefoxitin (61.8%) and vancomycin (47.1%). On the other hand, the highest degree of antibiotic sensitivity was found for clindamycin and erythromycin, both showing 70.6% sensitivity (X2= 5.47; p<0 xss=removed xss=removed xss=removed xss=removed>
Table 4: Frequent use of antibiotics and the presence of wound infection were found among study participants
Where χ2 = Chi-square; * = Significant at p < 0>
Table 5: Data analysis of the antibiotic susceptibility test of S. aureus isolates according to the participants' department.
Figure 1: Bar chart showing the overall antibiotic susceptibility pattern of S. aureus nasal isolates recovered from the study participants.
Approximately 20-30% of healthy individuals have S. aureus present in their nasal passages as a common commensal, with many being carriers unknowingly [23]. Nasal carriage of S. aureus, especially the methicillin-resistant strain (MRSA), has been mainly associated with healthcare workers and individuals within hospital environments [5-8,24-26]. MRSA has been identified in various geographical locations worldwide,27 including Nigeria, where studies have shown an overall increase in its prevalence.9 In this study, the focus was on assessing the nasal carriage of S. aureus and MRSA among medical undergraduate students at Babcock University, Ilishan-Remo, Ogun State.
Among the 200 nasal swabs examined, the carriage rate of S. aureus among the study participants was found to be 34%. This rate is lower than the 63.1% reported by Garoy et al [5].in Asmara, Eritrea, and the 91.2% reported by Elimian et al [17] among outpatients in selected health facilities in Benin City, Nigeria. It was however lower than the 30.5% reported by Chai et al [5]. among animal handlers in Peninsular Malaysia. These variations could be attributed to differences in geographical locations, socio-demographics, and hygiene levels among the study participants.
Additionally, in this study, the prevalence of MRSA was found to be 61.8%. This percentage is higher compared to the 46.9% and 1.2% reported by Adeiza et al [28].and Chai et al [6]. in a study conducted among patients and staff of state-owned hospitals in North-West Nigeria and animal handlers in Malaysia, respectively. However, it is lower than the 72.0% reported by Garoy et al [5]. among patients in Asmara, Eritrea.
In this current study, when considering gender, the carriage rate was higher among females (57.4%) compared to their male counterparts (42.6%). This is consistent with the work of Othman et al [26]. who reported a higher prevalence in females than in males (OR = 1.96; χ2 = 10.75; p=0.001). However, it contradicts the work of Ibrahim and Sule [17], who reported a higher carriage rate among males (11.2%) than females (5.6%).
Regarding age, the carriage of S. aureus and MRSA was highest among individuals in the age group of 21-25 years, with rates of 54.4% and 57.1%, respectively. This finding is consistent with the study by Ibrahim and Sule [17] who also reported the highest carriage rate among individuals aged 21-30 years (8.4%). It further aligns with the work of Garoy et al [5].who found a higher carriage of S. aureus in patients under the age of 18 compared to those over the age of 61 years.
Furthermore, concerning the departments assessed in this study, the prevalence of MRSA was highest among Medicine and Surgery students, with a prevalence of 30%, followed by Nursing Science students (21%), and Medical Laboratory Science students (11.8%), which had the lowest prevalence. A similar study by Adeiza et al.28 reported the highest MRSA prevalence among physicians in a health center in Sokoto, North-West of Nigeria. According to Albrich et al [29].the high prevalence rate of MRSA among healthcare workers can be attributed to their exposure to the hospital environment without adequate preventive measures and hospital hygiene. From the questionnaire, it was observed that Medical students had the lowest practice of nose hygiene compared to the other two groups. A similar study by Rongpharpi et al [30].emphasized major risk factors contributing to the spread of S. aureus in a hospital community, including poor sanitary and hygienic measures among healthcare workers.
The S. aureus isolates recovered in this study exhibited varying susceptibility patterns to the different antibiotics tested. Clindamycin and erythromycin were found to be the most effective, with the highest overall susceptible rate of 70.6
The high prevalence of Methicillin Resistant Staphylococcus aureus (MRSA) among medical undergraduate students underscores the urgent need for policy regulations on antibiotic prescription and usage. Implementing stringent guidelines for MRSA detection and control measures is crucial to curb the spread of resistant strains and combat antibiotic resistance effectively. Key measures include regular surveillance for MRSA, appropriate use of antibiotics, infection control protocols, and promoting antimicrobial stewardship programs. These actions are essential to safeguard public health and preserve the effectiveness of antibiotics for future generations.
Competing Interests
The authors declare no competing interests.
Authors’ Contributions:
Study concept and design: E.O.A., A.E.A.;
Acquisition of data: E.O.A., A.E.A., S.S.E.;
Analysis and interpretation of data: E.O.A., A.E.A.;
Drafting of the manuscript: E.O.A., A.E.A., S.S.E.;
Critical revision of the manuscript for important intellectual content: E.O.A., A.E.A., S.S.E.;
Statistical analysis: E.O.A., A.E.A.;
Study supervision: A.E.A.
Data Availability
Data supporting the findings of this study are available on reasonable request from the corresponding author [SSE], exclusively for non-commercial use and under a Data Usage Agreement.
Consent
Authors declared that a written informed consent was obtained from each study participant before the commencement of the research.
Conflict of Interest
There is no conflict of interest reported by the authors.
Funding
This study received no external funding.
Ethical Approval
Ethical approval (with the ethical registered number: BUHREC 342/22) was obtained from the Babcock University Health Research Ethics Committee (BUHREC) before the commencement of the research.
Acknowledgments
We are incredibly appreciative of the cooperation received from all the study participants.
Competing Interests
The authors declare that they have no competing interests.
Disclaimer:
The authors wish to declare that this manuscript has been previously submitted as a preprint for the purpose of peer review and feedback only on Qeios platform. Manuscript available at: https://www.qeios.com/read/DMF88Z
Disclaimer:
The authors wish to declare that this manuscript has been previously submitted as a preprint for the purpose of peer review and feedback only on Qeios platform. Manuscript available at: https://www.qeios.com/read/DMF88Z
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Dear Dr. Jessica Magne, Editorial Coordinator 0f Clinical Cardiology and Cardiovascular Interventions, I hope this message finds you well. I want to express my utmost gratitude for your excellent work and for the dedication and speed in the publication process of my article titled "Navigating Innovation: Qualitative Insights on Using Technology for Health Education in Acute Coronary Syndrome Patients." I am very satisfied with the peer review process, the support from the editorial office, and the quality of the journal. I hope we can maintain our scientific relationship in the long term.
Dear Monica Gissare, - Editorial Coordinator of Nutrition and Food Processing. ¨My testimony with you is truly professional, with a positive response regarding the follow-up of the article and its review, you took into account my qualities and the importance of the topic¨.
Dear Dr. Jessica Magne, Editorial Coordinator 0f Clinical Cardiology and Cardiovascular Interventions, The review process for the article “The Handling of Anti-aggregants and Anticoagulants in the Oncologic Heart Patient Submitted to Surgery” was extremely rigorous and detailed. From the initial submission to the final acceptance, the editorial team at the “Journal of Clinical Cardiology and Cardiovascular Interventions” demonstrated a high level of professionalism and dedication. The reviewers provided constructive and detailed feedback, which was essential for improving the quality of our work. Communication was always clear and efficient, ensuring that all our questions were promptly addressed. The quality of the “Journal of Clinical Cardiology and Cardiovascular Interventions” is undeniable. It is a peer-reviewed, open-access publication dedicated exclusively to disseminating high-quality research in the field of clinical cardiology and cardiovascular interventions. The journal's impact factor is currently under evaluation, and it is indexed in reputable databases, which further reinforces its credibility and relevance in the scientific field. I highly recommend this journal to researchers looking for a reputable platform to publish their studies.
Dear Editorial Coordinator of the Journal of Nutrition and Food Processing! "I would like to thank the Journal of Nutrition and Food Processing for including and publishing my article. The peer review process was very quick, movement and precise. The Editorial Board has done an extremely conscientious job with much help, valuable comments and advices. I find the journal very valuable from a professional point of view, thank you very much for allowing me to be part of it and I would like to participate in the future!”
Dealing with The Journal of Neurology and Neurological Surgery was very smooth and comprehensive. The office staff took time to address my needs and the response from editors and the office was prompt and fair. I certainly hope to publish with this journal again.Their professionalism is apparent and more than satisfactory. Susan Weiner
My Testimonial Covering as fellowing: Lin-Show Chin. The peer reviewers process is quick and effective, the supports from editorial office is excellent, the quality of journal is high. I would like to collabroate with Internatioanl journal of Clinical Case Reports and Reviews.
My experience publishing in Psychology and Mental Health Care was exceptional. The peer review process was rigorous and constructive, with reviewers providing valuable insights that helped enhance the quality of our work. The editorial team was highly supportive and responsive, making the submission process smooth and efficient. The journal's commitment to high standards and academic rigor makes it a respected platform for quality research. I am grateful for the opportunity to publish in such a reputable journal.
My experience publishing in International Journal of Clinical Case Reports and Reviews was exceptional. I Come forth to Provide a Testimonial Covering the Peer Review Process and the editorial office for the Professional and Impartial Evaluation of the Manuscript.
