|Year : 2019 | Volume
| Issue : 4 | Page : 226-230
Prevalence and factors associated with methicillin-resistant Staphylococcus aureus colonization among clinical medical students
Nora Naser Albusayes1, Khalifa Binkhamis2, Ruba Mohammed Alselaimy1, Monirah Misfer Alsalouli1, Raghad Abdulaziz Alnafisah1, Lina Abdullah Albawardi1, Ali M Somily2, Abiola Senok3
1 College of Medicine King Saud University, King Saud University Medical City, Riyadh, Saudi Arabia
2 Department of Pathology and Laboratory Medicine, College of Medicine King Saud University, King Saud University Medical City, Riyadh, Saudi Arabia
3 Department of Basic Medical Sciences, College of Medicine, Mohammed Bin Rashid University of Medicine and Health Sciences, Dubai, UAE
|Date of Web Publication||4-Oct-2019|
Nora Naser Albusayes
College of Medicine King Saud University, Riyadh
Source of Support: None, Conflict of Interest: None
Background: This study was carried out to assess the prevalence and determinants of methicillin-resistant Staphylococcus aureus(MRSA) colonization among clinical clerkship medical students in Saudi Arabia. Methods: A cross-sectional study was performed at King Saud University Medical City (KSUMC) in Riyadh, Saudi Arabia. Nasal samples were obtained from 360 clinical clerkship medical students (3rd–5th years). Questionnaires were filled. MRSA identification was done using the standard laboratory procedures. Data were analyzed using SPSS Pc + 21.0 software. Results: Of 360 samples, 100 (27.7%) were positive for S. aureus and 12 (3.3%) were MRSA positive. The following variables and the outcome (MRSA+/MRSA−) showed statistically significant association; previous hospital admissions, immunocompromised status, chronic disease, and female gender. We found that our MRSA colonization prevalence rate of 3.3% predominately in female gender. Third-year medical students have the highest MRSA colonization of 4.8%, then 4th year 2.8%, and 5th year 1.2%. 17.6% of students with history of hospital admission where found to be MRSA positive, 10% of bronchial asthma sufferers, and 37.5% of immunocompromised students either due to medication or cancer were MRSA positive. Conclusion: MRSA nasal carriage among clinical medical students in KSUMC was found to be 3.3%. We recommend teaching standard practices of infection control protocols and additional precautions.
Keywords: Medical students, methicillin-resistant Staphylococcus aureus, nasal carriage
|How to cite this article:|
Albusayes NN, Binkhamis K, Alselaimy RM, Alsalouli MM, Alnafisah RA, Albawardi LA, Somily AM, Senok A. Prevalence and factors associated with methicillin-resistant Staphylococcus aureus colonization among clinical medical students. J Nat Sci Med 2019;2:226-30
|How to cite this URL:|
Albusayes NN, Binkhamis K, Alselaimy RM, Alsalouli MM, Alnafisah RA, Albawardi LA, Somily AM, Senok A. Prevalence and factors associated with methicillin-resistant Staphylococcus aureus colonization among clinical medical students. J Nat Sci Med [serial online] 2019 [cited 2022 Aug 12];2:226-30. Available from: https://www.jnsmonline.org/text.asp?2019/2/4/226/260445
| Introduction|| |
Methicillin-resistant Staphylococcus aureuss(MRSA) is associated with various forms of infections, ranging from mild skin infections to potentially fatal invasive infections such as sepsis. Healthcare workers and medical students as a part of the healthcare team have a higher risk for asymptomatic MRSA carriage and could be the source of transmitting these organisms to patients. High prevalence of MRSA nasal colonization has been reported among medical students in Oman (20.8%) and Jeddah (6.7%)., On the other hand, MRSA nasal colonization prevalence around the world is profoundly less than that in the Middle East, with the mean of 2.06%.,,,,, MRSA carriage has many associated factors; the first and foremost is centered around being exposed to hospital environment either as a healthcare worker (i.e., medical student) or as a patient, due to the increasing length of hospitalization. Another factor of the spread of MRSA is the contact between healthcare personnel and patients. Other reported risk factors include sharing of personal items, male gender, and participation in contact sports.,,,, Individuals who have had previous MRSA carriage possess a significantly higher risk of recurrence in the future after being decolonized. Disruption of skin barrier, e.g., open wounds, presence of underlying comorbidities, immunocompromised status, and recent antibiotic use are factors which increased risk of MRSA colonization and infection.,,, Hand hygiene protocols and the adherence of healthcare worker to such protocols reduce MRSA nasal colonization and limit its spread. Pets and farm animals could also play a part in transmission of MRSA to humans., Determining the MRSA prevalence among clinical clerkship students and identification of the associated risk factors as well as knowledge of preventive measures are important to limit the spread of MRSA in our setting. This study aimed at determining the prevalence and factors contributing to MRSA colonization among clinical medical students in King Saud University Medical City (KSUMC), Riyadh, Saudi Arabia.
| Methods|| |
This is a quantitative, analytical, observational cross-sectional study. The study was conducted at KSUMC, Riyadh, Saudi Arabia, from October 2017 to April 2018. All King Saud University medical students in the clinical clerkship phase (3rd–5th years) were eligible to participate. Three hundred and sixty 3rd–5th-year medical students (clinical clerkship phase) were enrolled in this study using convenience sampling technique. MRSA screening was carried out by the collection of nasal swabs from both anterior nares using a nonpremoistened sterile swab with transport media. Investigators rotated swabs five times in each nostril. All participants completed a questionnaire designed to collect demographic data and information related to MRSA risk factors [Table 1]. Hygiene knowledge score as a risk factor was calculated using the WHO evaluation tool (hand hygiene knowledge questionnaire). Ethical approval for the study was given by institutional review board at KSUMC and informed consent was obtained from all participants.
|Table 1: Association of categorical study variables with methicillins-resistant Staphylococcus aureus colonization|
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All samples received in KSUMC Microbiology Laboratory were inoculated on both mannitol salt agar (Saudi Prepared Media, Riyadh, Saudi Arabia) and 5% sheep blood agar plates (Saudi Prepared Media, Saudi Arabia). Plates were inoculated for 24–48 h and rapid biochemical tests for catalase and coagulase performed for presumptive identification of S. aureus. Definitive identification of methicillin-sensitive S. aureus and MRSA was done using the microscan (panel Pos Breakpoint Combo-28, Beckman Coulter, California, USA) and the GeneXpert (Xpert SA Nasal Complete kit, Cepheid, California, USA). Data were analyzed using IBM Corp, IBM SPSS statistics software for windows, version +21.0, Armonk, NY, USA. Comparison of mean values of quantitative study variables (age, body mass index [BMI], and hygiene knowledge) in relation to MRSA colonization was carried out using independent t-test. Association of categorical study variables with MRSA colonization using Chi-square and odds ratio (OR). A P ≤ 0.05 and 95% confidence intervals (CIs) were used to report statistical significance and precision of results. This study (research project number: CMED 305-F4-2017-18) was reviewed and approved, for methodological and ethical issues by the review committee for CMED 305 course research projects of the family and community medicine department.
| Results|| |
A total number of 360 nasal swabs were collected from medical students in their clinical years (3rd, 4th, and 5th) in KSUMC. Swabs were collected from 166 (46.1%) male students and 194 (53.9%) female students. Of the total 360 participants, 168 (46.7%), 107 (29.7%), and 85 (23.6%) were in their 3rd, 4th, and 5th year, respectively [Table 2]. One hundred (27.7%) of the collected samples were positive for S. aureus and 12 (3.3%) of those were MRSA positive.MRSA was found in 8 (4.8%) of 3rd-year, 3 (2.8%) of 4th-year, and 1 (1.2%) of 5th-year students. The quantitative variables, i.e., age, BMI, and hygiene knowledge score, appear to be statistically significant for the age (P < 0.036) and statistically insignificant for the BMI and hygiene knowledge score [Table 3]. The association between the following variables and the outcome (MRSA ± MRSA−) shows statistically significant association: gender with female predominance (OR = 4.457, 95% CI = [0.962, 20.637]), hospital admission (OR = 7.95, 95% CI = [1.938, 32.632]), immunocompromised state (OR = 22.867, 95% CI = [4.724, 110.680]), chronic disease (OR = 4.3, 95% CI = [1.24, 15.10]) [Table 1]. While variables as antibiotics use within the last month, recurrent skin disease/infection shows an association without statistical significance. Some variables such as contact with MRSA colonized/infected patient, previously diagnosed with MRSA colonization/infection, participation in skin-to-skin contact sports/gym, sharing personal items, close association with farm animals/pets have showed neither association nor significance [Table 1]. BMI classifications (underweight, healthy normal, overweight, and obese) showed some variability, as low and high classes (underweight, obese) showed association with MRSA colonization, whereas moderately high and normal classes (overweight, healthy) elicited no association [Table 1]. According to hand hygiene knowledge grades (high >18/27, medium 18–9/27, and low <9/27) depending on the score of the quiz, the ones who got high scores were found to be more likely to get MRSA colonization with significant association; on the other hand, participants who got medium and low scores had no association nor significance [Table 1].
|Table 2: Sociodemographic and factors associated with methicillin-resistant Staphylococcus aureus colonization|
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|Table 3: Comparison of mean values of quantitative study variables in relation to methicillin-resistant Staphylococcus aureus colonization|
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| Discussion|| |
There is variability in the prevalence rate of MRSA nasal colonization according to the geographic area and the type of population and type of study. We found that our study population has nasal colonization prevalence rate of 3.3%, which is comparative to the international prevalence rate reported in published articles which ranges from 0.81% to 4.5%.,,,,, However, the prevalence rate of MRSA colonization found in the present study is lower compared to reported data from Oman (20.8%) and Jeddah, Saudi Arabia (6.7%)., This variability in the rate of MRSA colonization might be due to the differences in study design.
Kirk A. Campbell (2015) demonstrated a male preponderance in MRSA carriage of up to two-fold compared to females. In contrast, our study revealed a female predominance (female 5.2% vs. male 1.2%). This higher rate of MRSA colonization in female students as compared to male is hard to explain, and we suggest larger multicenter studies to address this. The 3rd-year students were found to have the highest carriage with 4.8% and then 4th-year students (2.8%), and those in the 5th-year had the lowest rate (1.2%). We believe that this might be related to the variability in the number of students screened for MRSA colonization between the three academic years.
Comparing associated factors to the literature, we found that hospital admission within the past 6 months was observed in 3 (17.6%) MRSA-positive subjects. This rate is close to that of a previous study carried out in Washington University School of Medicine, where 8 (18.2%) of their MRSA-positive participants had more than five admissions in the previous 12 months. In the literature, MRSA carriage has been found to be associated with some chronic diseases as inflammatory bowel diseases, chronic renal insufficiency, and asthma.,, Asthma (10%) was the only chronic disease associated with MRSA in this study population which might be related to the age group of the participants. Chemotherapy in the past 30 days as an attributable factor to lowering immunity has been found to have an association with MRSA nasal carriage (14, 31.8%). Three MRSA-positive individuals were either on immunosuppressive medication due to the use of azathioprine (Imuran) drug, glucocorticosteroid medication for asthma and the one patient has papillary thyroid cancer; this could explain their MRSA colonization.
Eczema and acne as skin diseases showed an association with MRSA which is similar to the findings in previous studies. In Schaefer et al.'s study, antibiotic use was found to be associated with MRSA nasal colonization (18, 31.57%); this result is much higher than our finding which is 3 (6.5%).
Medical students would be a key target group to introduce awareness of hospital-acquired infections in educational sessions, and to teach them about standard practices on infection control protocols and additional precautions at the beginning of their clinical years. This would be helpful to both; comprehend the magnitude of the problem and to the limit spread through students. This study had some limitations: extranasal colonization sites (axillary, groin) were neither swabbed nor cultured, which could have affected our carriage rate. In addition, the collected samples were only in KSUMC, so generalizing the prevalence to Saudi Arabia would not be completely accurate. Furthermore, the study could have enrolled intern students as well, since they are more exposed to clinical work than medical students. The length of the questions listed in the hand hygiene knowledge section of our questionnaire may have influenced the dedication of the subjects owing to the false results showing increased chances of colonization in high scored individuals. Exposure to the hospital environment is considered an associated factor.
| Conclusion|| |
MRSA nasal carriage among clinical medical students in KSUMC was found to be 3.3%. The study revealed an association between MRSA carriage and recent hospital admission, chronic diseases, high and low BMI classes (underweight and obese), antibiotics use within the last month, and recurrent skin disease/infection. We strongly recommend the orientation of medical students to standard infection control practices of protocols and contact precautions. Further studies required to compare the nasal carriage of MRSA in clinical medical students with the general population.
We would like to show our gratitude to Mr. Muhammad Absar and Mr. Muhammad Arshad Zulfiqar (Laboratory Specialists, Microbiology Laboratory, KSUMC) for helping us with the processing of the samples.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Okamo B, Moremi N, Seni J, Mirambo MM, Kidenya BR, Mshana SE. Prevalence and antimicrobial susceptibility profiles of Staphylococcus aureus
nasal carriage among pre-clinical and clinical medical students in a Tanzanian University. BMC Res Notes 2016;9:47.
Bettin A, Causil C, Reyes N. Molecular identification and antimicrobial susceptibility of Staphylococcus aureus
nasal isolates from medical students in Cartagena, Colombia. Braz J Infect Dis 2012;16:329-34.
Pathare NA, Asogan H, Tejani S, Al Mahruqi G, Al Fakhri S, Zafarulla R, et al.
Prevalence of methicillin resistant Staphylococcus aureus
[MRSA] colonization or carriage among health-care workers. J Infect Public Health 2016;9:571-6.
Zakai SA. Prevalence of methicillin-resistant Staphylococcus aureus
nasal colonization among medical students in Jeddah, Saudi Arabia. Saudi Med J 2015;36:807-12.
Tiewsoh JB, Dias M. Screening of methicillin-resistant Staphylococcus aureus
in healthcare workers and students and its susceptibility to mupirocin in a tertiary care teaching hospital in South India. J Lab Physicians 2017;9:239-42.
] [Full text]
López-Aguilera S, Goñi-Yeste Mdel M, Barrado L, González-Rodríguez-Salinas MC, Otero JR, Chaves F. Staphylococcus aureus
nasal colonization in medical students: Importance in nosocomial transmission. Enferm Infecc Microbiol Clin 2013;31:500-5.
Rodríguez-Avial C, Alvarez-Novoa A, Losa A, Picazo JJ. Significant increase in the colonisation of Staphylococcus aureus
among medical students during their hospital practices. Enferm Infecc Microbiol Clin 2013;31:516-9.
Piechowicz L, Garbacz K, Wiśniewska K, Dąbrowska-Szponar M. Screening of Staphylococcus aureus
nasal strains isolated from medical students for toxin genes. Folia Microbiol (Praha) 2011;56:225-9.
De Boeck H, Vandendriessche S, Hallin M, Batoko B, Alworonga JP, Mapendo B, et al. Staphylococcus aureus
nasal carriage among healthcare workers in Kisangani, the democratic republic of the Congo. Eur J Clin Microbiol Infect Dis 2015;34:1567-72.
Schaefer AM, Mcmullen KM, Mayfield JL, Richmond A, Warren DK, Dubberke ER. Risk Factors Associated with Methicillin-Resistant Staphylococcus aureus Colonization on Hospital Admission among Oncology Patients. Am J Infect Control 2013;37:603-5.
Campbell KA, Cunningham C, Hasan S, Hutzler L, Bosco JA. Risk Factors for Developing Staphylococcus aureus Nasal Colonization in Spine and Arthroplasty Surgery. Bull Hosp Jt Dis [Internet] 2015;73:276-81.
Creech CB, Saye E, McKenna BD, Johnson BG, Jimenez N, Talbot TR, et al.
One-year surveillance of methicillin-resistant Staphylococcus aureus
nasal colonization and skin and soft tissue infections in collegiate athletes. Arch Pediatr Adolesc Med 2010;164:615-20.
Karanika S, Kinamon T, Grigoras C, Mylonakis E. Colonization with methicillin-resistant Staphylococcus aureus
and risk for infection among asymptomatic athletes: A systematic review and metaanalysis. Clin Infect Dis 2016;63:195-204.
Nerby JM, Gorwitz R, Lesher L, Juni B, Jawahir S, Lynfield R, et al.
Risk factors for household transmission of community-associated methicillin-resistant Staphylococcus aureus
. Pediatr Infect Dis J 2011;30:927-32.
Sassmannshausen R, Deurenberg RH, Köck R, Hendrix R, Jurke A, Rossen JW, et al.
MRSA prevalence and associated risk factors among health-care workers in non-outbreak situations in the Dutch-German EUREGIO. Front Microbiol 2016;7:1273.
Saadatian-Elahi M, Tristan A, Laurent F, Rasigade JP, Bouchiat C, Ranc AG, et al.
Basic rules of hygiene protect health care and lab workers from nasal colonization by Staphylococcus aureus
: An international cross-sectional study. PLoS One 2013;8:e82851.
Schulze-Geisthövel SV, Tappe EV, Schmithausen RM, Lepkojis J, Röttgen K, Petersen B, et al.
Survey on the risk awareness of German pig and cattle farmers in relation to dealing with MRSA and antibiotics. Infect Ecol Epidemiol 2016;6:29817.
[Table 1], [Table 2], [Table 3]