Abstract
Asymptomatic carriage of methicillin-resistant Staphylococci (MRS) may allow for the unseen dissemination of antibiotic-resistant strains through the population. This study investigates the prevalence and epidemiological risk factors that contribute to the spread of MRS in a university setting in Amman, Jordan. A cross-sectional questionnaire-based study was performed in December 2019. Five hundred and four students enrolled in the study and provided skin and nasal swabs. Swabs were then processed to isolate MRS on Mannitol Salt Agar (MSA) + 4 µg/ml oxacillin. Isolates were tested for their antibiotic susceptibility using the disc diffusion assay. Epidemiological risk assessment was performed using the Chi-square test and univariate and multivariant analysis. The percentage carriage of MRS in the 504 students was 40.4%. The carriage rate of methicillin-resistant Staphylococcus aureus (MRSA) and methicillin-resistant Staphylococcus epidermidis (MRSE) from the skin and nasal areas was 13.5% and 26.9%, respectively. The percentage of male carriers was significantly higher than females, and the only identified epidemiological risk factor related to the carriage was attendance at a fitness club. All MRS isolates were resistant to oxacillin (100%), cefoxitin (45.5%), erythromycin (35.2%), gentamycin (10.2%), ciprofloxacin (12.7%), nitrofurantoin (12.2%), linezolid (7.8%), amikacin (1.47%), and Vancomycin (0.49%). 42% of MRS expressed a multiple antibiotic resistance (MAR) index above 0.2. Three isolates expressed a MAR index of 0.8. MRS has been exhibited to be present in an otherwise healthy population of students, which may then act as a reservoir for MAR strains.
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Guo, Y., Song, G., Sun, M., Wang, J., & Wang, Y. (2020). Prevalence and therapies of antibiotic-resistance in Staphylococcus aureus. Frontiers in cellular and Infection Microbiology, 10, 107. https://doi.org/10.3389/fcimb.2020.00107
Barbier, F., Ruppé, E., Hernandez, D., Lebeaux, D., Francois, P., Felix, B., & Ruimy, R. (2010). Methicillin-resistant coagulase-negative staphylococci in the community: High homology of SCCmec IVa between Staphylococcus epidermidis and major clones of methicillin-resistant Staphylococcus aureus. The Journal of Infectious Diseases, 202(2), 270–281. https://doi.org/10.1086/653483
Misic, A. M., Davis, M. F., Tyldsley, A. S., Hodkinson, B. P., Tolomeo, P., Hu, B., & Grice, E. A. (2015). The shared microbiota of humans and companion animals as evaluated from Staphylococcus carriage sites. Microbiome, 3(1), 1–19. https://doi.org/10.1186/s40168-014-0052-7
Reinoso, E. B., Ibañez, F., Raspanti, C., Odierno, L., & Bogni, C. I. (2006). Characterization of Staphylococcus aureus strains isolated from humans in Argentina. Journal of Basic Microbiology, 46(4), 286–293. https://doi.org/10.1002/jobm.200510100
Kitti, T., Boonyonying, K., & Sitthisak, S. (2011). Prevalence of methicillin-resistant Staphylococcus aureus among university students in Thailand. Southeast Asian Journal of Tropical Medicineand Public Health, 42(6), 1498.
Peyrusson, F., Varet, H., Nguyen, T. K., Legendre, R., Sismeiro, O., Coppée, J. Y., & Van Bambeke, F. (2020). Intracellular Staphylococcus aureus persisters upon antibiotic exposure. Nature Communications, 11(1), 1–14. https://doi.org/10.1038/s41467-020-15966-7
Rohde, R. E., Denham, R., & Brannon, A. (2009). Methicillin resistant Staphylococcus aureus: Carriage rates and characterization of students in a Texas university. American Society for Clinical Laboratory Science, 22(3), 176–184.
De Giusti, M., Marinelli, L., Aurigemma, C., Tufi, D., Mannocci, A., Solimini, A. G., & La Torre, G. (2013). Prevalence of Staphylococcus aureus colonization and antibiotic susceptibility: A survey among biomedical students. Public Health, 127(4), 392–394.
Pourhoseingholi, M. A., Vahedi, M., & Rahimzadeh, M. (2013). Sample size calculation in medical studies. Gastroenterology and Hepatology from Bed to Bench, 6(1), 14.
Kumurya, A. S. (2017). Use of Mannitol Salt Agar (MSA) and cefoxitin as a selective culture medium for growing MRSA strains. Frontiers in Biomedical Sciences, 2(1), 1–5.
Clinical and Laboratory Standards Institute. (2012). Performance standards for antimicrobial disk susceptibility tests; approved standard. CLSI Document M02-A11.
Nomura, R., Nakaminami, H., Takasao, K., Muramatsu, S., Kato, Y., Wajima, T., & Noguchi, N. (2020). A class A β-lactamase produced by borderline oxacillin-resistant Staphylococcus aureus hydrolyses oxacillin. Journal of Global Antimicrobial Resistance, 22, 244–247.
Dibah, S., Arzanlou, M., Jannati, E., & Shapouri, R. (2014). Prevalence and antimicrobial resistance pattern of methicillin resistant Staphylococcus aureus (MRSA) strains isolated from clinical specimens in Ardabil, Iran. Iranian Journal of Microbiology, 6(3), 163.
McDougal, L. K., Fosheim, G. E., Nicholson, A., Bulens, S. N., Limbago, B. M., Shearer, J. E., & Patel, J. B. (2010). Emergence of resistance among USA300 methicillin-resistant Staphylococcus aureus isolates causing invasive disease in the United States. Antimicrobial Agents and Chemotherapy, 54(9), 3804–3811.
Otter, J. A., & French, G. L. (2011). Utility of antimicrobial susceptibility-based algorithms for the presumptive identification of genotypically-defined community-associated methicillin-resistant Staphylococcus aureus at a London teaching hospital. European Journal of Clinical Microbiology & Infectious Diseases, 30(3), 459–463.
Cuny, C., Wieler, L. H., & Witte, W. (2015). Livestock-associated MRSA: The impact on humans. Antibiotics, 4(4), 521–543.
Boswihi, S. S., Udo, E. E., Mathew, B., Noronha, B., Verghese, T., & Tappa, S. B. (2020). Livestock-associated methicillin-resistant Staphylococcus aureus in patients admitted to Kuwait hospitals in 2016–2017. Frontiers in Microbiology, 10, 2912. https://doi.org/10.3389/fmicb.2019.02912
Heikens, E., Fleer, A., Paauw, A., Florijn, A., & Fluit, A. C. (2005). Comparison of genotypic and phenotypic methods for species-level identification of clinical isolates of coagulase-negative staphylococci. Journal of Clinical Microbiology, 43(5), 2286–2290.
Alkhawaja, E., Hammadi, S., Abdelmalek, M., Mahasneh, N., Alkhawaja, B., & Abdelmalek, S. M. (2020). Antibiotic resistant Cutibacterium acnes among acne patients in Jordan: A cross sectional study. BMC Dermatology, 20(1), 1–9. https://doi.org/10.1186/s12895-020-00108-9
Ayandele, A. A., Oladipo, E. K., Oyebisi, O., & Kaka, M. O. (2020). Prevalence of multi-antibiotic resistant Escherichia coli and Klebsiella species obtained from a tertiary medical institution in Oyo State, Nigeria. Qatar Medical Journal, 2020(1), 9.
Yan, M., Pamp, S. J., Fukuyama, J., Hwang, P. H., Cho, D. Y., Holmes, S., & Relman, D. A. (2013). Nasal microenvironments and interspecific interactions influence nasal microbiota complexity and S. aureus carriage. Cell Host & Microbe, 14(6), 631–640.
Alzoubi, H., Al Madadha, M., Al-Mnayyis, A., Azzam, M., Aldawoud, A., Hwaiti, D., ... & Qatamin, M. (2020, June). Detection of Methicillin Susceptible and Resistant Staphylococcus aureus Nasal Carriage and Its Antibiotic Sensitivity among Basic and Clinical Years Medical Students. In Healthcare (Vol. 8, No. 2, p. 161). Multidisciplinary Digital Publishing Institute.
Al-Tamimi, M., Himsawi, N., Abu-Raideh, J., Al-jawaldeh, H., Mahmoud, S. A. H., Hijjawi, N., & Hawamdeh, H. (2018). Nasal colonization by methicillin-sensitive and methicillin-resistant Staphylococcus aureus among medical students. The Journal of Infection in Developing Countries, 12(05), 326–335.
Khasawneh, A. I., Himsawi, N., Abu-Raideh, J., Salameh, M. A., Al-Tamimi, M., Mahmoud, S. A. H., & Saleh, T. (2020). Status of biofilm-forming genes among Jordanian nasal carriers of methicillin-sensitive and methicillin-resistant Staphylococcus aureus. Iranian Biomedical Journal, 24(6), 386.
Al-Bakri, A. G., Al-Hadithi, H., Kasabri, V., Othman, G., Kriegeskorte, A., & Becker, K. (2013). The epidemiology and molecular characterization of methicillin-resistant staphylococci sampled from a healthy Jordanian population. Epidemiology & Infection, 141(11), 2384–2391.
Kumar, H., & Mansoor, S. M. (2016). A study of community-acquired methicillin-resistant Staphylococcus aureus infections among college students. Indian Journal of Communicable Diseases. https://doi.org/10.21088/ijcd.2395.6631.2216.3
Jaradat, Z. W., Khwaileh, M., Al Mousa, W., Ababneh, Q. O., & Al Nabulsi, A. (2021). Occurrence, distribution and pattern analysis of methicillin resistant (MRSA) and methicillin sensitive (MSSA) Staphylococcus aureus on fomites in public facilities. Pathogens and Global Health, 115(6), 377–391.
Prates, K. A., Torres, A. M., Garcia, L. B., Ogatta, S. F. Y., Cardoso, C. L., & Tognim, M. C. B. (2010). Nasal carriage of methicillin-resistant Staphylococcus aureus in university students. Brazilian Journal of Infectious Diseases, 14, 316–318.
Zhou, Y. P., Wilder-Smith, A., & Hsu, L. Y. (2014). The role of international travel in the spread of methicillin-resistant Staphylococcus aureus. Journal of Travel Medicine, 21(4), 272–281.
Stevens, A. M., Hennessy, T., Baggett, H. C., Bruden, D., Parks, D., & Klejka, J. (2010). Methicillin-resistant Staphylococcus aureus carriage and risk factors for skin infections, Southwestern Alaska, USA. Emerging Infectious Diseases, 16(5), 797.
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The authors acknowledge the Deanship of Scientific Research at the University of Petra for facilitating all phases of this research.
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SMAA had the original idea for this work, which was completed at experimentally by MWQ under the supervision of SMAA. RAE performed statistical analysis. SMAA wrote the first draft of the paper and subsequently, PJC made an intellectual contribution to the completion of the work and all subsequent drafts of the manuscript.
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Abdelmalek, S.M.A., Qinna, M.W., Al-Ejielat, R. et al. Methicillin-Resistant Staphylococci (MRS): Carriage and Antibiotic Resistance Patterns in College Students. J Community Health 47, 416–424 (2022). https://doi.org/10.1007/s10900-022-01065-9
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DOI: https://doi.org/10.1007/s10900-022-01065-9