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Methicillin-Resistant Staphylococci (MRS): Carriage and Antibiotic Resistance Patterns in College Students

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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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References

  1. 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

    Article  PubMed  PubMed Central  Google Scholar 

  2. 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

    Article  CAS  PubMed  Google Scholar 

  3. 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

    Article  Google Scholar 

  4. 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

    Article  CAS  PubMed  Google Scholar 

  5. 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.

    Google Scholar 

  6. 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

    Article  CAS  Google Scholar 

  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.

    Google Scholar 

  8. 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.

    Article  Google Scholar 

  9. Pourhoseingholi, M. A., Vahedi, M., & Rahimzadeh, M. (2013). Sample size calculation in medical studies. Gastroenterology and Hepatology from Bed to Bench, 6(1), 14.

    PubMed  PubMed Central  Google Scholar 

  10. 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.

    Google Scholar 

  11. Clinical and Laboratory Standards Institute. (2012). Performance standards for antimicrobial disk susceptibility tests; approved standard. CLSI Document M02-A11.

  12. 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.

    Article  Google Scholar 

  13. 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.

    PubMed  PubMed Central  Google Scholar 

  14. 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.

    Article  CAS  Google Scholar 

  15. 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.

    Article  CAS  Google Scholar 

  16. Cuny, C., Wieler, L. H., & Witte, W. (2015). Livestock-associated MRSA: The impact on humans. Antibiotics, 4(4), 521–543.

    Article  Google Scholar 

  17. 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

    Article  PubMed  PubMed Central  Google Scholar 

  18. 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.

    Article  CAS  Google Scholar 

  19. 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

    Article  CAS  Google Scholar 

  20. 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.

    Article  CAS  Google Scholar 

  21. 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.

    Article  CAS  Google Scholar 

  22. 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.

  23. 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.

    Article  CAS  Google Scholar 

  24. 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.

    PubMed  PubMed Central  Google Scholar 

  25. 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.

    Article  CAS  Google Scholar 

  26. 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

    Article  Google Scholar 

  27. 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.

    Article  CAS  Google Scholar 

  28. 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.

    Article  Google Scholar 

  29. 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.

    Article  Google Scholar 

  30. 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.

    Article  Google Scholar 

Download references

Acknowledgements

The authors acknowledge the Deanship of Scientific Research at the University of Petra for facilitating all phases of this research.

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No external funding was used for conducting this study.

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Contributions

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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Correspondence to Suzanne M. A. Abdelmalek or Phillip J. Collier.

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Ethical approval for the study was obtained from the scientific and the ethics committees at UOP (12H-11-2019).

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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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