Molecular Characterization of Staphylococcus aureus Isolates Obtained from Hemodialyzed Patients at the Hospital de Clínicas of Paraguay: A pilot study


  • Rubén Arturo Silvero Isidre, Universidad Nacional de Asunción, Paraguay.
  • Fátima Rodríguez Acosta Universidad Nacional de Asunción, Paraguay
  • César Rodrigo Cristaldo Vargas Universidad Nacional de Asunción, Paraguay
  • Genaro Américo Velázquez Romero Universidad Nacional de Asunción, Paraguay.
  • José Félix Plans Perrota Universidad Nacional de Asunción, Paraguay.
  • Rosa María Guillén Fretes Universidad Nacional de Asunción, Paraguay



Staphylococcus aureus, Hemodialysis, Antibiotic resistance, bacterial typing


Background: Patients undergoing hemodialysis are susceptible to the nasal carriage of Staphylococcus aureus, increasing the risk of developing infections associated with higher morbidity and mortality. The objective of this study was to describe the frequency of S. aureus carriage in hemodialysis patients and to perform molecular analysis of isolates by applying multiple-locus variable analysis.

Methods: We conducted a descriptive cross sectional study with non-probabilistic sampling that included 28 hemodialysis patients attending the Nephrology Department of Hospital de Clínicas in Asunción, Paraguay. We obtained clinical data from medical records and interviews with patients. Nasal swabs were collected and analyzed by microbiological and molecular methods.

Results: The frequency of S. aureus carriage was 50% (14/28), 93% of which (13/14) were methicillin resistant, 57% (6/14) were gentamicin resistant and 36% (5/14) were resistant to more than 4 antibiotic classes. S. aureus carriers showed higher frequency of rhinitis (p=0.02 odds ratio [OR]=6.6 (1.2- 34.4)). Seven methicillin-resistant S. aureus isolates had been analyzed by multiple-locus variable analysis, two of them showed identical pattern bands.

Conclusion: We found a high frequency of methicillin-resistant Staphylococcus aureus colonization and the presence of two isolates with identical profile in the multiple-locus variable analysis indicating the possibility of transmission between patients.


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Author Biography

Rubén Arturo Silvero Isidre,, Universidad Nacional de Asunción, Paraguay.

Artu¬ro Silvero Isidre is a fi¬nal-year medical student of a six-year program at the Universidad Nacional de Asunción, Paraguay. He is editor of a scientific journal called CIMEL and a member of a scientific so¬ciety of medical students (SOCIEM-UNA) in Paraguay


1. Giarola LB, dos Santos RR, Tognim MCB, Borelli SD, Bedendo J. Carriage frequency, phenotypic and genotypic characteristics of Staphylococcus au¬reus isolated from dialysis and kidney transplant patients at a hospital in Northern Paraná. Braz J Microbiol. 2012 Jul;43(3):923-30.
2. Greiner W, Rasch A, Köhler D, Salzberger B, Fätkenheuer G, Leidig M. Clini¬cal outcome and costs of nosocomial and community-acquired Staphylococ¬cus aureus bloodstream infection in haemodialysis patients. Clin Microbiol Infect. 2007 Mar;13(3):264–8.
3. Enright MC, Day NPJ, Davies CE, Peacock SJ, Spratt BG. Multilocus Sequence Typing for Characterization of Methicillin-Resistant and Methicillin-Suscepti¬ble Clones of Staphylococcus aureus. J Clin Microbiol. 2000 Mar;38(3):1008-15.
4. Saxena AK, Panhotra BR. The Prevalence of Nasal Carriage of Staphylo¬coccus aureus and Associated Vascular Access-Related Septicemia Among Patients on Hemodialysis in Al-Hasa Region of Saudi Arabia. Saudi J Kidney Dis Transpl. 2003 Jan;14(1):30-8.
5. Sanavi S, Ghods A, Afshar R. Catheter associated infections in hemodialysis patients. Saudi J Kidney Dis Transpl. 2007 Jan;18(1):43.
6. Vandecasteele SJ, Boelaert JR, De Vriese AS. Staphylococcus aureus In¬fections in Hemodialysis: What a Nephrologist Should Know. Clin J Am Soc Nephrol. 2009 Aug;4(8):1388-400.
7. Schmid H, Romanos A, Schiffl H, Lederer SR. Persistent nasal methici¬llin-resistant Staphylococcus aureus carriage in hemodialysis outpatients: a predictor of worse outcome. BMC Nephrol. 2013 Apr;14:93.
8. Lai CF, Liao CH, Pai MF, Chu FY, Hsu SP, Chen HY, et al. Nasal carriage of me¬thicillin-resistant Staphylococcus aureus is associated with higher all-cause mortality in hemodialysis patients. Clin J Am Soc Nephrol. 2011 Jan;6(1):167- 74.
9. Peacock SJ, de Silva GD, Justice A, Cowland A, Moore CE, Winearls CG, et al. Comparison of Multilocus Sequence Typing and Pulsed-Field Gel Electropho¬resis as Tools for Typing Staphylococcus aureus Isolates in a Microepidemio¬logical Setting. J Clin Microbiol. 2002 Oct;40(10):3764-70.
10. Chung S, Yi J, Jang MH, Joo S-I, Ra EK, Kim SY, et al. Comparison of Modified Multiple-locus Variable-number Tandem-repeat Fingerprinting with Pulsed-field Gel Electrophoresis for Typing Clinical Isolates of Staphylococcus aureus. Ann Lab Med. 2012 Jan;32(1):50-6.
11. Manfredi EA, Leotta GA, Rivas M. Multiplex PCR for the detection of sea, seb, sec, sed and see genes of Staphylococcus aureus. Characterization of isolates from food. Rev Argent Microbiol. 2010 Sep;42(3):212-5.
12. Sabat A, Krzyszton-Russjan J, Strzalka W, Filipek R, Kosowska K, Hryniewicz W, et al. New Method for Typing Staphylococcus aureus Strains: Multiple-Lo¬cus Variable-Number Tandem Repeat Analysis of Polymorphism and Genetic Relationships of Clinical Isolates. J Clin Microbiol. 2003 Apr;41(4):1801-4.
13. Sambrook J, Russell D. Molecular Cloning. A Laboratory Manual. 3rd ed. New York: Cold Spring Harbor Laboratory; 2001.
14. Jamil B, Bokhari MT, Saeed A, Mukhtar Bokhari MZ, Hussain Z, Khalid T, et al. Bacteremia: Prevalence and antimicrobial resistance profiling in chro¬nic kidney diseases and renal transplant patients. J Pak Med Assoc. 2016 Jun;66(6):705–9.
15. Mohajeri P, Azizkhani S, Farahani A, Norozi B. Genotyping of coa and aroA Genes of Methicillin-Resistant Staphylococcus aureus Strains Isolated From Nasal Samples in Western Iran. Jundishapur J Microbiol. 2016 Jan;9(1):e26460.
16. Verhoeven PO, Gagnaire J, Haddar CH, Grattard F, Thibaudin D, Afiani A, et al. Identifying Hemodialysis Patients With the Highest Risk of Staphylococcus aureus Endogenous Infection Through a Simple Nasal Sampling Algorithm. Medicine (Baltimore). 2016 Apr;95(14):e3231.
17. Price A, Sarween N, Gupta I, Baharani J. Meticillin-resistant Staphylococ¬cus aureus and meticillin-susceptible Staphylococcus aureus screening in a cohort of haemodialysis patients: carriage, demographics and outcomes. J Hosp Infect. 2015 May;90(1):22–7.
18. Devraj A, Siva Tez Pinnamaneni V, Biswal M, Ramachandran R, Jha V. Extranasal Staphylococcus aureus colonization predisposes to bloodstream infections in patients on hemodialysis with noncuffed internal jugular vein catheters. Hemodial Int. 2016 Jun;doi:10.1111/hdi.12450.
19. Zacharioudakis IM, Zervou FN, Ziakas PD, Mylonakis E. Meta-Analysis of Methicillin-Resistant Staphylococcus aureus Colonization and Risk of Infec¬tion in Dialysis Patients. J Am Soc Nephrol. 2014 Sep; 25(9):2131-41.
20. Lim CJ, Cheng AC, Kennon J, Spelman D, Hale D, Melican G, et al. Prevalen¬ce of multidrug-resistant organisms and risk factors for carriage in long-term care facilities: a nested case-control study. J Antimicrob Chemother. 2014 Jul;69(7):1972-80.
21. Rabelo MA, Bezerra Neto AM, Loibman SO, Lima JL, Ferreira EL, Leal NC, et al. The occurrence and dissemination of methicillin and vancomycin-resis¬tant Staphylococcus in samples from patients and health professionals of a university hospital in Recife, State of Pernambuco, Brazil. Rev Soc Bras Med Trop. 2014 Aug;47(4):437-46.
22. Reyes J, Rincón S, Díaz L, Panesso D, Contreras GA, Zurita J, et al. Dissemi¬nation of Methicillin-Resistant Staphylococcus aureus USA300 Sequence Type 8 Lineage in Latin America. Clin Infect Dis. 2009 Dec;49(12):1861–7.
23. Tenover FC, Vaughn RR, McDougal LK, Fosheim GE, McGowan JE Jr. Multi¬ple-Locus Variable-Number Tandem-Repeat Assay Analysis of Methicillin-Re¬sistant Staphylococcus aureus Strains. J Clin Microbiol. 2007 Jul;45(7):2215–9.
24. Malachowa N, Sabat A, Gniadkowski M, Krzyszton-Russjan J, Empel J, Miedzobrodzki J, et al. Comparison of Multiple-Locus Variable-Number Tan¬dem-Repeat Analysis with Pulsed-Field Gel Electrophoresis, spa Typing, and Multilocus Sequence Typing for Clonal Characterization of Staphylococcus aureus Isolates. J Clin Microbiol. 2005 Jul;43(7):3095–100.
25. Garnacho-Montero J, Huici-Moreno MJ, Gutiérrez-Pizarraya A, López I, Már¬quez-Vácaro JA, Macher H, et al. Prognostic and diagnostic value of eosinope¬nia, C-reactive protein, procalcitonin, and circulating cell-free DNA in critically ill patients admitted with suspicion of sepsis. Crit Care. 2014 Jun;18(3):R116.
26. Gröger M, Bernt A, Wolf M, Mack B, Pfrogner E, Becker S, et al. Eosinophils and mast cells: a comparison of nasal mucosa histology and cytology to markers in nasal discharge in patients with chronic sino-nasal diseases. Eur Arch Otorhinolaryngol. 2013 Sep;270(10):2667-76.
27. Çevik C, Yula E, Yengil E, Gülmez M?, Akbay E. Identification of nasal bacterial flora profile and carriage rates of methicillin-resistant Staphylococ¬cus aureus in patients with allergic rhinitis. Eur Arch Otorhinolaryngol. 2014 Jan;271(1):103-7.
28. Mettang T, Kremer AE. Uremic pruritus. Kidney Int. 2015 Apr;87(4):685-91.
29. Kim YC, Kim MH, Song JE, Ahn JY, Oh DH, Kweon OM, et al. Trend of me¬thicillin-resistant Staphylococcus aureus (MRSA) bacteremia in an institution with a high rate of MRSA after the reinforcement of antibiotic stewardship and hand hygiene. Am J Infect Control. 2013 May;41(5):e39-43.



How to Cite

Silvero Isidre, R. A., Rodríguez Acosta, F., Cristaldo Vargas, C. R., Velázquez Romero, G. A., Plans Perrota, J. F., & Guillén Fretes, R. M. (2017). Molecular Characterization of Staphylococcus aureus Isolates Obtained from Hemodialyzed Patients at the Hospital de Clínicas of Paraguay: A pilot study. International Journal of Medical Students, 5(1), 14–19.



Original Article