Iranian Journal of Medical Sciences

Document Type : Brief Report(s)


1 Department of Biology, College of Basic Sciences, Damghan Branch, Islamic Azad University, Damgan, Iran

2 Department of Pathobiology and Laboratory Sciences, Faculty of Medicine, North Khorasan University of Medical Sciences, Bojnurd, Iran



The present study aimed to investigate secondary bacterial infections among patients infected with severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2). Coagulase-negative Staphylococci can infect immunocompromised patients. Linezolid resistance among Staphylococcus epidermidis is one of the most critical issues. 
In 2019, 185 SARS-CoV-2-positive patients who were admitted to North Khorasan Province Hospital (Bojnurd, Iran), were investigated. Patients having positive SARS-CoV-2 reverse transcriptase real-time polymerase chain reaction (RT-PCR) test results, who had a history of intubation, mechanical ventilation, and were hospitalized for more than 48 hours were included. 
After microbiological evaluation of pulmonary samples, taken from intubated patients with clinical manifestation of pneumonia, co-infections were found in 11/185 patients (5.94%) with S. epidermidis, Staphylococcus aureus, and Acinetobacter baumani, respectively. Remarkably, seven out of nine S. epidermidis isolates were linezolid resistant. Selected isolates were characterized using antimicrobial resistance patterns and molecular methods, such as Staphylococcal cassette chromosome mec (SCCmec) typing, and gene detection for ica, methicillin resistance (mecA), vancomycin resistance (vanA), and chloramphenicol–florfenicol resistance (cfr) genes. 
All of the isolates were resistant to methicillin, and seven isolates were resistant to linezolid. Nine out of 11 isolated belonged to the SCCmec I, while two belonged to the SCCmec IV. It should be noted that all patients had the underlying disease, and six patients had already passed away.
The increasing linezolid resistance in bacterial strains becomes a real threat to patients, and monitoring such infections, in conjunction with surveillance and infection prevention programs, is very critical for reducing the number of linezolid-resistant Staphylococcal strains.


  1. Sharifipour E, Shams S, Esmkhani M, Khodadadi J, Fotouhi-Ardakani R, Koohpaei A, et al. Evaluation of bacterial co-infections of the respiratory tract in COVID-19 patients admitted to ICU. BMC Infect Dis. 2020;20:646. doi: 10.1186/s12879-020-05374-z. PubMed PMID: 32873235; PubMed Central PMCID: PMCPMC7461753.
  2. Wang J, Liu F, Tan JBX, Harbarth S, Pittet D, Zingg W. Implementation of infection prevention and control in acute care hospitals in Mainland China - a systematic review. Antimicrob Resist Infect Control. 2019;8:32. doi: 10.1186/s13756-019-0481-y. PubMed PMID: 30792854; PubMed Central PMCID: PMCPMC6371478.
  3. Nunez-Nunez M, Navarro MD, Palomo V, Rajendran NB, Del Toro MD, Voss A, et al. The methodology of surveillance for antimicrobial resistance and healthcare-associated infections in Europe (SUSPIRE): a systematic review of publicly available information. Clin Microbiol Infect. 2018;24:105-9. doi: 10.1016/j.cmi.2017.07.014. PubMed PMID: 28750921.
  4. Cortes MF, Andre C, Martins Simoes P, Corvec S, Caillon J, Tristan A, et al. Persistence of a multidrug-resistant worldwide-disseminated methicillin-resistant Staphylococcus epidermidis clone harbouring the cfr linezolid resistance gene in a French hospital with evidence of interspecies transfer to several Staphylococcus aureus lineages. J Antimicrob Chemother. 2022;77:1838-46. doi: 10.1093/jac/dkac119. PubMed PMID: 354259
  5. Hashemi SA, Safamanesh S, Ghasemzadeh-Moghaddam H, Ghafouri M, Mohajerzadeh-Heydari MS, Namdar-Ahmadabad H, et al. Report of death in children with SARS-CoV-2 and human metapneumovirus (hMPV) coinfection: Is hMPV the trigger? J Med Virol. 2021;93:579-81. doi: 10.1002/jmv.26401. PubMed PMID: 32767680; PubMed Central PMCID: PMCPMC7436913.
  6. Performance Standards for Antimicrobial Susceptibility Testing; 24th Informational Supplement. Wayne: Clinical and Laboratory Standards Institute; 2017.
  7. Xu Z, Cave R, Chen L, Yangkyi T, Liu Y, Li K, et al. Antibiotic resistance and molecular characteristics of methicillin-resistant Staphylococcus epidermidis recovered from hospital personnel in China. J Glob Antimicrob Resist. 2020;22:195-201. doi: 10.1016/j.jgar.2020.02.013. PubMed PMID: 32097759.
  8. Halaji M, Karimi A, Shoaei P, Nahaei M, Khorvash F, Ataei B, et al. Distribution of SCCmec Elements and Presence of Panton-Valentine Leukocidin in Methicillin-Resistant Staphylococcusepidermidis Isolated from Clinical Samples in a University Hospital of Isfahan City, Iran. J Clin Diagn Res. 2017;11:DC27-DC31. doi: 10.7860/JCDR/2017/25518.10258. PubMed PMID: 28892893; PubMed Central PMCID: PMCPMC5583865.
  9. Langford BJ, So M, Raybardhan S, Leung V, Westwood D, MacFadden DR, et al. Bacterial co-infection and secondary infection in patients with COVID-19: a living rapid review and meta-analysis. Clin Microbiol Infect. 2020;26:1622-9. doi: 10.1016/j.cmi.2020.07.016. PubMed PMID: 32711058; PubMed Central PMCID: PMCPMC7832079.
  10. MacIntyre CR, Chughtai AA, Barnes M, Ridda I, Seale H, Toms R, et al. The role of pneumonia and secondary bacterial infection in fatal and serious outcomes of pandemic influenza a(H1N1)pdm09. BMC Infect Dis. 2018;18:637. doi: 10.1186/s12879-018-3548-0. PubMed PMID: 30526505; PubMed Central PMCID: PMCPMC6286525.
  11. Maarouf L, Omar H, El-Nakeeb M, Abouelfetouh A. Prevalence and mechanisms of linezolid resistance among staphylococcal clinical isolates from Egypt. Eur J Clin Microbiol Infect Dis. 2021;40:815-23. doi: 10.1007/s10096-020-04045-w. PubMed PMID: 33104900.
  12. Kosecka-Strojek M, Sadowy E, Gawryszewska I, Klepacka J, Tomasik T, Michalik M, et al. Emergence of linezolid-resistant Staphylococcus epidermidis in the tertiary children’s hospital in Cracow, Poland. Eur J Clin Microbiol Infect Dis. 2020;39:1717-25. doi: 10.1007/s10096-020-03893-w. PubMed PMID: 32350737; PubMed Central PMCID: PMCPMC7427702.
  13. Ruiz-Ripa L, Fessler AT, Hanke D, Eichhorn I, Azcona-Gutierrez JM, Alonso CA, et al. Mechanisms of Linezolid Resistance Among Clinical Staphylococcus spp. in Spain: Spread of Methicillin- and Linezolid-Resistant S. epidermidis ST2. Microb Drug Resist. 2021;27:145-53. doi: 10.1089/mdr.2020.0122. PubMed PMID: 32456543.
  14. Shirvani F, Dashti AS, Seifi K. Staphylococcus and linezolid resistance in Iran. Archives of Pediatric Infectious Diseases. 2018;6. doi: 10.5812/pedinfect.12236.
  15. Romero LC, de Souza da Cunha MLR. Insights into the epidemiology of community-associated methicillin-resistant Staphylococcus aureus in special populations and at the community-healthcare interface. Braz J Infect Dis. 2021;25:101636. doi: 10.1016/j.bjid.2021.101636. PubMed PMID: 34672988; PubMed Central PMCID: PMCPMC9392173.