Detection of ica C gene involved in biofilm formation in methicillin-resistant Staphylococcus aureus (MRSA) isolates

Document Type : Original Article

Authors

1 Medical Microbiology and Immunology department, Faculty of Medicine, Beni-Suef University, Egypt

2 Medical Microbiology and Immunology Department, Faculty of Medicine, Beni-Suef University, Egypt.

3 M.B.B.CH Faculty of Medicine, Cairo University, Egypt

4 Internal medicine department, Faculty of Medicine, Beni-Suef University, Egypt

5 Medical Microbiology Department, Faculty of Pharmacy, Beni-Suef University, Egypt.

Abstract

Background: Staphylococcus aureus (S.aureus) is one of the gram-positive bacteria that causes a wide range of nosocomial infections. Our present study aimed to investigate genotypic and phenotypic aspects involved in biofilm formation in methicillin-resistant S.aureus strains isolated from hospital-acquired infections at Beni-Suef University Hospital Methodology: A total of 100 patients, 86 S. aureus strains were collected from all departments of Beni Suef University Hospital. The   antibiotic resistance pattern, phenotypes of biofilm formation and ica C gene were studied using Congo Red Agar (CRA) then molecular conformation was done by PCR. Results: We found that 80 out of 86 samples (93%) were mecicillin resistant S. aureus (MRSA). The highest frequency of resistance was found for oxacillin (95.3%), cefoxitin (88.4%), and ceftazidime (82.6%). Phenotypic results showed that 68.8% were high biofilm producers, while 10% and 21.2% were intermediate and low biofilm producers, respectively. From the 63 strong and intermediate biofilm producers isolates, we found that 55 specimens had the icaC gene (87.3%). Conclusion: Our study concluded that adherence ability and biofilm production are important for enhancing virulence factors among isolates of S. aureus strains.

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Main Subjects


  1. Khandan Del, A., Kaboosi, H., Jamalli, A., & Peyravii Ghadikolaii, F. (2019): Prevalence and Expression of ica C Gene in Biofilm-Producing aureus Clinical Isolates. Jundishapur Journal of Microbiology, 12(8).‏
  2. Gurung, R. R., Maharjan, P., & Chhetri, G. G. (2020): Antibiotic resistance pattern of aureus with reference to MRSA isolates from pediatric patients. Future science OA, 6(4), FSO464.‏
  3. Musini, A., Chilumoju, S. P., & Giri, A. (2022): Biofilm Formation in Drug-Resistant Pathogen aureus. In Microbial Biofilms (pp. 23). CRC Press.
  4. Kot, B., Sytykiewicz, H., & Sprawka, I. (2018): Expression of the biofilm-associated genes in MASA in biofilm and planktonic conditions. International journal of molecular sciences, 19(11), 3487.
  5. Zhang, Y., Xu, D., Shi, L., Cai, R., Li, C., & Yan, H. (2018): Association between agar type, virulence factors, biofilm formation and antibiotic resistance of aureus isolates from pork production. Frontiers in microbiology, 1876.
  6. Balaure, P.C.; Grumezescu, A.M. (2020): Recent Advances in Surface Nanoengineering for Biofilm Prevention and Control. Part I: Molecular Basis of Biofilm Recalcitrance. Passive Anti-Biofouling Nanocoatings. Nanomaterials, 10, 1230.
  7. Guzmán-Soto, I., McTiernan, C., Gonzalez-Gomez, M., Ross, A., Gupta, K., Suuronen, E. J., et al. (2021). Mimicking biofilm formation and development: recent progress in in-vitro and in vivo biofilm models. iScience 24:102.
  8. Miquel, S., Lagrafeuille, R., Souweine, B., and Forestier, C. (2016). Anti-biofilm activity as a health issue. Front. Microbiol. 7:592.
  9. Meeker, D. G., Beenken, K. E., Mills, W. B., Loughran, A. J., Spencer, H. J., Lynn, W. B., et al. (2016). Evaluation of antibiotics active against methicillin-resistant aureus based on activity in an established biofilm. Antimicrob. Agents Chemother. 60, 5688.
  10. Branstetter, J., Searcy, H., Benner, K., Yarbrough, A., Crowder, C., and Troxler, B. (2020). Ceftaroline vs vancomycin for the treatment of acute pulmonary exacerbations in pediatric patients with cystic fibrosis. Pediatr. Pulmonol. 55, 3337.
  11. Mottola, C., Matias, C. S., Mendes, J. J., Melo-Cristino, J., Tavares, L., Cavaco-Silva, P., et al. (2016). Susceptibility patterns of aureus biofilms in diabetic foot infections. BMC Microbiol. 16:119.
  12. Abbanat, D., Shang, W., Amsler, K., Santoro, C., Baum, E., Crespo-Carbone, S., et al. (2014): Evaluation of the in vitro activities of ceftobiprole and comparators in staphylococcal colony or microtitre plate biofilm assays. Int. Journal of Antimicrob. Agents 43, 32.
  13. Silva, V., Almeida, L., Gaio, V., Cerca, N., Manageiro, V., Caniça, M., Capelo, J. L., Igrejas, G., & Poeta, P. (2021). Biofilm Formation of Multidrug-Resistant MRSA Strains Isolated from Different Types of Human Infections. Pathogens (Basel, Switzerland), 10(8), 970.
  14. Allam, N. (2017): Correlation between Biofilm Production and Bacterial Urinary Tract Infections: New Therapeutic Approach. Egyptian Journal of Microbiology, 52(1), 39.
  15. Zhen, X., Lundborg, C. S., Zhang, M., Sun, X., Li, Y., Hu, X., ... & Dong, H. (2020). Clinical and economic impact of methicillin-resistant aureus: a multicentre study in China. Scientific reports10(1), 3900.
  16. Chen, L., Tang, Z. Y., Cui, S. Y., Ma, Z. B., Deng, H., Kong, W. L., Yang, L. W., Lin, C., Xiong, W. G., & Zeng, Z. L. (2020). Biofilm Production Ability, Virulence and Antimicrobial Resistance Genes in  aureus from Various Veterinary Hospitals. Pathogens (Basel, Switzerland), 9(4), 264. https://doi.org/10.3390/pathogens9040264
  17. Mirzaee, M., Najar-Peerayeh, S., Behmanesh, M., & Moghadam, M. F. (2015). Relationship between adhesin genes and biofilm formation in vancomycin-intermediate aureus clinical isolates. Current microbiology, 70(5), 665–670.
  18. Arciola, C. R., Baldassarri, L., & Montanaro, L. (2001). Presence of icaA and icaD genes and slime production in a collection of staphylococcal strains from catheter-associated infections. Journal of clinical microbiology, 39(6), 2151–2156. https://doi.org/10.1128/JCM.39.6.2151-2156.2001
  19. Sapkota, J., Sharma, M., Jha, B., & Bhatt, C. P. (2019). Prevalence of staphylococcus aureus isolated from clinical samples in a tertiary care hospital: A descriptive cross-sectional study. JNMA: Journal of the Nepal Medical Association57(220), 398.
  20. Koukos, G., Sakellari, D., Arsenakis, M., Tsalikis, L., Slini, T., & Konstantinidis, A. (2015). Prevalence of Staphylococcus aureus and methicillin resistant Staphylococcus aureus (MRSA) in the oral cavity. Archives of oral biology60(9), 1410-1415.
  21. Musa, I., Saadu, M., & Jibril, F. (2022). Antibiogram and detection of mecA gene among MRSA at Specialist Hospital Sokoto. Microbes and Infectious Diseases.
  22. Bhat, Y. J., Hassan, I., Bashir, S., Farhana, A., & Maroof, P. (2016). Clinico-bacteriological profile of primary pyodermas in Kashmir: a hospital-based study. Journal of the Royal College of Physicians of Edinburgh46(1), 8-13.
  23. Qureshi, A. H., Rafi, S., Qureshi, S. M., & Ali, A. M. (2004). The current susceptibility patterns of methicillin resistant Staphylococcus aureus to conventional anti Staphylococcus antimicrobials at Rawalpindi. Pak J Med Sci20(4), 361-364.
  24. Mehta, A. A., Rodrigues, C. C., Kumar, R. R., Rattan, A. A., Sridhar, H. H., Mattoo, V. V., & Ginde, V. V. (1996). A pilot programme of MRSA surveillance in India.(MRSA Surveillance Study Group). Journal of Postgraduate medicine42(1), 1
  25. Rajaduraipandi, K., Mani, K. R., Panneerselvam, K., Mani, M., Bhaskar, M., & Manikandan, P. (2006). Prevalence and antimicrobial susceptibility pattern of methicillin resistant aureus: A multicentre study. Indian journal of medical microbiology24(1), 34-38.
  26. Das, B., Mandal, D., Dash, S. K., Chattopadhyay, S., Tripathy, S., Dolai, D. P., ... & Roy, S. (2016). Eugenol provokes ROS-mediated membrane damage-associated antibacterial activity against clinically isolated multidrug-resistant Staphylococcus aureus strains. Infectious Diseases: Research and Treatment9, IDRT-S31741.
  27. Abdel-Maksoud, M., El-Shokry, M., Ismail, G., Hafez, S., El-Kholy, A., Attia, E., & Talaat, M. (2016). Methicillin-resistant aureus recovered from healthcare-and community-associated infections in Egypt. International journal of bacteriology2016.
  28. Singh, S., Datta, S., Narayanan, K. B., & Rajnish, K. N. (2021). Bacterial exo-polysaccharides in biofilms: role in antimicrobial resistance and treatments. Journal, genetic engineering & biotechnology19(1), 140. https://doi.org/10.1186/s43141-021-00242-y
  29. Jian, Z., Zeng, L., Xu, T., Sun, S., Yan, S., Yang, L., ... & Dou, T. (2021). Antibiotic resistance genes in bacteria: Occurrence, spread, and control. Journal of Basic Microbiology61(12), 1049-1070.
  30. Kord, M., Ardebili, A., Jamalan, M., Jahanbakhsh, R., Behnampour, N., & Ghaemi, E. A. (2018). Evaluation of Biofilm Formation and Presence of IcaGenes in Staphylococcus epidermidis Clinical Isolates. Osong public health and research perspectives9(4), 160–166. https://doi.org/10.24171/j.phrp.2018.9.4.04
  31. Agarwal, A., & Jain, A. (2013). Glucose & sodium chloride induced biofilm production & ica operon in clinical isolates of staphylococci. The Indian journal of medical research138(2), 262.
  32. Oniciuc, E. A., Cerca, N., & Nicolau, A. I. (2016). Compositional analysis of biofilms formed by aureus isolated from food sources. Frontiers in microbiology7, 390.
  33. Mirzaee, M., Najar Peerayeh, S., & Ghasemian, A. M. (2014). Detection of icaABCD genes and biofilm formation in clinical isolates of methicillin resistant aureusIranian Journal of Pathology9(4), 257-262.
  34. 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 aureusIranian Biomedical Journal24(6), 386.
  35. Parastan, R., Kargar, M., Solhjoo, K., & Kafilzadeh, F. (2020). A synergistic association between adhesion-related genes and multidrug resistance patterns of aureus isolates from different patients and healthy individuals. Journal of Global Antimicrobial Resistance22, 379-385.
  36. Ballah, F. M., Islam, M. S., Rana, M. L., Ferdous, F. B., Ahmed, R., Pramanik, P. K., ... & Rahman, M. T. (2022). Phenotypic and Genotypic Detection of Biofilm-Forming aureus from Different Food Sources in Bangladesh. Biology11(7), 949.
  37. Fariña N, Samudio M, Carpinelli L, Nentwich MM and de Kaspar H M (2017): Methicillin resistance and biofilm production of Staphylococcus epidermidis isolates from infectious and normal flora conjunctiva. Int Ophthalmol.; 37(4): 819-825
  38. Post V, Harris LG, Morgenstern M, Mageiros L, Hitchings MD, Méric G, Pascoe B, Sheppard SK, Richards RG and Moriarty TF (2017): A comparative genomics study of Staphylococcus epidermidis from orthopedic device-related infections correlated with patient outcome. J Clin Microbiol. Aug 9 [Epub ahead of print].
  39. Mahamuni-Badiger, P. P., Patil, P. M., Badiger, M. V., Patel, P. R., Thorat-Gadgil, B. S., Pandit, A., & Bohara, R. A. (2020). Biofilm formation to inhibition: Role of zinc oxide-based nanoparticles. Materials Science and Engineering: C108, 110319.