Journal of Veterinary Science

The Korean Society of Veterinary Science (대한수의학회)
권호 표지
DOI QR코드

DOI QR Code

Effectiveness of cephalosporins in hydrolysis and inhibition of Staphylococcus aureus and Escherichia coli biofilms

  • Jawaria Aslam (Department of Physiology and Biochemistry, Cholistan University of Veterinary and Animal Sciences) ;
  • Hafiz Muhammad Ali (Faculty of Veterinary and Animal Sciences, The Islamia University of Bahawalpur) ;
  • Shujaat Hussain (PMAS Arid Agriculture University) ;
  • Muhammad Zishan Ahmad (PMAS Arid Agriculture University) ;
  • Abu Baker Siddique (Institute of Microbiology, Government College University) ;
  • Muhammad Shahid (Department of Biochemistry, University of Agriculture) ;
  • Mirza Imran Shahzad (Center for Comparative Medicine, University of California) ;
  • Hina Fatima (Department of Biochemistry, University of Agriculture) ;
  • Sarah Tariq (Department of Biochemistry, Institute of Biochemistry, Biotechnology and Bioinformatics, The Islamia University of Bahawalpur) ;
  • Fatima Sadiq (Department of Biochemistry, Institute of Biochemistry, Biotechnology and Bioinformatics, The Islamia University of Bahawalpur) ;
  • Maria Aslam (Department of Computer Science, The Islamia University of Bahawalpur) ;
  • Umar Farooq (Department of Physiology and Biochemistry, Cholistan University of Veterinary and Animal Sciences) ;
  • Saadiya Zia (Department of Biochemistry, University of Agriculture) ;
  • Rawa Saad Aljaluod (Department of Botany and Microbiology, College of Science, King Saud University) ;
  • Khaloud Mohammed Alarjani (Department of Botany and Microbiology, College of Science, King Saud University)
  • Received : 2023.10.18
  • Accepted : 2024.01.28
  • Published : 2024.05.31
Download PDF
⟨ Previous Next ⟩

Abstract

Importance: Staphylococcus aureus and Escherichia coli contribute to global health challenges by forming biofilms, a key virulence element implicated in the pathogenesis of several infections. Objective: The study examined the efficacy of various generations of cephalosporins against biofilms developed by pathogenic S. aureus and E. coli. Methods: The development of biofilms by both bacteria was assessed using petri-plate and microplate methods. Biofilm hydrolysis and inhibition were tested using first to fourth generations of cephalosporins, and the effects were analyzed by crystal violet staining and phase contrast microscopy. Results: Both bacterial strains exhibited well-developed biofilms in petri-plate and microplate assays. Cefradine (first generation) showed 76.78% hydrolysis of S. aureus biofilm, while significant hydrolysis (59.86%) of E. coli biofilm was observed by cefipime (fourth generation). Similarly, cefuroxime, cefadroxil, cefepime, and cefradine caused 78.8%, 71.63%, 70.63%, and 70.51% inhibition of the S. aureus biofilms, respectively. In the case of E. coli, maximum biofilm inhibition (66.47%) was again shown by cefepime. All generations of cephalosporins were more effective against S. aureus than E. coli, which was confirmed by phase contrast microscopy. Conclusions and Relevance: Cephalosporins exhibit dual capabilities of hydrolyzing and inhibiting S. aureus and E. coli biofilms. First-generation cephalosporins exhibited the highest inhibitory activity against S. aureus, while the third and fourth generations significantly inhibited E. coli biofilms. This study highlights the importance of tailored antibiotic strategies based on the biofilm characteristics of specific bacterial strains.

Keywords

Acknowledgement

The authors extend their appreciation to the Researchers supporting project number (RSP2024R185) King Saud University, Riyadh, Saudi Arabia.

References

  1. Kong C, Chee CF, Richter K, Thomas N, Abd Rahman N, Nathan S. Suppression of Staphylococcus aureus biofilm formation and virulence by a benzimidazole derivative, UM-C162. Sci Rep. 2018;8(1):2758.
  2. Miao J, Lin S, Soteyome T, Peters BM, Li Y, Chen H, et al. Biofilm formation of Staphylococcus aureus under food heat processing conditions: first report on CML production within biofilm. Sci Rep. 2019;9(1):1312.
  3. Liu L, Ye C, Soteyome T, Zhao X, Xia J, Xu W, et al. Inhibitory effects of two types of food additives on biofilm formation by foodborne pathogens. Microbiologyopen. 2019;8(9):e00853.
  4. Karygianni L, Ren Z, Koo H, Thurnheer T. Biofilm matrixome: extracellular components in structured microbial communities. Trends Microbiol. 2020;28(8):668-681.
  5. Shaukat N, Farooq U, Akram K, Shafi A, Hayat Z, Naz A, et al. Antimicrobial potential of banana peel: a natural preservative to improve food safety. Asian J Agric Biol. 2023;(1):202003188.
  6. Fluit AC. Livestock-associated Staphylococcus aureus. Clin Microbiol Infect. 2012;18(8):735-744.
  7. Mora-Hernandez Y, Murguia V, Stinenbosch E, Jauregui PH, van Dijl JM, Buist G. Molecular typing and antimicrobial resistance profiling of 33 mastitis-related Staphylococcus aureus isolates from cows in the Comarca Lagunera region of Mexico. Sci Rep. 2021;11(1):6912.
  8. Haag AF, Fitzgerald JR, Penades JR. Staphylococcus aureus in animals. Microbiol Spectr. 2019;7(3).
  9. Hunduma D, Amenu K, Desta H, Grace D, Agga GE, Kerro Dego O. Prevalence and antimicrobial resistance of Escherichia coli O157:H7 and Salmonella, and the prevalence of Staphylococcus aureus in dairy cattle and camels under pastoral production system. Antibiotics (Basel). 2023;13(1):26.
  10. Pomwised R, Naknaen A, Surachat K, Issuriya A, Prochantasene S, Wiriyaprom R, Ngasaman R. Antibiotic-resistant Escherichia coli from goat farms and the potential treatment by Acalypha indica L. extract. Small Rum Res. 2023;219:106889.
  11. Smiet E, Grinwis GCM, van den Top JGB, Sloet van Oldruitenborgh-Oosterbaan MM. Equine mammary gland disease with a focus on botryomycosis: a review and case study. Equine Vet Educ. 2012;24(7):357-366.
  12. Lozano C, Gharsa H, Ben Slama K, Zarazaga M, Torres C. Staphylococcus aureus in animals and food: methicillin resistance, prevalence and population structure. A review in the African continent. Microorganisms. 2016;4(1):12.
  13. Ben Chehida F, Gharsa H, Tombari W, Selmi R, Khaldi S, Daaloul M, et al. First report of antimicrobial susceptibility and virulence gene characterization associated with Staphylococcus aureus carriage in healthy camels from Tunisia. Animals (Basel). 2021;11(9):2754.
  14. Latif A, Wadood A, Iqbal J, Syed Z, Durdana , Malik SS, et al. Prevalence of multiple drug resistance among avian pathogenic E. coli isolates from commercial poultry. Pak-Euro J Med life Sci. 2019;2(4):83-88.
  15. Rasheed MB, Ahsan A, Irshad H, Shahzad MA, Usman M, Riaz A, et al. Occurrence of Shiga toxin-producing E. coli in zoo animals of Rawalpindi and Islamabad zoos. Asian J Agric Biol. 2023;(2):2022080.
  16. Omwenga EO, Hensel A, Shitandi A, Goycoolea FM. Chitosan nanoencapsulation of flavonoids enhances their quorum sensing and biofilm formation inhibitory activities against an E.coli top 10 biosensor. Colloids Surf B Biointerfaces. 2018;164:125-133.
  17. Billings N, Millan M, Caldara M, Rusconi R, Tarasova Y, Stocker R, et al. The extracellular matrix component Psl provides fast-acting antibiotic defense in Pseudomonas aeruginosa biofilms. PLoS Pathog. 2013;9(8):e1003526.
  18. Tote K, Horemans T, Vanden Berghe D, Maes L, Cos P. Inhibitory effect of biocides on the viable masses and matrices of Staphylococcus aureus and Pseudomonas aeruginosa biofilms. Appl Environ Microbiol. 2010;76(10):3135-3142.
  19. Pinto RM, Soares FA, Reis S, Nunes C, Van Dijck P. Innovative strategies toward the disassembly of the EPS matrix in bacterial biofilms. Front Microbiol. 2020;11:952.
  20. Archer NK, Mazaitis MJ, Costerton JW, Leid JG, Powers ME, Shirtliff ME. Staphylococcus aureus biofilms: properties, regulation, and roles in human disease. Virulence. 2011;2(5):445-459.
  21. Chattopadhyay MK. Use of antibiotics as feed additives: a burning question. Front Microbiol. 2014;5:334.
  22. Dutta TK, Yadav SK, Chatterjee A. Antibiotics as feed additives for livestock: human health concerns. Indian J Anim Health. 2019;58(2):121-136.
  23. Chen X, Thomsen TR, Winkler H, Xu Y. Influence of biofilm growth age, media, antibiotic concentration and exposure time on Staphylococcus aureus and Pseudomonas aeruginosa biofilm removal in vitro. BMC Microbiol. 2020;20(1):264.
  24. Karlowsky JA, Hackel MA, Tsuji M, Yamano Y, Echols R, Sahm DF. In vitro activity of cefiderocol, a siderophore cephalosporin, against gram-negative bacilli isolated by clinical laboratories in North America and Europe in 2015-2016: SIDERO-WT-2015. Int J Antimicrob Agents. 2019;53(4):456-466.
  25. Shchelik IS, Gademann K. Synthesis and antimicrobial evaluation of new cephalosporin derivatives containing cyclic disulfide moieties. ACS Infect Dis. 2022;8(11):2327-2338.
  26. Ribeiro AR, Sures B, Schmidt TC. Cephalosporin antibiotics in the aquatic environment: a critical review of occurrence, fate, ecotoxicity and removal technologies. Environ Pollut. 2018;241:1153-1166.
  27. Iwase T, Uehara Y, Shinji H, Tajima A, Seo H, Takada K, et al. Staphylococcus epidermidis Esp inhibits Staphylococcus aureus biofilm formation and nasal colonization. Nature. 2010;465(7296):346-349.
  28. Shahid SA, Anwar F, Shahid M, Majeed N, Azam A, Bashir M, et al. Laser-assisted synthesis of Mn0. 50Zn0. 50Fe2O4 nanomaterial: characterization and in vitro inhibition activity towards Bacillus subtilis biofilm. J Nanomater. 2015;2015:896185.
  29. Eladawy M, El-Mowafy M, El-Sokkary MMA, Barwa R. Effects of lysozyme, proteinase K and cephalosporins on biofilm formation by clinical isolates of Pseudomonas aeruginosa. Interdiscip Perspect Infect Dis. 2020;2020:6156720.
  30. Aslam J, Shahzad MI, Ali HM, Ramzan M, Aleem MT, Minhas A, et al. A multidirectional phytochemical profiling, antimicrobial, antioxidant and toxicity studies of Neurada procumbens L.: a desert medicinal plant. J King Saud Uni Sci. 2023;35(8):102862.
  31. Aslam J, Shahzad MI, Ali HM, Dilbar GH, Ahmad FD, Locatelli M, et al. In vitro and in vivo anti-inflammatory potential of Octhochloa compressa extracts in carrageenan induced rats. Pak-Euro J Med Life Sci. 2021;4(4):265-274.
  32. Schilcher K, Horswill AR. Staphylococcal biofilm development: structure, regulation, and treatment strategies. Microbiol Mol Biol Rev. 2020;84(3):e00026-19.
  33. Nguyen HT, Nguyen TH, Otto M. The staphylococcal exopolysaccharide PIA - biosynthesis and role in biofilm formation, colonization, and infection. Comput Struct Biotechnol J. 2020;18:3324-3334.
  34. Kamble E, Pardesi K. Antibiotic tolerance in biofilm and stationery-phase planktonic cells of Staphylococcus aureus. Microb Drug Resist. 2021;27(1):3-12.
  35. Goel N, Fatima SW, Kumar S, Sinha R, Khare SK. Antimicrobial resistance in biofilms: exploring marine actinobacteria as a potential source of antibiotics and biofilm inhibitors. Biotechnol Rep (Amst). 2021;30:e00613.
  36. Liu Y, Zhang J, Ji Y. Environmental factors modulate biofilm formation by Staphylococcus aureus. Sci Prog. 2020;103(1):36850419898659.
  37. Vazquez-Munoz R, Meza-Villezcas A, Fournier PGJ, Soria-Castro E, Juarez-Moreno K, Gallego-Hernandez AL, et al. Enhancement of antibiotics antimicrobial activity due to the silver nanoparticles impact on the cell membrane. PLoS One. 2019;14(11):e0224904.
  38. Pfaller MA, Flamm RK, Mendes RE, Streit JM, Smart JI, Hamed KA, et al. Ceftobiprole activity against gram-positive and-negative pathogens collected from the United States in 2006 and 2016. Antimicrob Agents Chemother. 2018;63(1):e01566-18.
  39. Idrees M, Sawant S, Karodia N, Rahman A. Staphylococcus aureus biofilm: morphology, genetics, pathogenesis and treatment strategies. Int J Environ Res Public Health. 2021;18(14):7602.
  40. Teteneva NA, Mart'yanov SV, Esteban-Lopez M, Kahnt J, Glatter T, Netrusov AI, et al. Multiple drug-induced stress responses inhibit formation of Escherichia coli biofilms. Appl Environ Microbiol. 2020;86(21):e01113-e01120.