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Antibacterial Activity of Boron Compounds Against Biofilm-Forming Pathogens

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Abstract

This study aimed to evaluate the antibacterial activity of nine boron derivatives against biofilm-forming pathogenic bacteria. The effect of boron derivatives (CMB, calcium metaborate; SMTB, sodium metaborate tetrahydrate; ZB, zinc borate; STFB, sodium tetra fluorine borate; STB, sodium tetraborate; PTFB, potassium tetra fluor borate; APTB, ammonium pentabo-rate tetrahydrate; SPM, sodium perborate monohydrate; Borax, ATFB, ammonium tetra fluorine borate) on bacteria isolated from blood culture was determined by the minimum inhibitory concentration (MIC) method. Then, biofilm formation potentials on microplates, tubes, and Congo red agar were examined. The cytotoxicity of boron derivatives was determined by using WST-1-based methods. The interaction between the biofilm-forming bacteria, fibroblast cells, and boron derivatives was determined with the infection model. We found that the sodium metaborate tetrahydrate molecule was effective against all pathogens. According to the optical density values detected at 630 nm in microplates, meticillin-resistant Staphylococcus aureus was observed to have the most substantial biofilm ability at 0.257 nm. As a result of cytotoxicity studies, it has been determined that a 1 µg/L concentration of boron derivatives is not toxic to fibroblast L929 cells. In cell culture experiments, these boron derivatives have very serious inhibitory activity against biofilm-forming pathogens in a short treatment period, such as 2–4 h. Furthermore, using these molecules on inanimate surfaces affected by biofilms would be appropriate instead of living cells.

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Change history

  • 11 September 2023

    The original version of this article was updated to correct the correct tagging of the author name A. M. Abd El‑Aty.

References

  1. Kurutepe S, Srcol S, Gazi H et al (2007) Metisiline-dirençli ve duyarlı Staphylococcus aureus suşlarının antibiyotiklere direnç oranları. İnfeksiyon Derg 21:187–191

    Google Scholar 

  2. Chung DR, Song JH, Kim SH, Thamlikitkul V, Huang SG, Wang H et al (2011) High prevalence of multidrug-resistant nonfermenters in hospital-acquired pneumonia in Asia. Am J Respir Crit Care Med 184(12):1409–1417

    Article  PubMed  Google Scholar 

  3. Hill KE, Malic S, McKee R, Rennison T, Harding KG, Williams DW et al (2010) An in vitro model of chronic wound biofilms to test wound dressings and assess antimicrobial susceptibilities. J Antimicrob Chemother 65(6):1195–1206

    Article  CAS  PubMed  Google Scholar 

  4. Jamal M, Ahmad W, Andleeb S, Jalil F, Imran M, Nawaz MA et al (2018) Bacterial biofilm and associated infections. J Chin Med Assoc 81(1):7–11

    Article  PubMed  Google Scholar 

  5. Hall CW, Mah TF (2017) Molecular mechanisms of biofilm-based antibiotic resistance and tolerance in pathogenic bacteria. FEMS Microbiol Rev 41(3):276–301

    Article  CAS  PubMed  Google Scholar 

  6. Yarwood JM, Schlievert PM (2003) Quorum sensing in Staphylococcus infections. J Clin Invest 112(11):1620–1625

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Tran PL, Lowry N, Campbell T, Reid TW, Webster DR, Tobin E et al (2012) (2012) An organoselenium compound inhibits Staphylococcus aureus biofilms on hemodialysis catheters in vivo. Antimicrob Agents Chemother 56(2):972–8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Stefani S, Goglio A (2010) Methicillin-resistant Staphylococcus aureus: related infections and antibiotic resistance. Int J Infect Dis 14(4):S19-22

    Article  PubMed  Google Scholar 

  9. McCarthy H, Rudkin JK, Black NS, Gallagher L, O’Neill E, O’Gara JP (2015) Methicillin resistance and the biofilm phenotype in Staphylococcus aureus. Front Cell Infect Microbiol 5:1

    Article  PubMed  PubMed Central  Google Scholar 

  10. Stoodley P, Sauer K, Davies DG, Costerton JW (2002) Biofilms as complex differentiated communities. Annu Rev Microbiol 56:187–209

    Article  CAS  PubMed  Google Scholar 

  11. Scorei R (2012) Is boron a prebiotic element? A mini-review of the essentiality of boron for the appearance of life on earth. Orig Life Evol Biosph 42:3–17

    Article  CAS  PubMed  Google Scholar 

  12. Ali F, Hosmane NS, Zhu Y (2020) Boron chemistry for medical applications. Molecules 25:828

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Nielsen FH (2008) Is boron nutritionally relevant? Nutr Rev 66:183–191

    Article  PubMed  Google Scholar 

  14. Tombuloglu A, Copoglu H, Aydin-Son Y, Guray NT (2020) In vitro effects of boric acid on human liver hepatoma cell line (HepG2) at the half-maximal inhibitory concentration. J Trace Elem Med Bio 62:126573

    Article  CAS  Google Scholar 

  15. Wei Y, Yuan FJ, Zhou WB, Wu L, Chen L, Wang JJ, Zhang YS (2016) Borax-induced apoptosis in HepG2 cells involves p53, Bcl-2, and Bax. Genet Mol Res 21(2):15

    Google Scholar 

  16. Köse DA (2008) Preparation and structure investigation of biopotent boron compounds with hydroxy-functionalized organic molecules. Hacettepe University, Science Institute, Ankara

    Google Scholar 

  17. Zumreoglu-Karan B, Kose DA (2015) Boric acid: a simple molecule of physiologic, therapeutic and prebiotic significance. Pure Appl Chem 87:155–162

    Article  CAS  Google Scholar 

  18. Horan TC, Andrus M, Dudeck MA (2008) CDC/NHSN surveillance definition of health care-associated infection and criteria for specific types of infections in the acute care setting. Am J Infect Control 36(5):309–332

    Article  PubMed  Google Scholar 

  19. Ausubel FM, Brient R, Kingston RE, Moore DD, Seidman JG, Smith JA et al (1995) Short protocols in molecular biology, 2nd edn. John Willey & Sons, New York

    Google Scholar 

  20. Axtell JC, Saleh LMA, Qian EA, Wixtrom AI, Spokoyny AM (2018) Synthesis and applications of perfunctionalized boron clusters. Inorg Chem 57:2333–2350

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Qian EA, Wixtrom AI, Axtell JC, Saebi A, Jung D, Rehak P et al (2017) Atomically precise organomimetic cluster nanomolecules assembled via perfluoroaryl-thiol SNAr chemistry. Nat Chem 9:333–340

    Article  CAS  PubMed  Google Scholar 

  22. Hawthorne MF, Maderna A (1999) Applications of radiolabeled boron clusters to the diagnosis and treatment of cancer. Chem Rev 99:3421–3434

    Article  CAS  PubMed  Google Scholar 

  23. Ye J, Ma Y, Liu Q, Zhao DL, Wang QY, Zhang YX (2008) Regulation of Vibrio alginolyticus virulence by the LuxS quorum-sensing system. J Fish Dis 31(3):161–169

    Article  CAS  PubMed  Google Scholar 

  24. Nasr AR, AbuShady MH, Hussein SH (2012) Biofilm formation and presence of icaAD gene in clinical isolates of staphylococci. The Egyptian Journal of Medical Human Genetics 13:269–274

  25. Oliver A, Weigel M, Rasheed JK, Raney Jr MJE, P, Tenover FC, (2002) Mechanisms of decreased susceptibility to cefpodoxime in Escherichia coli. Antimicrob Agents Chemother 46(12):3829–3836

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Pagani L, Dell’Amico E, Migliavacca R et al (2003) Multiple CTX-M-type extended-spectrum β-lactamases in nosocomial iso-lates of Enterobacteriaceae from a hospital in Northern Italy. J Clin Microbiol 41(9):4264–4269

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Celebi D, Aydın E, Rakici E et al (2023) Evaluation of presence of clone ST131 and biofilm formation in ESBL producing and non-producing Escherichia coli strains. Mol Biol Rep. https://doi.org/10.1007/s11033-023-08532-z

    Article  PubMed  PubMed Central  Google Scholar 

  28. Turton JF, Baklan H, Siu LK, Kaufmann ME, Pitt TL (2008) Evaluation of a multiplex PCR for detection of serotypes K1, K2 and K5 in Klebsiella sp and comparison of isolates within these serotypes. FEMS Microbiol Lett 284(2):247–52

    Article  CAS  PubMed  Google Scholar 

  29. Yeh KM, Karup A, Siu LK et al (2007) Capsular serotype K1 or K2, rather than magA and rmpA, is a major virulece determinant for Klebsiella pneumoniae liver abscess in Singapore and Taiwan. J Clin Microbiol 45(2):466–71

    Article  CAS  PubMed  Google Scholar 

  30. Mamlouk K, Boubaker IBB, Gautier V et al (2006) Emergence and outbreaks of CTX-M -lactamase-producing Escherichia coli and Klebsiella pneumoniae strains in a Tunisian hospital. J Clin Microbiol 44(11):4049–4056

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. El Fertas-Aissani R, Messai Y, Alouache S, Bakour R (2013) Virulence profiles and antibiotic susceptibility patterns of Klebsiella pneumoniae strains isolated from different clinical specimens. Pathol Biol (Paris) 61(5):209–216

    Article  PubMed  Google Scholar 

  32. Xu M, Fu Y, Fang Y, Xu H, Kong H, Liu Y (2019) High prevalence of KPC-2-producing hypervirulent Klebsiella pneumoniae causing meningitis in Eastern China. Infect Drug Resist 12:641

    Article  PubMed  PubMed Central  Google Scholar 

  33. Czajkowska J, Junka A, Hoppe J, Toporkiewicz M, Pawlak A, Migdal P et al (2021) The co-culture of Staphylococcal biofilm and fibroblast cell line: the correlation of biological phenomena with metabolic NMR (1) footprint. Int J Mol Sci 22:11

    Article  Google Scholar 

  34. Peleg AY, Hooper DC (2010) Hospital-acquired infections due to gram-negative bacteria. N Engl J Med 362(19):1804–1813

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Cha JO, Yoo JI, Yoo JS, Chung HS, Park SH, Kim HS et al (2013) Investigation of biofilm formation and its association with the molecular and clinical characteristics of methicillin-resistant Staphylococcus aureus. Osong Public Health Res Perspect 4(5):225–232

    Article  PubMed  PubMed Central  Google Scholar 

  36. Altınöz AA, Öksüz Ş, Şahin I, Öztürk C, Avcıoğlu F (2013) Kan kültürlerinden izole edilen Staphylococcus aureus suşlarında antibiyotiklere direnç. ANKEM Derg 27:60–3

    Google Scholar 

  37. Güngör S, Karaayak UB, Gül YS, Baran N (2012) Kan kültürlerinden izole edilen Staphylococcus aureus suşlarında antibiyotiklere direnç. ANKEM Derg 26:171–175

    Google Scholar 

  38. Turhanoglu M, Koyuncu E, Bayındır BF, Onur A, Tekay F (2016) Evaluation of the results obtained from microbiological analysis of blood cultures over 5 years. J Fam Med Health Care 2:43–50

    Article  Google Scholar 

  39. Çetin F, Mumcuoğlu I, Aksoy A, Gürkan Y, Aksu N (2014) Kan kültürlerinden izole edilen mikroorganizmalar ve antimikrobiyal duyarlılıkları. Turk Hij Den Biyol Derg 71:67–74

    Google Scholar 

  40. Loonen AJ, Wolffs PF, Bruggeman CA, van den Brule AJ (2014) Developments for improved diagnosis of bacterial bloodstream infections. Eur J Clin Microbiol Infect Dis 33(10):1687–1702

    Article  CAS  PubMed  Google Scholar 

  41. Mitgang EA, Hartley DM, Malchione MD, Koch M, Goodman JL (2018) Review and mapping of carbapenem-resistant Enterobacteriaceae in Africa: using diverse data to inform surveillance gaps. Int J Antimicrob Agents 52(3):372–384

    Article  CAS  PubMed  Google Scholar 

  42. Corbella M, Mariani B, Ferrari C, Comandatore F, Scaltriti E, Marone P, Cambieri P (2017) Three cases of mcr-1-positive colistin-resistant Escherichia coli bloodstream infections in Italy, August 2016 to January 2017. Euro Surveill 22(16):30517. https://doi.org/10.2807/1560-7917.ES.2017.22.16.30517

  43. Koldemir-Gündüz M, Aydin HE, Berikten D, Kaymak G, Köse DA, Arslantaş A (2021) Synthesis of new boron derived compounds; anticancer, antioxidant and antimicrobial effect in vitro glioblastoma tumor model. J Korean Neurosurg Soc 64(6):864–872

    Article  PubMed  PubMed Central  Google Scholar 

  44. Koldemir-Gündüz M, Bolat M, Kaymak G, Berikten D, Köse DA (2022) Therapeutic effects of newly synthesized boron compounds (BGM and BGD) on hepatocellular Carcinoma. Biol Trace Elem Res 200(1):134–146

    Article  Google Scholar 

  45. Ni N, Li M, Wang J, Wang B (2009) Inhibitors and antagonists of bacterial quorum sensing. Med Res Rev 29(1):65–124

    Article  CAS  PubMed  Google Scholar 

  46. Zan R, Hubbezoglu I, Sumer Z, Tunc T, Tanalp J (2013) Antibacterial effects of two different types of laser and aqueous ozone against Enterococcus faecalis in root canals. Photomed Laser Surg 31(4):150–154

    Article  CAS  PubMed  Google Scholar 

  47. Pointer BR, Boyer MP, Schmidt M (2015) Boric acid destabilizes the hyphal cytoskeleton and inhibits invasive growth of Candida albicans. Yeast 32(4):389–398. https://doi.org/10.1002/yea.306681

    Article  CAS  PubMed  Google Scholar 

  48. Ahmad S, Haque MM, Ashraf SM, Ahmad S (2004) Urethane modified boron filled polyesteramide: a novel anti-microbial polymer from a sustainable resource. Eur Polym J 40:2097–2104

    Article  CAS  Google Scholar 

  49. Yılmaz MT (2012) Minimum inhibitory and minimum bactericidal concentrations of boron compounds against several bacterial strains. Turk J Med Sci 42(2):1423–1429

    Google Scholar 

  50. Sarac N, Ugur A, Boran R, Elgin ES (2015) The use of boron compounds for stabilization of lipase from Pseudomonas aeruginosa ES3 for the detergent industry. J Surfactants Deterg 18(2):275–285

    Article  CAS  Google Scholar 

  51. Sayin Z, Ucan US, Sakmanoglu A (2016) Antibacterial and antibiofilm effects of boron on different bacteria. Biol Trace Elem Res 173:241–246

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors want to thank all the participants.

Funding

This research received no specific grant from any funding agency in the public, commercial or not-for-profit sectors.

Author information

Authors and Affiliations

  1. Department of Medical Microbiology, Faculty of Medicine, Ataturk University, 25240, Erzurum, Turkey

    Ozgur Celebi & Sumeyye Baser

  2. Department of Microbiology, Faculty of Veterinary Medicine, Ataturk University, 25240, Erzurum, Turkey

    Demet Celebi

  3. Ataturk University Vaccine Application and Development Center, Ataturk University, 25240, Erzurum, Turkey

    Demet Celebi

  4. Vocational School of Health Services, Kütahya Health Sciences University, Kütahya, Turkey

    Elif Aydın

  5. Department of Medical Microbiology, Faculty of Medicine, Recep Tayyip Erdogan University, 53020, Rize, Turkey

    Erva Rakıcı

  6. Department of Field Crops, Faculty of Agriculture and Natural Science, Duzce University, 81620, Düzce, Turkey

    Serpil Uğraş

  7. Traditional and Complementary Medicine Applied and Research Center, Duzce University, Duzce, Turkey

    Pınar Ağyar Yoldaş

  8. Department of Biochemistry, Faculty of Pharmacy, Ataturk University, 25240, Erzurum, Turkey

    Nurcan Kılıç Baygutalp

  9. Department of Medical Pharmacology, Faculty of Medicine, Ataturk University, 25240, Erzurum, Turkey

    A. M. Abd El-Aty

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Contributions

All the authors contributed to the study conception and design.

All authors: OC, DC, SB, EA, ER, SU, PAY, NB, AMA contributed to the development of the study methodology, data collection and analysis. All authors participated in writing, reviewing and editing the manuscript, and approved the final version.

Corresponding author

Correspondence to Elif Aydın.

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Ethical Considerations

The study was approved by the local institutional ethical board (University Non-

Interventional Clinical Research Ethics Committee; File number: 2018/11).

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- The authors declare that the proposed manuscript describes original research and is not published or under consideration by another scientific journal.

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Celebi, O., Celebi, D., Baser, S. et al. Antibacterial Activity of Boron Compounds Against Biofilm-Forming Pathogens. Biol Trace Elem Res 202, 346–359 (2024). https://doi.org/10.1007/s12011-023-03768-z

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