Skip to main content

Advertisement

SpringerLink
Log in

Antibacterial effect of bismuth subsalicylate nanoparticles synthesized by laser ablation

  • Research Paper
  • Published:
Journal of Nanoparticle Research Aims and scope Submit manuscript

Abstract

The antimicrobial properties of bismuth subsalicylate (BSS) nanoparticles against four opportunistic pathogens; E. coli, P. aeruginosa, S. aureus, and S. epidermidis were determined. BSS nanoparticles were synthesized by pulse laser ablation of a solid target in distilled water under different conditions. The nanoparticles were characterized using high-resolution transmission electron microscopy and absorption spectra and small angle X-ray scattering. The analysis shows that the colloids maintained the BSS structure and presented average particle size between 20 and 60 nm, while the concentration ranges from 95 to 195 mg/L. The antibacterial effect was reported as the inhibition ratio of the bacterial growth after 24 h and the cell viability was measured using the XTT assay. The results showed that the inhibition ratio of E. coli and S. epidermidis was dependant on the NPs size and/or concentration, meanwhile P. aeruginosa and S. aureus were more sensitive to the BSS nanoparticles independently of both the size and the concentration. In general, the BSS colloids with average particle size of 20 nm were the most effective, attaining inhibition ratios >80 %, similar or larger than those obtained with the antibiotic used as control. The results suggest that the BSS colloids could be used as effective antibacterial agents with potential applications in the medical area.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Adams CP, Walker KA, Obare SO, Docherty KM (2014) Size-dependent antimicrobial effects of novel palladium nanoparticles. PLoS ONE 9:e85981. doi:10.1371/journal.pone.0085981

    Article  Google Scholar 

  • Alipour M, Dorval C, Suntres ZE, Omri A (2011) Bismuth-ethanedithiol incorporated in a liposome-loaded tobramycin formulation modulates the alginate levels in mucoid Pseudomonas aeruginosa. J Pharm Pharmacol 63:999–1007. doi:10.1111/j.2042-7158.2011.01304.x

    Article  Google Scholar 

  • Andreasen JJ, Andersen LP (1987) In vitro susceptibility of Campylobacter pyloridis to cimetidine, sucralfate, bismuth and sixteen antibiotics. Acta Pathologica, Microbiologica, et Immunologica Scandinavica Sect B 95:147–149

    Google Scholar 

  • Andrews PC, Deacon GB, Forsyth CM, Junk PC, Kumar I, Maguire M (2006) Towards a structural understanding of the anti-ulcer and anti-gastritis drug bismuth subsalicylate. Angew Chem 45:5638–5642. doi:10.1002/anie.200600469

    Article  Google Scholar 

  • Bera RK, Mandal SM, Raj CR (2014) Antimicrobial activity of fluorescent Ag nanoparticles. Lett Appl Microbiol 58:520–526. doi:10.1111/lam.12222

    Article  Google Scholar 

  • Botequim D, Maia J, Lino MM, Lopes LM, Simoes PN, Ilharco LM, Ferreira L (2012) Nanoparticles and surfaces presenting antifungal, antibacterial and antiviral properties. Langmuir 28:7646–7656. doi:10.1021/la300948n

    Article  Google Scholar 

  • Brogan AP, Verghese J, Widger WR, Kohn H (2005) Bismuth-dithiol inhibition of the Escherichia coli rho transcription termination factor. J Inorg Biochem 99:841–851. doi:10.1016/j.jinorgbio.2004.12.019

    Article  Google Scholar 

  • Cornick NA, Silva M, Gorbach SL (1990) In vitro antibacterial activity of bismuth subsalicylate. Rev Infect Dis 12(Suppl 1):S9–S10

    Article  Google Scholar 

  • Cremet L et al (2015) Pathogenic potential of Escherichia coli clinical strains from orthopedic implant infections towards human osteoblastic cells. Pathog Dis. doi:10.1093/femspd/ftv065

    Google Scholar 

  • Delchier JC, Malfertheiner P, Thieroff-Ekerdt R (2014) Use of a combination formulation of bismuth, metronidazole and tetracycline with omeprazole as a rescue therapy for eradication of Helicobacter pylori. Aliment Pharmacol Therap 40:171–177. doi:10.1111/apt.12808

    Article  Google Scholar 

  • dos Santos CA et al (2014) Silver nanoparticles: therapeutical uses, toxicity, and safety issues. J Pharma Sci 103:1931–1944. doi:10.1002/jps.24001

    Article  Google Scholar 

  • DuPont HL (1987) Bismuth subsalicylate in the treatment and prevention of diarrheal disease. Drug Intell Clin Pharm 21:687–693

    Google Scholar 

  • DuPont HL, Sullivan P, Pickering LK, Haynes G, Ackerman PB (1977) Symptomatic treatment of diarrhea with bismuth subsalicylate among students attending a Mexican university. Gastroenterology 73:715–718

    Google Scholar 

  • Elmi F et al (2014) The use of antibacterial activity of ZnO nanoparticles in the treatment of municipal wastewater. Water Sci Technol 70:763–770. doi:10.2166/wst.2014.232

    Article  Google Scholar 

  • Ericsson CD, Evans DG, DuPont HL, Evans DJ Jr, Pickering LK (1977) Bismuth subsalicylate inhibits activity of crude toxins of Escherichia coli and Vibrio cholerae. J Infect Dis 136:693–696

    Article  Google Scholar 

  • Fayaz AM, Balaji K, Girilal M, Yadav R, Kalaichelvan PT, Venketesan R (2010) Biogenic synthesis of silver nanoparticles and their synergistic effect with antibiotics: a study against gram-positive and Gram-negative bacteria. Nanomed-Nanotechnol 6:103–109

    Article  Google Scholar 

  • Feris K et al (2010) Electrostatic interactions affect nanoparticle-mediated toxicity to Gram-negative bacterium Pseudomonas aeruginosa PAO1. Langmuir 26:4429–4436

    Article  Google Scholar 

  • Ge R, Chen Z, Zhou Q (2012) The actions of bismuth in the treatment of Helicobacter pylori infections: an update. Metallomics 4:239–243. doi:10.1039/c2mt00180b

    Article  Google Scholar 

  • Goodman CM, McCusker CD, Yilmaz T, Rotello VM (2004) Toxicity of gold nanoparticles functionalized with cationic and anionic side chains. Bioconjugate Chem 15:897–900. doi:10.1021/bc049951i

    Article  Google Scholar 

  • Hajipour MJ et al (2012) Antibacterial properties of nanoparticles. Trends Biotechnol 30:499–511. doi:10.1016/j.tibtech.2012.06.004

    Article  Google Scholar 

  • Harris LG, Foster SJ, Richards RG (2002) An introduction to Staphylococcus aureus, and techniques for identifying and quantifying S. aureus adhesins in relation to adhesion to biomaterials: review. Eur Cell Mater 4:39–60

    Google Scholar 

  • Hernandez L, Vazquez B, Lopez-Bravo A, Parra J, Goni I, Gurruchaga M (2007) Acrylic bone cements with bismuth salicylate: behavior in simulated physiological conditions. J Biomed Mater Res, Part A 80:321–332. doi:10.1002/jbm.a.30947

    Article  Google Scholar 

  • Hernandez-Delgadillo R, Velasco-Arias D, Diaz D, Arevalo-Nino K, Garza-Enriquez M, De la Garza-Ramos MA, Cabral-Romero C (2012) Zerovalent bismuth nanoparticles inhibit Streptococcus mutans growth and formation of biofilm. Int J Nanomed 7:2109–2113. doi:10.2147/IJN.S29854

    Google Scholar 

  • Hernandez-Delgadillo R, Velasco-Arias D, Martinez-Sanmiguel JJ, Diaz D, Zumeta-Dube I, Arevalo-Nino K, Cabral-Romero C (2013) Bismuth oxide aqueous colloidal nanoparticles inhibit Candida albicans growth and biofilm formation. Int J Nanomed 8:1645–1652. doi:10.2147/IJN.S38708

    Google Scholar 

  • Huh AJ, Kwon YJ (2011) “Nanoantibiotics”: a new paradigm for treating infectious diseases using nanomaterials in the antibiotics resistant era. J Control Release 156:128–145. doi:10.1016/j.jconrel.2011.07.002

    Article  Google Scholar 

  • Jiang W, Mashayekhi H, Xing BS (2009) Bacterial toxicity comparison between nano- and micro-scaled oxide particles. Environ Pollut 157:1619–1625

    Article  Google Scholar 

  • Khan SS, Mukherjee A, Chandrasekaran N (2011) Studies on interaction of colloidal silver nanoparticles (SNPs) with five different bacterial species. Colloid Surf B 87:129–138

    Article  Google Scholar 

  • Kim EC, Lee BC, Chang HS, Lee W, Hong CU, Min KS (2008) Evaluation of the radiopacity and cytotoxicity of Portland cements containing bismuth oxide. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 105:e54–e57. doi:10.1016/j.tripleo.2007.08.001

    Article  Google Scholar 

  • Kim SH, Tramontina VA, Papalexiou V, Luczsyzyn SM, De Lima AA, do Prado AM (2012) Bismuth subgallate as a topical haemostatic agent at the palatal wounds: a histologic study in dogs. Int J Oral Maxillofac Surg 41:239–243. doi:10.1016/j.ijom.2011.12.002

    Article  Google Scholar 

  • Lipovsky A, Gedanken A, Nitzan Y, Lubart R (2011) Enhanced inactivation of bacteria by metal-oxide nanoparticles combined with visible light irradiation. Lasers Surg Med 43:236–240. doi:10.1002/lsm.21033

    Article  Google Scholar 

  • Luo Y, Hossain M, Wang CM, Qiao Y, An JC, Ma LY, Su M (2013) Targeted nanoparticles for enhanced X-ray radiation killing of multidrug-resistant bacteria. Nanoscale 5:687–694

    Article  Google Scholar 

  • Mahony DE, Woods A, Eelman MD, Burford N, Veldhuyzen van Zanten SJ (2005) Interaction of bismuth subsalicylate with fruit juices, ascorbic acid, and thiol-containing substrates to produce soluble bismuth products active against Clostridium difficile. Antimicrob Agents Chemother 49:431–433. doi:10.1128/AAC.49.1.431-433.2005

    Article  Google Scholar 

  • Manhart MD (1990) In vitro antimicrobial activity of bismuth subsalicylate and other bismuth salts. Rev Infect Dis 12(Suppl 1):S11–S15

    Article  Google Scholar 

  • Markowska K, Grudniak AM, Wolska KI (2013) Silver nanoparticles as an alternative strategy against bacterial biofilms. Acta Biochim Pol 60:523–530

    Google Scholar 

  • Mijnendonckx K, Leys N, Mahillon J, Silver S, Van Houdt R (2013) Antimicrobial silver: uses, toxicity and potential for resistance. Biometals 26:609–621. doi:10.1007/s10534-013-9645-z

    Article  Google Scholar 

  • Morones JR, Elechiguerra JL, Camacho A, Holt K, Kouri JB, Ramirez JT, Yacaman MJ (2005) The bactericidal effect of silver nanoparticles. Nanotechnology 16:2346–2353

    Article  Google Scholar 

  • Nazari P et al (2014) The antimicrobial effects and metabolomic footprinting of carboxyl-capped bismuth nanoparticles against Helicobacter pylori. Appl Biochem Biotechnol 172:570–579. doi:10.1007/s12010-013-0571-x

    Article  Google Scholar 

  • Pacifico L, Osborn JF, Anania C, Vaira D, Olivero E, Chiesa C (2012) Review article: bismuth-based therapy for Helicobacter pylori eradication in children. Aliment Pharmacol Ther. doi:10.1111/j.1365-2036.2012.05055.x

    Google Scholar 

  • Palanikumar L, Ramasamy SN, Balachandran C (2014) Size-dependent antimicrobial response of zinc oxide nanoparticles. IET Nanobiotechnol 8:111–117. doi:10.1049/iet-nbt.2012.0008

    Article  Google Scholar 

  • Pardo OA, Pardo Castello V (1952) The treatment of early syphilis with penicillin and bismuth subsalicylate; follow-up report. Am J Syph Gonorrhea Vener Dis 36:342–345

    Google Scholar 

  • Purvis JE (1926) CV.: the absorption spectra of various derivatives of salicylic acid. J Chem Soc 48:775–778

    Article  Google Scholar 

  • Purvis JE (1927) The absorption spectra of various alkaloids and their salicylates and of derivatives of salicylic acid. J Chem Soc:2715-2719

  • Riool M et al (2014) Staphylococcus epidermidis originating from titanium implants infects surrounding tissue and immune cells. Acta Biomater 10:5202–5212. doi:10.1016/j.actbio.2014.08.012

    Article  Google Scholar 

  • Rispoli F, Angelov A, Badia D, Kumar A, Seal S, Shah V (2010) Understanding the toxicity of aggregated zero valent copper nanoparticles against Escherichia coli. J Hazard Mater 180:212–216. doi:10.1016/j.jhazmat.2010.04.016

    Article  Google Scholar 

  • Roy A, Gauri SS, Bhattacharya M, Bhattacharya J (2013) Antimicrobial activity of CaO nanoparticles. J Biomed Nanotechnol 9:1570–1578

    Article  Google Scholar 

  • Rybtke M, Hultqvist LD, Givskov M, Tolker-Nielsen T (2015) Pseudomonas aeruginosa biofilm infections: community structure, antimicrobial tolerance and immune response. J Mol Biol. doi:10.1016/j.jmb.2015.08.016

    Google Scholar 

  • Schaller M, Laude J, Bodewaldt H, Hamm G, Korting HC (2004) Toxicity and antimicrobial activity of a hydrocolloid dressing containing silver particles in an ex vivo model of cutaneous infection. Skin Pharmacol Physiol 17:31–36. doi:10.1159/000074060

    Article  Google Scholar 

  • Serena T et al (2007) Bismuth subgallate/borneol (suile) is superior to bacitracin in the human forearm biopsy model for acute wound healing. Adv Skin Wound Care 20:485–492. doi:10.1097/01.ASW.0000288208.85807.b8

    Article  Google Scholar 

  • Shaikh AR, Giridhar R, Yadav MR (2007) Bismuth-norfloxacin complex: synthesis, physicochemical and antimicrobial evaluation. Int J Pharm 332:24–30. doi:10.1016/j.ijpharm.2006.11.037

    Article  Google Scholar 

  • Slikkerveer A, de Wolff FA (1989) Pharmacokinetics and toxicity of bismuth compounds. Med Toxicol Advers Drug Exp 4:303–323

    Article  Google Scholar 

  • Sox TE, Olson CA (1989) Binding and killing of bacteria by bismuth subsalicylate. Antimicrob Agents Chemother 33:2075–2082

    Article  Google Scholar 

  • Steinhoff MC, Douglas RG Jr, Greenberg HB, Callahan DR (1980) Bismuth subsalicylate therapy of viral gastroenteritis. Gastroenterology 78:1495–1499

    Google Scholar 

  • Tillman LA, Drake FM, Dixon JS, Wood JR (1996) Review article: safety of bismuth in the treatment of gastrointestinal diseases. Aliment Pharmacol Therap 10:459–467

    Article  Google Scholar 

  • Tomita RJ, de Matos RA, Vallim MA, Courrol LC (2014) A simple and effective method to synthesize fluorescent nanoparticles using tryptophan and light and their lethal effect against bacteria. J Photochem Photobiol, B 140C:157–162. doi:10.1016/j.jphotobiol.2014.07.015

    Article  Google Scholar 

  • Tramontina VA, Machado MA, Nogueira Filho Gda R, Kim SH, Vizzioli MR, Toledo S (2002) Effect of bismuth subgallate (local hemostatic agent) on wound healing in rats. Histol Histometric Find Braz Dent J 13:11–16

    Google Scholar 

  • Tsuang YH, Sun JS, Huang YC, Lu CH, Chang WHS, Wang CC (2008) Studies of photokilling of bacteria using titanium dioxide nanoparticles. Artif Organs 32:167–174

    Article  Google Scholar 

  • Wang ZP, Lee YH, Wu B, Horst A, Kang YS, Tang YJJ, Chen DR (2010) Anti-microbial activities of aerosolized transition metal oxide nanoparticles. Chemosphere 80:525–529

    Article  Google Scholar 

  • Weir E, Lawlor A, Whelan A, Regan F (2008) The use of nanoparticles in anti-microbial materials and their characterization. Analyst 133:835–845. doi:10.1039/b715532h

    Article  Google Scholar 

  • Yang G (2012) Laser ablation in liquids: principles and applications in the preparation of nanomaterials. Pan Stanford Publishing Pte Ltd, Boston

    Book  Google Scholar 

  • Zhang LL, Jiang YH, Ding YL, Povey M, York D (2007) Investigation into the antibacterial behaviour of suspensions of ZnO nanoparticles (ZnO nanofluids). J Nanopart Res 9:479–489

    Article  Google Scholar 

Download references

Acknowledgements

The authors thank María de Jesús Salinas Nájera and Hermilo Zarco for their technical assistance. Supported by DGAPA-PAPIIT #IN18814, #IN118914, and CONACYT 152995 grants.

Author information

Authors and Affiliations

  1. Instituto Nacional de Investigaciones Nucleares, Apdo. Postal 18-1027, CP 11801, Mexico, D. F., Mexico

    Mariela Flores-Castañeda, Enrique Camps & Mario Pérez

  2. Facultad de Odontología, DEPeI, I, Universidad Nacional Autónoma de México, Circuito exterior s/n, Ciudad Universitaria, CP 04510, Mexico, D. F., Mexico

    Alejandro L. Vega-Jiménez & Argelia Almaguer-Flores

  3. Unidad de Ingeniería de Tejidos, Terapia Celular y Medicina Regenerativa, Instituto Nacional de Rehabilitación, Calz. México-Xochimilco No. 289, Col. Arenal de Guadalupe, CP 14389, Mexico, D. F., Mexico

    Phaedra Silva-Bermudez

  4. FarmaQuimia SA de CV., Ampere No. 11, Parque Industrial Cuamatla, CP 54730, Cuautitlan Izcalli, Estado de México, Mexico

    Edgardo Berea

  5. Instituto de Investigaciones en Materiales, Universidad Nacional Autónoma de México, Circuito exterior s/n, Ciudad Universitaria, CP 04510, Mexico, D. F., Mexico

    Sandra E. Rodil

Authors
  1. Mariela Flores-Castañeda
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alejandro L. Vega-Jiménez
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Argelia Almaguer-Flores
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Enrique Camps
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mario Pérez
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Phaedra Silva-Bermudez
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Edgardo Berea
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Sandra E. Rodil
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alejandro L. Vega-Jiménez.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Flores-Castañeda, M., Vega-Jiménez, A.L., Almaguer-Flores, A. et al. Antibacterial effect of bismuth subsalicylate nanoparticles synthesized by laser ablation. J Nanopart Res 17, 431 (2015). https://doi.org/10.1007/s11051-015-3237-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11051-015-3237-5

Keywords

Search

Navigation