Skip to main content
SpringerLink
Log in

Antibacterial mechanism and activity of cerium oxide nanoparticles

氧化铈纳米粒子的抗菌机理及应用

  • Reviews
  • Published:
Science China Materials Aims and scope Submit manuscript

Abstract

Nanomaterials have been applied as antibacterial agents by virtue of their unique functioning mechanism different from that of conventional antibiotics. Cerium oxide nanoparticles (CeO2 NPs) are important antibacterial agents due to their relatively low toxicity to normal cells and their distinct antibacterial mechanism based on the reversible conversion between two valence states of Ce(III)/Ce (IV). Some studies have been conducted to explore their antibacterial activities; however, systematic research reviews on the related mechanisms and influencing factors are still quite rare. In this review, we discuss the plausible mechanisms of the antibacterial activity of CeO2 NPs, analyze different influencing factors, and summarize various research reports on antibacterial effects on E. coli and S. aureus. We also propose the potential applications and prospects, and hope to provide an in-depth understanding on the antibacterial mechanism and a better guidance to the design and applications of this promising antibacterial material in the future.

摘要

纳米材料因其特殊的抗菌机理, 在抗菌领域得到了广泛应 用. 氧化铈纳米粒子是重要的抗菌材料之一, 具有对正常细胞毒性 低, 且抗菌机理基于可逆价态转化的优势. 目前已有许多关于氧化 铈纳米粒子抗菌活性的研究报道, 但系统性探究其抗菌机理的文 章则极为少见. 本文首先系统性地探究了氧化铈纳米粒子可能的 抗菌机理, 即静电相互作用在抗菌过程中发挥重要作用, 此外抗菌 过程还伴随活性氧物种的产生和纳米粒子对细菌的机械损伤. 其 次, 本文分析了氧化铈纳米粒子抗菌效果的影响因素, 并总结了不 同研究中氧化铈纳米粒子对大肠杆菌和金黄葡萄球菌的抗菌效果. 最后提出了氧化铈纳米粒子可能的应用前景. 本文将有利于对氧 化铈纳米粒子抗菌机理的深入理解, 并为该类材料在未来的设计 和应用提供借鉴.

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

Similar content being viewed by others

References

  1. Stryjewski ME, Corey GR. Methicillin-resistant staphylococcus aureus: An evolving pathogen. Clin Infect Dis, 2014, 58: S10–S19

    CAS  Google Scholar 

  2. Seil JT, Webster TJ. Antimicrobial applications of nanotechnology: methods and literature. Int J Nanomed, 2012, 7: 2767

    CAS  Google Scholar 

  3. Shrivastava S, Bera T, Roy A, et al. Characterization of enhanced antibacterial effects of novel silver nanoparticles. Nanotechnology, 2007, 18: 225103

    Google Scholar 

  4. Sondi I, Salopek-Sondi B. Silver nanoparticles as antimicrobial agent: A case study on E. coli as a model for Gram-negative bacteria. J Colloid Interface Sci, 2004, 275: 177–182

    CAS  Google Scholar 

  5. Stoimenov PK, Klinger RL, Marchin GL, et al. Metal oxide nanoparticles as bactericidal agents. Langmuir, 2002, 18: 6679–6686

    CAS  Google Scholar 

  6. Tran AX, Lester ME, Stead CM, et al. Resistance to the antimicrobial peptide polymyxin requires myristoylation of escherichia coli and salmonella typhimurium lipid A. J Biol Chem, 2005, 280: 28186–28194

    CAS  Google Scholar 

  7. Usman MS, El Zowalaty ME, Shameli K, et al. Synthesis, characterization, and antimicrobial properties of copper nanoparticles. Int J Nanomed, 2013, 8: 4467

    Google Scholar 

  8. Jones N, Ray B, Ranjit KT, et al. Antibacterial activity of ZnO nanoparticle suspensions on a broad spectrum of microorganisms. FEMS MicroBiol Lett, 2008, 279: 71–76

    CAS  Google Scholar 

  9. Cho M, Chung H, Choi W, et al. Linear correlation between inactivation of E. coli and OH radical concentration in TiO2 photocatalytic disinfection. Water Res, 2004, 38: 1069–1077

    CAS  Google Scholar 

  10. AshaRani PV, Low Kah Mun G, Hande MP, et al. Cytotoxicity and genotoxicity of silver nanoparticles in human cells. ACS Nano, 2008, 3: 279–290

    Google Scholar 

  11. Tarnuzzer RW, Colon J, Patil S, et al. Vacancy engineered ceria nanostructures for protection from radiation-induced cellular damage. Nano Lett, 2005, 5: 2573–2577

    CAS  Google Scholar 

  12. Tsai YY, Oca-Cossio J, Agering K, et al. Novel synthesis of cerium oxide nanoparticles for free radical scavenging. Nanomedicine, 2007, 2: 325–332

    CAS  Google Scholar 

  13. Park B, Donaldson K, Duffin R, et al. Hazard and risk assessment of a nanoparticulate cerium oxide-based diesel fuel additive—A case study. Inhalation Toxicol, 2008, 20: 547–566

    CAS  Google Scholar 

  14. De Marzi L, Monaco A, De Lapuente J, et al. Cytotoxicity and genotoxicity of ceria nanoparticles on different cell lines in vitro. Int J Mol Sci, 2013, 14: 3065–3077

    Google Scholar 

  15. Ingle AP, Duran N, Rai M. Bioactivity, mechanism of action, and cytotoxicity of copper-based nanoparticles: A review. Appl Microbiol Biotechnol, 2014, 98: 1001–1009

    CAS  Google Scholar 

  16. Chen BH, Suresh Babu K, Anandkumar M, et al. Cytotoxicity and antibacterial activity of gold-supported cerium oxide nanoparticles. Int J Nanomed, 2014, 9: 5515

    Google Scholar 

  17. Sun C, Li H, Chen L. Nanostructured ceria-based materials: Synthesis, properties, and applications. Energy Environ Sci, 2012, 5: 8475

    CAS  Google Scholar 

  18. Wang X, Jiang Z, Zheng B, et al. Synthesis and shape-dependent catalytic properties of CeO2 nanocubes and truncated octahedra. CrystEngComm, 2012, 14: 7579–7582

    CAS  Google Scholar 

  19. Wang Y, Liu R, LüG M, et al. Ceria nanostructures and their catalytic applications. J Chin Rare Earth Soc, 2014, 32: 257

    CAS  Google Scholar 

  20. Xing S, Yu S, Deng Y, et al. Effect of cerium on abrasive wear behaviour of hardfacing alloy. J Rare Earths, 2012, 30: 69–73

    CAS  Google Scholar 

  21. Feng X, Sayle DC, Wang ZL, et al. Converting ceria polyhedral nanoparticles into single-crystal nanospheres. Science, 2006, 312: 1504–1508

    CAS  Google Scholar 

  22. Yahiro H. High temperature fuel cell with ceria-yttria solid electrolyte. J Electrochem Soc, 1988, 135: 2077

    CAS  Google Scholar 

  23. Atkinson A, Barnett S, Gorte RJ, et al. Advanced Anodes for High-Temperature Fuel Cells. Materials for Sustainable Energy: A Collection of Peer-Reviewed Research and Review Articles from Nature Publishing Group. Singapore: World Scientific, 2010, 213–223

    Google Scholar 

  24. Lv GM, Wang YJ, Liu R, et al. The application of nanoceria in the bio-antioxidation. Sci Sin Chim, 2013, 43: 1309–1321

    Google Scholar 

  25. Li R. Synthesis and UV-shielding properties of ZnO- and CaO-doped CeO2 via soft solution chemical process. Solid State Ion, 2002, 151: 235–241

    CAS  Google Scholar 

  26. Hirst SM, Karakoti AS, Tyler RD, et al. Anti-inflammatory properties of cerium oxide nanoparticles. Small, 2009, 5: 2848–2856

    CAS  Google Scholar 

  27. Trovarelli A, Fornasiero P. Catalysis by Ceria and Related Materials. Singapore: World Scientific, 2013

    Google Scholar 

  28. Blank JH, Beckers J, Collignon PF, et al. Redox kinetics of ceria-based mixed oxides in selective hydrogen combustion. Chem-PhysChem, 2007, 8: 2490–2497

    CAS  Google Scholar 

  29. Chen HT, Choi YM, Liu M, et al. A theoretical study of surface reduction mechanisms of CeO2 (111) and (110) by H2. Chem-PhysChem, 2007, 8: 849–855

    CAS  Google Scholar 

  30. Mo L, Zheng X, Yeh CT. A novel CeO2/ZnO catalyst for hydrogen production from the partial oxidation of methanol. Chem-PhysChem, 2005, 6: 1470–1472

    CAS  Google Scholar 

  31. Jasinski P, Suzuki T, Anderson HU. Nanocrystalline undoped ceria oxygen sensor. Senor Actuat B-Chem, 2003, 95: 73–77

    CAS  Google Scholar 

  32. Eguchi K, Setoguchi T, Inoue T, et al. Electrical properties of ceria-based oxides and their application to solid oxide fuel cells. Solid State Ion, 1992, 52: 165–172

    CAS  Google Scholar 

  33. Keating PRL, Scanlon DO, Watson GW. Intrinsic ferromagnetism in CeO2: Dispelling the myth of vacancy site localization mediated superexchange. J Phys-Condens Matter, 2009, 21: 405502

    CAS  Google Scholar 

  34. Song YQ, Zhang HW, Yang QH, et al. Electronic structure and magnetic properties of Co-doped CeO2: based on first principle calculation. J Phys-Condens Matter, 2009, 21: 125504

    CAS  Google Scholar 

  35. Shoko E, Smith MF, McKenzie RH. Charge distribution near bulk oxygen vacancies in cerium oxides. J Phys-Condens Matter, 2010, 22: 223201

    CAS  Google Scholar 

  36. Skorodumova NV, Simak SI, Lundqvist BI, et al. Quantum origin of the oxygen storage capability of ceria. Phys Rev Lett, 2002, 89: 166601

    CAS  Google Scholar 

  37. Deshpande S, Patil S, Kuchibhatla SV, et al. Size dependency variation in lattice parameter and valency states in nanocrystalline cerium oxide. Appl Phys Lett, 2005, 87: 133113

    Google Scholar 

  38. Krishnamoorthy K, Veerapandian M, Zhang LH, et al. Surface chemistry of cerium oxide nanocubes: Toxicity against pathogenic bacteria and their mechanistic study. J Ind Eng Chem, 2014, 20: 3513–3517

    CAS  Google Scholar 

  39. Korsvik C, Patil S, Seal S, et al. Superoxide dismutase mimetic properties exhibited by vacancy engineered ceria nanoparticles. Chem Commun, 2007, 303: 1056–1058

    Google Scholar 

  40. Pirmohamed T, Dowding JM, Singh S, et al. Nanoceria exhibit redox state-dependent catalase mimetic activity. Chem Commun, 2010, 46: 2736–2738

    CAS  Google Scholar 

  41. Asati A, Santra S, Kaittanis C, et al. Oxidase-like activity of polymer-coated cerium oxide nanoparticles. Angew Chem Int Ed, 2009, 48: 2308–2312

    CAS  Google Scholar 

  42. Huang Y, Ren J, Qu X. Nanozymes: Classification, catalytic mechanisms, activity regulation, and applications. Chem Rev, 2019, 119: 4357–4412

    CAS  Google Scholar 

  43. Gupta A, Das S, Neal CJ, et al. Controlling the surface chemistry of cerium oxide nanoparticles for biological applications. J Mater Chem B, 2016, 4: 3195–3202

    CAS  Google Scholar 

  44. Schubert D, Dargusch R, Raitano J, et al. Cerium and yttrium oxide nanoparticles are neuroprotective. Biochem BioPhys Res Commun, 2006, 342: 86–91

    CAS  Google Scholar 

  45. Kirchner C, Liedl T, Kudera S, et al. Cytotoxicity of colloidal CdSe and CdSe/ZnS nanoparticles. Nano Lett, 2005, 5: 331–338

    CAS  Google Scholar 

  46. Franklin NM, Rogers NJ, Apte SC, et al. Comparative toxicity of nanoparticulate ZnO, bulk ZnO, and ZnCl2 to a freshwater microalga (Pseudokirchneriella subcapitata): The importance of particle solubility. Environ Sci Technol, 2007, 41: 8484–8490

    CAS  Google Scholar 

  47. Hoecke KV, Quik JTK, Mankiewicz-Boczek J, et al. Fate and effects of CeO2 nanoparticles in aquatic ecotoxicity tests. Environ Sci Technol, 2009, 43: 4537–4546

    Google Scholar 

  48. Dickson JS, Koohmaraie M. Cell surface charge characteristics and their relationship to bacterial attachment to meat surfaces. Appl Environ Microbiol, 1989, 55: 832–836

    CAS  Google Scholar 

  49. Thill A, Zeyons O, Spalla O, et al. Cytotoxicity of CeO2 nano-particles for escherichia coli. physico-chemical insight of the cytotoxicity mechanism. Environ Sci Technol, 2006, 40: 6151–6156

    CAS  Google Scholar 

  50. Zeyons O, Thill A, Chauvat F, et al. Direct and indirect CeO2 nanoparticles toxicity for escherichia coli and synechocystis. Nanotoxicology, 2009, 3: 284–295

    CAS  Google Scholar 

  51. Pelletier DA, Suresh AK, Holton GA, et al. Effects of engineered cerium oxide nanoparticles on bacterial growth and viability. Appl Environ MicroBiol, 2010, 76: 7981–7989

    CAS  Google Scholar 

  52. He X, Kuang Y, Li Y, et al. Changing exposure media can reverse the cytotoxicity of ceria nanoparticles for escherichia coli. Nanotoxicology, 2012, 6: 233–240

    CAS  Google Scholar 

  53. Sobek JM, Talburt DE. Effects of the rare earth cerium on Escherichia coli. J Bacteriol, 1968, 95: 47–51

    CAS  Google Scholar 

  54. Li Y, Zhang W, Niu J, et al. Mechanism of photogenerated reactive oxygen species and correlation with the antibacterial properties of engineered metal-oxide nanoparticles. ACS Nano, 2012, 6: 5164–5173

    CAS  Google Scholar 

  55. Aruguete DM, Kim B, Hochella MF, et al. Antimicrobial nano-technology: Its potential for the effective management of microbial drug resistance and implications for research needs in microbial nanotoxicology. Environ Sci-Processes Impacts, 2013, 15: 93–102

    CAS  Google Scholar 

  56. Alpaslan E, Geilich BM, Yazici H, et al. pH-controlled cerium oxide nanoparticle inhibition of both Gram-positive and Gramnegative bacteria growth. Sci Rep, 2017, 7: 45859

    CAS  Google Scholar 

  57. Arumugam A, Karthikeyan C, Haja Hameed AS, et al. Synthesis of cerium oxide nanoparticles using Gloriosa superba L. leaf extract and their structural, optical and antibacterial properties. Mater Sci Eng-C, 2015, 49: 408–415

    CAS  Google Scholar 

  58. Tong GX, Du FF, Liang Y, et al. Polymorphous ZnO complex architectures: Selective synthesis, mechanism, surface area and Zn-polar plane-codetermining antibacterial activity. J Mater Chem B, 2013, 1: 454–463

    CAS  Google Scholar 

  59. Akhavan O, Ghaderi E. Toxicity of graphene and graphene oxide nanowalls against bacteria. ACS Nano, 2010, 4: 5731–5736

    CAS  Google Scholar 

  60. Charbgoo F, Ahmad MB, Darroudi M. Cerium oxide nano-particles: Green synthesis and biological applications. Int J Nanomed, 2017, Volume 12: 1401–1413

    CAS  Google Scholar 

  61. Farias IAP, Dos Santos CCL, Sampaio FC. Antimicrobial activity of cerium oxide nanoparticles on opportunistic microorganisms: A systematic review. Biomed Res Int, 2018, 2018(3): 1–14

    Google Scholar 

  62. Roduner E. Size matters: Why nanomaterials are different. Chem Soc Rev, 2006, 35: 583–592

    CAS  Google Scholar 

  63. Farokhzad OC, Cheng J, Teply BA, et al. Targeted nanoparticleaptamer bioconjugates for cancer chemotherapy in vivo. Proc Natl Acad Sci USA, 2006, 103: 6315–6320

    CAS  Google Scholar 

  64. Kuang Y, He X, Zhang Z, et al. Comparison study on the antibacterial activity of nano- or bulk-cerium oxide. J Nanosci Nanotech, 2011, 11: 4103–4108

    CAS  Google Scholar 

  65. Gottenbos B, Grijpma DW, van der Mei HC, et al. Antimicrobial effects of positively charged surfaces on adhering Gram-positive and Gram-negative bacteria. J Antimicrob Chemother, 2001, 48: 7–13

    CAS  Google Scholar 

  66. Zhu Y, Ran T, Li Y, et al. Dependence of the cytotoxicity of multi-walled carbon nanotubes on the culture medium. Nanotechnology, 2006, 17: 4668–4674

    CAS  Google Scholar 

  67. Limbach LK, Li Y, Grass RN, et al. Oxide nanoparticle uptake in human lung fibroblasts: Effects of particle size, agglomeration, and diffusion at low concentrations. Environ Sci Technol, 2005, 39: 9370–9376

    CAS  Google Scholar 

  68. Mathew TV, Kuriakose S. Studies on the antimicrobial properties of colloidal silver nanoparticles stabilized by bovine serum albumin. Colloids Surfs B-Biointerfaces, 2013, 101: 14–18

    CAS  Google Scholar 

  69. Babenko L, Zholobak N, Shcherbakov A, et al. Antibacterial activity of cerium colloids against opportunistic microorganisms in vitro. Mikrobiolohichnyĭ zhurnal, 2012, 74: 54–62

    CAS  Google Scholar 

  70. Surendra TV, Roopan SM. Photocatalytic and antibacterial properties of phytosynthesized CeO2 NPs using Moringa oleifera peel extract. J PhotoChem PhotoBiol B-Biol, 2016, 161: 122–128

    CAS  Google Scholar 

  71. Cuahtecontzi-Delint R, Mendez-Rojas MA, Bandala ER, et al. Enhanced antibacterial activity of CeO2 nanoparticles by surfactants. Int J Chem Reactor Eng, 2013, 11: 781–785

    Google Scholar 

  72. Maqbool Q, Nazar M, Naz S, et al. Antimicrobial potential of green synthesized CeO2 nanoparticles from Olea europaea leaf extract. Int J Nanomed, 2016, Volume 11: 5015–5025

    CAS  Google Scholar 

  73. Patil SN, Paradeshi JS, Chaudhari PB, et al. Bio-therapeutic potential and cytotoxicity assessment of pectin-mediated synthesized nanostructured cerium oxide. Appl Biochem Biotechnol, 2016, 180: 638–654

    CAS  Google Scholar 

  74. Gopinath K, Karthika V, Sundaravadivelan C, et al. Mycogenesis of cerium oxide nanoparticles using Aspergillus niger culture filtrate and their applications for antibacterial and larvicidal activities. J Nanostruct Chem, 2015, 5: 295–303

    CAS  Google Scholar 

  75. Reddy Yadav LS, Manjunath K, Archana B, et al. Fruit juice extract mediated synthesis of CeO2 nanoparticles for antibacterial and photocatalytic activities. Eur Phys J Plus, 2016, 131: 154

    Google Scholar 

  76. Malleshappa J, Nagabhushana H, Sharma SC, et al. Leucas aspera mediated multifunctional CeO2 nanoparticles: Structural, photoluminescent, photocatalytic and antibacterial properties. Spectro-Chim Acta Part A-Mol Biomol Spectr, 2015, 149: 452–462

    CAS  Google Scholar 

  77. Ravishankar TN, Ramakrishnappa T, Nagaraju G, et al. Synthesis and characterization of CeO2 nanoparticles via solution combustion method for photocatalytic and antibacterial activity studies. ChemistryOpen, 2015, 4: 146–154

    CAS  Google Scholar 

  78. Wang Q, Perez JM, Webster TJ. Inhibited growth of pseudomonas aeruginosa by dextran- and polyacrylic acid-coated ceria nano-particles. Int J Nanomed, 2013, 8: 3395

    Google Scholar 

  79. Huang X, Li LD, Lyu GM, et al. Chitosan-coated cerium oxide nanocubes accelerate cutaneous wound healing by curtailing persistent inflammation. Inorg Chem Front, 2018, 5: 386–393

    CAS  Google Scholar 

Download references

Acknowledgments

We gratefully acknowledge the support from the National Funds for Excellent Young Scientists of China (21522106), the National Key R&D Program of China (2017YFA0208000), and the 111 Project (B18030) from China.

Author information

Authors and Affiliations

  1. Tianjin Key Lab for Rare Earth Materials and Applications, Center for Rare Earth and Inorganic Functional Materials, School of Materials Science and Engineering & National Institute for Advanced Materials, Nankai University, Tianjin, 300350, China

    Mengzhen Zhang  (张萌真), Chao Zhang  (张超), Xinyun Zhai  (翟欣昀), Yaping Du  (杜亚平) & Chunhua Yan  (严纯华)

  2. IMDEA Nanoscience, Faraday 9, Ciudad Universitaria de Cantoblanco, Madrid, 28049, Spain

    Feng Luo  (罗锋)

  3. Beijing National Laboratory for Molecular Sciences, State Key Laboratory of Rare Earth Materials Chemistry and Applications, PKU-HKU Joint Laboratory in Rare Earth Materials and Bioinorganic Chemistry, College of Chemistry and Molecular Engineering, Peking University, Beijing, 100871, China

    Chunhua Yan  (严纯华)

  4. College of Chemistry and Chemical Engineering, Lanzhou University, Lanzhou, 730000, China

    Chunhua Yan  (严纯华)

Authors
  1. Mengzhen Zhang  (张萌真)
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chao Zhang  (张超)
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xinyun Zhai  (翟欣昀)
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Feng Luo  (罗锋)
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yaping Du  (杜亚平)
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Chunhua Yan  (严纯华)
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Du Y and Yan C proposed the overall concept. Zhang M wrote the paper with the guidance from Du Y, Luo F and Zhai X; Zhang M, Zhang C and Zhai X revised the manuscript. All authors contributed to the general discussion.

Corresponding author

Correspondence to Xinyun Zhai  (翟欣昀).

Additional information

Conflict of interest

The authors declare no conflict of interest.

Mengzhen Zhang is a PhD student at the School of Chemistry, Nankai University. Her research interest focuses on the rare earth based functional materials.

Chunhua Yan is the President of Lanzhou University and the Director of the State Key Laboratory of Rare Earth Materials Chemistry and Applications at Peking University, and the Center for Rare Earth and Inorganic Functional Materials at Nankai University. He received his BSc, MSc, and PhD degrees from Peking University.

Xinyun Zhai is a lecturer at the School of Material Science and Engineering, Nankai University. She received her BSc degree and MSc degree from Tianjin University in 2010 and 2013, respectively and PhD degree from The University of Hong Kong in 2017. Her research interests focus on rare-earth based biomedical materials and rare-earth based functional materials.

Yaping Du is a full professor at the School of Material Science and Engineering, Nankai University. He is the director of Tianjin Key Lab for Rare Earth Materials and Applications and Deputy Director of the Centre for Rare Earth and Inorganic Functional Materials. His research interests focus on rare-earth functional materials. He has more than 90 publications in peer-reviewed scientific journals and was a winner of the National Science Fund for Excellent Young Scholars in 2015. He received his BSc degree from Lanzhou University in 2004 and PhD degree from Peking University in 2009.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, M., Zhang, C., Zhai, X. et al. Antibacterial mechanism and activity of cerium oxide nanoparticles. Sci. China Mater. 62, 1727–1739 (2019). https://doi.org/10.1007/s40843-019-9471-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40843-019-9471-7

Keywords

Search

Navigation