ZnO and TiO2 nanoparticles as novel antimicrobial agents for oral hygiene: a review

  • Shams Tabrez Khan
  • Abdulaziz A. Al-Khedhairy
  • Javed Musarrat
Review
First Online:
Received:
Accepted:

Abstract

Oral cavity is inhabited by more than 25,000 different bacterial phylotypes; some of them cause systemic infections in addition to dental and periodontal diseases. Emergence of multiple antibiotic resistance among these bacteria necessitates the development of alternative antimicrobial agents that are safe, stable, and relatively economic. This review focuses on the significance of metal oxide nanoparticles, especially zinc oxide and titanium dioxide nanoparticles as supplementary antimicrobials for controlling oral infections and biofilm formation. Indeed, the ZnO NPs and TiO2 NPs have exhibited significant antimicrobial activity against oral bacteria at concentrations which is not toxic in in vivo toxicity assays. These nanoparticles are being produced at an industrial scale for use in a variety of commercial products including food products. Thus, the application of ZnO and TiO2 NPs as nanoantibiotics for the development of mouthwashes, dental pastes, and other oral hygiene materials is envisaged. It is also suggested that these NPs could serve as healthier, innocuous, and effective alternative for controlling both the dental biofilms and oral planktonic bacteria with lesser side effects and antibiotic resistance.

Keywords

ZnO and TiO2 nanoparticles Oral bacteria Biofilm Nanoantibiotics Antibiotic resistance Nanomedicine Health effects 

Notes

Acknowledgments

This project was funded by the National Plan for Science, Technology and Innovation (MAARIFAH), King Abdul Aziz City for Science and Technology, Kingdom of Saudi Arabia Award Number (12-NAN-2490-2).

Conflict interest

The authors declare no conflict of interest whatsoever.

References

  1. Aas JA, Paster BJ, Stokes LN, Olsen I, Dewhirst FE (2005) Defining the normal bacterial flora of the oral cavity. J Clin Microbiol 43:5721–5732Google Scholar
  2. Abeylath SC, Turos E (2008) Drug delivery approaches to overcome bacterial resistance to β-lactam antibiotics. Expert Opin Drug Deliv 5:931–949Google Scholar
  3. Adams PC, Walker KA, Obare SO, Docherty KM (2014) Size-dependent antimicrobial effects of novel palladium nanoparticles. PLoS ONE 9(1):e85981Google Scholar
  4. Ahmad J, Dwivedi S, Alarifia S, Al-Khedhairy AA, Musarrat J (2012) Use of β-galactosidase (lacZ) gene α-complementation as a novel approach for assessment of titanium oxide nanoparticles induced mutagenesis. Mutat Res 747:246–252Google Scholar
  5. Ahn J, Chen CY, Hayes RB (2012) Oral microbiome an oral and gastrointestinal cancer risk. Cancer Cause Control 23:399–404Google Scholar
  6. Akbar A, Kumar A (2014) Zinc oxide nanoparticles loaded active packaging, a challenge study against Salmonella typhimurium and Staphylococcus aureus in ready-to-eat poultry meat. Food Control 38:88–95Google Scholar
  7. Ali J, Pramod K, Tahir MA, Ansari SH (2011) Autoimmune responses in periodontal diseases. Autoimmun Rev 10:426–431Google Scholar
  8. Allaker RP (2010) The use of nanoparticles to control oral biofilm formation. J Dent Res 89:1175–1186Google Scholar
  9. Allaker RP, Memarzadeh K (2014) Nanoparticles and the control of oral infections. Int J Antimicrob Agents 43:95–104Google Scholar
  10. Applerot G, Lellouche J, Perkas N, Nitzan Y, Gedanken A, Banin E (2012) ZnO nanoparticle-coated surfaces inhibit bacterial biofilm formation and increase antibiotic susceptibility. RSC Adv 2:2314–2321Google Scholar
  11. Ardila CM, López MA, Guzmán IC (2010) High resistance against clindamycin, metronidazole and amoxicillin in Porphyromonas gingivalis and Aggregatibacter actinomycetemcomitans isolates of periodontal disease. Med Oral Patol Oral Cir Bucal 15:e947–e951Google Scholar
  12. Aydin-Sevinç AB, Hanley L (2010) Antibacterial activity of dental composites containing zinc oxide nanoparticles. J Biomed Mater Res B 94:22–31Google Scholar
  13. Azam A, Ahmed SA, Oves M, Khan MS, Memic A (2012) Size-dependent antimicrobial properties of CuO nanoparticles against Gram-positive and -negative bacterial strains. Int J Nanomed 7:3527–3535Google Scholar
  14. Baek YW, An YJ (2011) Microbial toxicity of metal oxide nanoparticles (CuO, NiO, ZnO, and Sb2O3) to Escherichia coli, Bacillus subtilis, and Streptococcus aureus. Sci Total Environ 409:1603–1608Google Scholar
  15. Balogh L, Swanson DR, Tomalia DA, Hagnauer GL, McManus AT (2001) Dendrimer-silver complexes and nanocomposites as antimicrobial agents. Nano Lett 1:18–21Google Scholar
  16. Bañobre-López M, Teijeiro A, Rivas J (2013) Magnetic nanoparticle-based hyperthermia for cancer treatment. Rep Pract Oncol Radiother 18:397–400Google Scholar
  17. Bascones-Martinez A, Matesanz-Perez P, Escribano-Bermejo M et al (2011) Periodontal disease and diabetes-review of the literature. Med Oral Patol Oral Cir Bucal 16:e722–e729Google Scholar
  18. Belda-Ferre P, Alcaraz LD, Cabrera-Rubio R et al (2011) The oral metagenome in health and disease. ISME J 6:46–56Google Scholar
  19. Berube DM, Searson EM, Morton TS, Cummings CL (2010) Project on emerging nanotechnologies—consumer product inventory evaluated. Nanotechnol Law Bus 7:152–163Google Scholar
  20. Bondarenko O, Juganson K, Ivask A, Kasemets K, Mortimer M, Kahru A (2013) Toxicity of Ag, CuO and ZnO nanoparticles to selected environmentally relevant test organisms and mammalian cells in vitro: a critical review. Arch Toxicol 87:1181–1200Google Scholar
  21. Bradshaw DJ, Homer KA, Marsh PD, Beighton D (1994) Metabolic cooperation in oral microbial communities during growth on mucin. Microbiol 140:3407–3412Google Scholar
  22. Bragg PD, Rainnie DJ (1974) The effect of silver ions on the respiratory chain of Escherichia coli. Can J Microbiol 20:883–889Google Scholar
  23. Brown MR, Allison DG, Gilbert P (1988) Resistance of bacterial biofilms to antibiotics: a growth-rate related effect? J Antimicrob Chemother 22:777–780Google Scholar
  24. Byrne GI, Kalayoglu MV (1999) Chlamydia pneumoniae and atherosclerosis: links to the disease process. Am Heart J 138:S488–S490Google Scholar
  25. Cai W, Gao T, Hong H, Sun J (2008) Applications of gold nanoparticles in cancer nanotechnology. Nanotechnol Sci Appl. doi:10.2147/NSA.S3788 Google Scholar
  26. Castellarin M, Warren RL, Freeman JD et al (2012) Fusobacterium nucleatum infection is prevalent in human colorectal carcinoma. Genome Res 22:299–306Google Scholar
  27. Cheng L, Weir MD, Xu HH et al (2012) Effect of amorphous calcium phosphate and silver nanocomposites on dental plaque microcosm biofilms. J Biomed Mater Res B 100:1378–1386Google Scholar
  28. Choi O, Deng KK, Kim NJ et al (2008) The inhibitory effects of silver nanoparticles, silver ions, and silver chloride colloids on microbial growth. Water Res 42:3066–3074Google Scholar
  29. Chun MJ, Shim E, Kho EH et al (2007) Surface modification of orthodontic wires with photocatalytic titanium oxide for its antiadherent and antibacterial properties. Angle Orthod 77:483–488Google Scholar
  30. Clarke JK (1924) On the bacterial factor in the etiology of dental caries. Br J Exp Pathol 5:141–147Google Scholar
  31. Cole MF, Evans M, Fitzsimmons S et al (1994) Pioneer oral Streptococci produce immunoglobulin A1 protease. Infect Immun 62:2165–2168Google Scholar
  32. Costerton JW, Lewandowski Z, Caldwell DE et al (1995) Microbial biofilms. Annu Rev Microbiol 49:711–745Google Scholar
  33. Dar-Odeh NS, Abu-Hammad OA, Al-Omiri MK, Khraisat AS, Shehabi AA (2010) Antibiotic prescribing practices by dentists: a review. Ther Clin Risk Manag 6:301–306Google Scholar
  34. Darveau PR (2010) Periodontitis: a polymicrobial disruption of host homeostasis. Nat Rev Microbiol 8:481–490Google Scholar
  35. Dastjerdi R, Montazer M (2010) A review on the application of inorganic nanostructured materials in the modification of textile: focus on antimicrobial properties. Colloids Surf B 79:5–18Google Scholar
  36. Davey ME, O’Toole GA (2000) Microbial biofilms: from ecology to molecular genetics. Microbiol Mol Biol Rev 64:847–867Google Scholar
  37. De Berardis B, Civitelli G, Condello M et al (2010) Exposure to ZnO nanoparticles induces oxidative stress and cytotoxicity in human colon carcinoma cells. Toxicol Appl Pharmacol 246:116–127Google Scholar
  38. De Jong WH, Borm PJA (2008) Drug delivery and nanoparticles: applications and hazards. Int J Nanomedicine 3:133–149Google Scholar
  39. Deshpande RG, Khan MB, Genco CA (1998) Invasion of aortic and heart endothelial cells by Porphyromonas gingivalis. Infect Immun 66:5337–5343Google Scholar
  40. Dewhirst FE, Chen T, Izard J et al (2010) The human oral microbiome. J Bacteriol 192:5002–5017Google Scholar
  41. Dietrich T, Sharma P, Walter C et al (2013) The epidemiological evidence behind the association between periodontitis and incident atherosclerotic cardiovascular disease. J Periodontol 84:S70–S84Google Scholar
  42. Drummen GPC (2010) Quantum dots—from synthesis to applications in biomedicine and life sciences. Int J Mol Sci 11:154–163Google Scholar
  43. Dwivedi P, Narvi SS, Tewari RP (2013) Application of polymer nanocomposites in the nanomedicine landscape: envisaging strategies to combat implant associated infections. J Appl Biomater Funct Mater 11:129–142Google Scholar
  44. Eshed M, Lellouche J, Matalon S et al (2012) Sonochemical coatings of ZnO and CuO nanoparticles inhibit Streptococcus mutans biofilm formation on teeth model. Langmuir 28:12288–12295Google Scholar
  45. Espinosa-Cristóbal FA, Martínez-Castañóna GA, Téllez-Déctorb EJ et al (2012) Adherence inhibition of Streptococcus mutans on dental enamel surface using silver nanoparticles. Mater Sci Eng C 33:2197–2202Google Scholar
  46. Fabrega J, Zhang R, Renshaw JC, Liu WT, Lead JR (2011) Impact of silver nanoparticles on natural marine biofilm bacteria. Chemosphere 85:961–966Google Scholar
  47. Fang M, Chen JH, Xu XL, Yang PH, Hildebr HF (2006) Antibacterial activities of inorganic agents on six bacteria associated with oral infections by two susceptibility tests. Int J Antimicrob Agents 27:513–517Google Scholar
  48. Fardini Y, Wang X, Temoin S et al (2011) Fusobacterium nucleatum adhesin FadA binds vascular endothelial cadherin and alters endothelial integrity. Mol Microbiol 82:1468–1480Google Scholar
  49. Fosse T, Madinier I, Hitzig C, Charbit Y (1999) Prevalence of beta-lactamase-producing strains among 149 anaerobic Gram-negative rods isolated from periodontal pockets. Oral Microbiol Immunol 14:352–357Google Scholar
  50. Frandsen EV, Theilade E, Ellegaard B, Kilian M (1986) Proportions and identity of IgA1-degrading bacteria in periodontal pockets from patients with juvenile and rapidly progressive periodontitis. J Periodontal Res 21:613–623Google Scholar
  51. Fröjd V, Linderbäck P, Wennerberg A, Chávez de Paz L, Svensäter G, Davies JR (2011) Effect of nanoporous TiO2 coating and anodized Ca2+ modification of titanium surfaces on early microbial biofilm formation. BMC Oral Health 11:8Google Scholar
  52. Fukui H, Horie M, Endoh S et al (2012) Association of zinc ion release and oxidative stress induced by intratracheal instillation of ZnO nanoparticles to rat lung. Chem Biol Interact 198:29–37Google Scholar
  53. Gilbert P, Das J, Foley I (1997) Biofilm susceptibility to antimicrobials. Adv Dent Res 11:160–167Google Scholar
  54. Hajipour MJ, Fromm KM, Ashkarran AA et al (2012) Antibacterial properties of nanoparticles. Trends Biotechnol 30:499–511Google Scholar
  55. Han YW, Wang X (2013) Mobile microbiome: oral bacteria in extra-oral infections and inflammation. J Dent Res 92:485–491Google Scholar
  56. Han YW, Fardini Y, Chen C et al (2010) Term stillbirth caused by oral Fusobacterium nucleatum. Obstet Gynecol 115:442–445Google Scholar
  57. Hanemann T, Szabó DV (2010) Polymer-nanoparticle composites: from synthesis to modern applications. Materials 3:3468–3517Google Scholar
  58. Hayashi C, Gudino CV, Gibson FCIII, Genco CA (2010) Review: pathogen-induced inflammation at sites distant from oral infection: bacterial persistence and induction of cell-specific innate immune inflammatory pathways. Mol Oral Microbiol 25:305–316Google Scholar
  59. Hernández-Sierra JF, Ruiz F, Pena DC et al (2008) The antimicrobial sensitivity of Streptococcus mutans to nanoparticles of silver, zinc oxide, and gold. Nanomedicine 4:237–240Google Scholar
  60. Herzberg MC, Meyer MW (1996) Effects of oral flora on platelets: possible consequences in cardiovascular disease. J Periodontol 67:1138–1142Google Scholar
  61. Hetrick EM, Shin JH, Paul SH, Schoenfisch MH (2009) Anti-biofilm efficacy of nitric oxide-releasing silica nanoparticles. Biomaterials 30:2782–2789Google Scholar
  62. Höglund ÅC, Haubek D, Kwamin F, Johansson A, Claesson R (2014) Leukotoxic activity of Aggregatibacter actinomycetemcomitans and periodontal attachment loss. PLoS One 9(8):e104095Google Scholar
  63. Hojo K, Nagaoka S, Ohshima T, Maeda N (2009) Bacterial interactions in dental biofilm development. J Dent Res 88:982–990Google Scholar
  64. Huh AJ, Kwon YJ (2011) “Nanoantibiotics”: a new paradigm for treating infectious diseases using nanomaterials in the antibiotics resistant era. J Controlled Release 156:128–145Google Scholar
  65. Hule RA, Pochan DJ (2007) Polymer nanocomposites for biomedical applications. MRS Bull 32:354–358Google Scholar
  66. Ismail Y, Mahendran V, Octavia S et al (2012) Investigation of the enteric pathogenic potential of oral Campylobacter concisus strains isolated from patients with inflammatory bowel disease. PLoS ONE 7:e38217Google Scholar
  67. Jenkinson HF (2011) Beyond the oral microbiome. Environ Microbiol 13:3077–3087Google Scholar
  68. Jin T, Sun D, Su JY, Zhang H (2009) Antimicrobial efficacy of zinc oxide quantum dots against Listeria monocytogenes, Salmonella enteritidis and E. coli O157:H7. J Food Sci 74:46–52Google Scholar
  69. Kamer AR, Dasanayake AP, Craig RG, Glodzik-Sobanska L, Bry M, de Leon MJ (2008) Alzheimer’s disease and peripheral infections: the possible contribution from periodontal infections, model and hypothesis. J Alzheimers Dis 13:437–449Google Scholar
  70. Keijser BJF, Zaura E, Huse SM et al (2008) Pyrosequencing analysis of the Oral microflora of healthy adults. J Dent Res 87:1016–1020Google Scholar
  71. Keller AA, McFerran S, Lazareva A, Suh S (2013) Global life cycle releases of engineered nanomaterials. J Nanopart Res 15:1692Google Scholar
  72. Khan ST, Ahmad M, Al-Khedhairy AA, Musarrat J (2013a) Biocidal effect of copper and zinc oxide nanoparticles on human oral microbiome and biofilm formation. Mater Lett 97:67–70Google Scholar
  73. Khan ST, Ahamed M, Alhadlaq HA, Musarrat J, Al-Khedhairy AA (2013b) Comparative effectiveness of NiCl2, Ni- and NiO-NPs in controlling oral bacterial growth and biofilm formation on oral surfaces. Arch Oral Biol 58:1804–1811Google Scholar
  74. Khan M, Khan ST, Khan M et al (2014a) Antibacterial properties of silver nanoparticles synthesized using Pulicaria glutinosa plant extract as a green bioreductant. Int J Nanomed 9:3551–3565Google Scholar
  75. Khan ST, Ahamed M, Musarrat J, Al-Khedhairy AA (2014b) Antibiofilm and antibacterial activities of zinc oxide nanoparticles against the oral opportunistic pathogens Rothia dentocariosa (Ora-7) and Rothia mucilaginosa (Ora-16) isolates. Eur J Oral Sci 122:397–403Google Scholar
  76. Kim JS, Kuk E, Yu KN et al (2007) Antimicrobial effects of silver nanoparticles. Nanomedicine 3:95–101Google Scholar
  77. Kirchner M, Mafura M, Hunt T, Card R, Anjum MF (2013) Antibiotic resistance gene profiling of faecal and oral anaerobes collected during an antibiotic challenge trial. Anaerobe 23:20–22Google Scholar
  78. Kolenbrander PE, London J (1993) Adhere today, here tomorrow: oral bacterial adherence. J Bacteriol 175:3247–3252Google Scholar
  79. Kolenbrander PE, Andersen RN, Blehert DS, Egland PG, Foster JS, Palmer RJ Jr (2002) Communication among oral bacteria. Microbiol Mol Biol Rev 66:486–505Google Scholar
  80. Kolenbrander PE, Palmer RJ, Periasamy S, Jakubovics NS (2010) Oral multispecies biofilm development and the key role of cell–cell distance. Nat Rev Microbiol 8:473–480Google Scholar
  81. Komoria R, Sato T, Yamamotoa T, Takahashi N (2012) Microbial composition of dental plaque microflora on first molars with orthodontic bands and brackets, and the acidogenic potential of these bacteria. J Ora Biosci 54:107–112Google Scholar
  82. Konishi K (1987) Antibacterial effect of the powdered semiconductor titanium oxide on the viability of oral microorganisms. Shika Igaku 50:119–125Google Scholar
  83. Koren O, Spor A, Felin J et al (2011) Human oral, gut, and plaque microbiota in patients with atherosclerosis. PNAS 108:4592–4598Google Scholar
  84. Kostic AD, Chun E, Robertson L et al (2013) Fusobacterium nucleatum potentiates intestinal tumorigenesis and modulates the tumor-immune microenvironment. Cell Host Microbe 14:207–215Google Scholar
  85. Kouidhi B, Zmantar T, Mahdouani K, Hentati H, Bakhrouf A (2011) Antibiotic resistance and adhesion properties of oral Enterococci associated to dental caries. BMC Microbiol 11:155Google Scholar
  86. Kühn KP, Cahberny IF, Massholder K et al (2003) Disinfection of surfaces by photocatalytic oxidation with titanium dioxide and UVA light. Chemosphere 53:71–77Google Scholar
  87. Kumar A, Pandey AK, Singh SS, Shanker R, Dhawan A (2011) Engineered ZnO and TiO2 nanoparticles induce oxidative stress and DNA damage leading to reduced viability of Escherichia coli. Free Radic Biol Med 51:1872–1881Google Scholar
  88. Lee HR, Jun HK, Kim HD, Lee SH, Choi BK (2012) Fusobacterium nucleatum GroEL induces risk factors of atherosclerosis in human microvascular endothelial cells and ApoE(−/−) mice. Mol Oral Microbiol 27:109–123Google Scholar
  89. Lee JH, Kim YG, Cho MH, Lee J (2014) ZnO nanoparticles inhibit Pseudomonas aeruginosa biofilm formation and virulence factor production. Microbiol Res 169:888–896Google Scholar
  90. Leistevuo J, Järvinen H, Österblad M, Leistevuo T, Huovinen P, Tenovuo J (2000) Resistance to mercury and antimicrobial agents in Streptococcus mutans isolates from human subjects in relation to exposure to dental amalgam fillings. Antimicrob Agents Chemother 44:456–457Google Scholar
  91. Li X, Kolltveit KM, Tronstad L, Olsen I (2000) Systemic diseases caused by oral infection. Clin Microbiol Rev 13:547–558Google Scholar
  92. Li Q, Mahendra S, Lyon DY et al (2008) Antimicrobial nanomaterials for water disinfection and microbial control: potential applications and implications. Water Res 42:4591–4602Google Scholar
  93. Li K, Zhao X, Hammer BK, Du S, Chen Y (2013) Nanoparticles inhibit DNA replication by binding to DNA: modeling and experimental validation. ACS Nano 7:9664–9674Google Scholar
  94. Liu Y, He L, Mustapha A, Li H, Hu ZQ, Lin M (2009) Antibacterial activities of zinc oxide nanoparticles against Escherichia coli O157:H7. J Appl Microbiol 107:1193–1201Google Scholar
  95. Liu B, Faller LL, Klitgord N et al (2012) Deep sequencing of the oral microbiome reveals signatures of periodontal disease. PLoS ONE 7(1–16):e37919Google Scholar
  96. Loesche WJ (1986) Role of Streptococcus mutans in human dental decay. Microbiol Rev 50(4):353–380Google Scholar
  97. Lu Z, Rong K, Li J, Yang H, Chen R (2013) Size-dependent antibacterial activities of silver nanoparticles against oral anaerobic pathogenic bacteria. J Mater Sci Mater Med 24:1465–1471Google Scholar
  98. Luo Morrin A, Killard AJ, Smyth MR (2006) Application of nanoparticles in electrochemical sensors and biosensors. Electroanalysis 18:319–326Google Scholar
  99. Madinier IM (1999) Resistance profile survey of 50 periodontal strains of Actinobacillus actinomycetemcomitans. J Periodontol 70:888–892Google Scholar
  100. Mah TFC, O’Toole GA (2001) Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol 9:34–39Google Scholar
  101. Mah TF, Pitts B, Pellock B, Walker GC, Stewart PS, O’Toole GA (2003) A genetic basis for Pseudomonas aeruginosa biofilm antibiotic resistance. Nature 426:306–310Google Scholar
  102. Mahmoudi M, Serpooshan V (2012) Silver-coated engineered magnetic nanoparticles are promising for the success in the fight against antibacterial resistance threat. ACS Nano 6:2656–2664Google Scholar
  103. Maness PC, Smolinski S, Blake DM, Huang Z, Wolfrum EJ, Jacoby WA (1999) Bactericidal activity of photocatalytic TiO2 reaction: toward an understanding of its killing mechanism. Appl Environ Microbiol 65:4094–4098Google Scholar
  104. Marambio-Jones C, Hoek EMV (2010) A review of the antibacterial effects of silver nanomaterials and potential implications for human health and the environment. J Nanopart Res 12:1531–1551Google Scholar
  105. Marcus AJ, Hajjar DP (1993) Vascular transcellular signaling. J Lipid Res 34:2017–2031Google Scholar
  106. Mattila KJ (1989) Viral and bacterial infections in patients with acute myocardial infarction. J Intern Med 225:293–296Google Scholar
  107. Maurer-Jones MA, Gunsolus IL, Meyer BM, Christenson CJ, Haynes CL (2013) Impact of TiO2 nanoparticles on growth, biofilm formation, and flavin secretion in Shewanella oneidensis. Anal Chem 85:5810–5818Google Scholar
  108. Moos PJ, Olszewski K, Honeggar M et al (2011) Responses of human cells to ZnO nanoparticles: a gene transcription study. Metallomics 3:1199–1211Google Scholar
  109. Morris JF, Sewell DL (1994) Necrotizing pneumonia caused by mixed infection with Actinobacillus actinomycetemcomitans and Actinomyces israelii: case report and review. Clin Infect Dis 18:450–452Google Scholar
  110. Munson MA, Banerjee A, Watson TF, Wade WG (2004) Molecular analysis of the microflora associated with dental caries. J Clin Microbiol 42:3023–3029Google Scholar
  111. Musarrat J, Saquib Q, Azam A, Naqvi SAH (2009) Zinc oxide nanoparticles-induced DNA damage in human lymphocytes. Int J Nanopart 2:402–415Google Scholar
  112. Nasidze I, Li J, Quinque D, Tang K, Stoneking M (2009) Global diversity in the human salivary microbiome. Genome Res 19:636–643Google Scholar
  113. Nyfors S, Könönen E, Syrjänen R, Komulainen E, Jousimies-Somer H (2003) Emergence of penicillin resistance among Fusobacterium nucleatum populations of commensal oral flora during early childhood. J Antimicrob Chemother 51:107–112Google Scholar
  114. Ou KL, Chu JS, Hosseinkhani H, Chiou JF, Yu CH (2014) Biomedical nanostructured coating for minimally invasive surgery devices applications: characterization, cell cytotoxicity evaluation and an animal study in rat. Surg Endosc 28(7):2174–2188Google Scholar
  115. Pal S, Tak YK, Song JM (2007) Does the antibacterial activity of silver nanoparticles depend on the shape of the nanoparticle? A study of the Gram-negative bacterium Escherichia coli. Appl Environ Microbiol 73:1712–1720Google Scholar
  116. Park H, Park HJ, Kim JA et al (2011) Inactivation of Pseudomonas aeruginosa PA01 biofilms by hyperthermia using superparamagnetic nanoparticles. J Microbiol Methods 84:41–45Google Scholar
  117. Paster BJ, Boches SK, Galvin JL et al (2001) Bacterial diversity in human subgingival plaque. J Bacteriol 183:3770–3783Google Scholar
  118. Paster BJ, Olsen I, Aas JA, Dewhirst FE (2006) The breadth of bacterial diversity in the human periodontal pocket and other oral sites. Periodontol 2000 42:80–87Google Scholar
  119. Peng JJ, Botelho MG, Matinlinna JP (2012) Silver compounds used in dentistry for caries management: a review. J Dent 40:531–541Google Scholar
  120. Piccinno F, Gottschalk F, Seeger S, Nowack B (2012) Industrial production quantities and uses of ten engineered nanomaterials for Europe and the world. J Nanopart Res 14:1109–1120Google Scholar
  121. Raghupathi KR, Koodali RT, Manna AC (2011) Size-dependent bacterial growth inhibition and mechanism of antibacterial activity of zinc oxide nanoparticles. Langmuir 27:4020–4028Google Scholar
  122. Rajakumar G, Rahuman AA, Roopan SM et al (2012) Fungus-mediated biosynthesis and characterization of TiO2 nanoparticles and their activity against pathogenic bacteria. Spectrochim Acta A 91:23–29Google Scholar
  123. Ready D, Bedi R, Spratt DA, Mullany P, Wilson M (2003) Prevalence, proportions, and identities of antibiotic-resistant bacteria in the oral microflora of healthy children. Microb Drug Resist 9:367–372Google Scholar
  124. Rôças IN, Siqueira JF Jr (2012) Antibiotic resistance genes in anaerobic bacteria isolated from primary dental root canal infections. Anaerobe 18:576–580Google Scholar
  125. Saito T, Iwase T, Horie J, Morioka T (1992) Mode of photocatalytic bactericidal action of powdered semiconductor TiO2 on mutans streptococci. J Photochem Photobiol B 14:369–379Google Scholar
  126. Sandhiya S, Dkhar SA, Surendiran A (2009) Emerging trends of nanomedicine—an overview. Fundam Clin Pharmacol 23:263–269Google Scholar
  127. Saunders SA (2009) Current practicality of nanotechnology in dentistry. Part 1: Focus on nanocomposite restoratives and biomimetics. Clin Cosmet Investig Dent 1:47–61Google Scholar
  128. Seyedmahmoudi SH, Harper SL, Weismiller MC, Haapala KR (2015) Evaluating the use of zinc oxide and titanium dioxide nanoparticles in a metalworking fluid from a toxicological perspective. J Nanopart Res 17:104Google Scholar
  129. Sheng Z, Liu Y (2011) Effects of silver nanoparticles on wastewater biofilms. Water Res 45:6039–6050Google Scholar
  130. Skopek RJ, Liljemark WF, Bloomquist CG, Rudney JD (1993) Dental plaque development on defined Streptococcal surfaces. Oral Microbiol Immunol 8:16–23Google Scholar
  131. Socransky SS, Haffajee AD, Cugini MA, Smith C, Kent RL Jr (1998) Microbial complexes in subgingival plaque. J Clin Periodontol 25:134–144Google Scholar
  132. Song W, Zhang J, Guo J et al (2010) Role of the dissolved zinc ion and reactive oxygen species in cytotoxicity of ZnO nanoparticles. Toxicol Lett 199:389–397Google Scholar
  133. Stewart PS (2002) Mechanisms of antibiotic resistance in bacterial biofilms. Int J Med Microbiol 292:107–113Google Scholar
  134. Suketa N, Sawase T, Kitaura H et al (2005) An antibacterial surface on dental implants, based on the photocatalytic bactericidal effect. Clin Implant Dent Relat Res 7:105–111Google Scholar
  135. Suri SS, Fenniri H, Singh B (2007) Nanotechnology-based drug delivery systems. J Occup Med Toxicol 2:16Google Scholar
  136. Sweeney LC, Dave J, Chambers PA, Heritage J (2004) Antibiotic resistance in general dental practice—a cause for concern? J Antimicrob Chemother 53:567–576Google Scholar
  137. Takahashi N (2005) Microbial ecosystem in the oral cavity: metabolic diversity in an ecological niche and its relationship with oral diseases. Int Congr Ser 1284:103–112Google Scholar
  138. Takahashi N, Schachtele CF (1990) Effect of pH on growth and proteolytic activity of Porphyromonas gingivalis and Bacteroides intermedius. J Dent Res 69:1244–1248Google Scholar
  139. Takahashi N, Saito K, Schachtele CF, Yamada T (1997) Acid tolerance of growth and neutralizing activity of Porphyromonas gingivalis, Prevotella intermedia and Fusobacterium nucleatum. Oral Microbiol Immunol 12:323–328Google Scholar
  140. Takatsuka T, Tanaka K, Iijima Y (2005) Inhibition of dentine demineralization by zinc oxide: in vitro and in situ studies. Dent Mater 21:1170–1177Google Scholar
  141. Talebiana N, Amininezhada SM, Doudi M (2013) Controllable synthesis of ZnO nanoparticles and their morphology-dependent antibacterial and optical properties. J Photochem Photobiol 120:66–73Google Scholar
  142. Tavassoli-Hojati S, Alaghemand H, Hamze F et al (2013) Antibacterial, physical and mechanical properties of flowable resin composites containing zinc oxide nanoparticles. Dent Mater 29:495–505Google Scholar
  143. Teles R, Wang CY (2011) Mechanisms involved in the association between periodontal diseases and cardiovascular disease. Oral Dis 17:450–461Google Scholar
  144. Témoin S, Chakaki A, Askari A et al (2012) Identification of oral bacterial DNA in synovial fluid of patients with arthritis with native and failed prosthetic joints. J Clin Rheumatol 18:117–121Google Scholar
  145. Tsuang YH, Sun JS, Huang YC et al (2008) Studies of photokilling of bacteria using titanium dioxide nanoparticles. Artif Organs 32:167–174Google Scholar
  146. Turnbaugh P, Ley R, Hamady M, Fraser-Liggett C, Knight R, Gordon JI (2007) The human microbiome project. Nature 449:804–810Google Scholar
  147. Valant J, Drobne D, Novak S (2012) Effect of ingested titanium dioxide nanoparticles on the digestive gland cell membrane of terrestrial isopods. Chemosphere 87:19–25Google Scholar
  148. Vandebriel RJ, De Jong WH (2012) A review of mammalian toxicity of ZnO nanoparticles. Nanotechnol Sci Appl 5:61–71Google Scholar
  149. Vargas-Reus MA, Memarzadeh K, Huang J, Ren GG, Allaker RP (2012) Antimicrobial activity of nanoparticulate metal oxides against peri-implantitis pathogens. Int J Antimicrob Agents 40:135–139Google Scholar
  150. Villedieu A, Diaz-Torres ML, Roberts AP et al (2004) Genetic basis of erythromycin resistance in oral bacteria. Antimicrob Agents Chemother 48:2298–2301Google Scholar
  151. von Moos N, Slaveykova VI (2014) Oxidative stress induced by inorganic nanoparticles in bacteria and aquatic microalgae—state of the art and knowledge gaps. Nanotoxicology 8:605–630Google Scholar
  152. Wang Z, Lee YH, Wu B et al (2010) Antimicrobial activities of aerosolized transition metal oxide nanoparticles. Chemosphere 80:525–529Google Scholar
  153. Wang J, Qi J, Zhao H et al (2013a) Metagenomic sequencing reveals microbiota and its functional potential associated with periodontal disease. Sci Rep 3:1843Google Scholar
  154. Wang X, Buhimschi CS, Temoin S, Bhandari V, Han YW, Buhimschi IA (2013b) Comparative microbial analysis of paired amniotic fluid and cord blood from pregnancies complicated by preterm birth and early-onset neonatal sepsis. PLoS ONE 8:e56131Google Scholar
  155. Warheit DB, Hoke RA, Finlay C et al (2007) Development of a base set of toxicity tests using ultrafine TiO2 particles as a component of nanoparticle risk management. Toxicol Lett 171:99–110Google Scholar
  156. Weir E, Lawlor A, Whelan A, Regan F (2008) The use of nanoparticles in anti-microbial materials and their characterization. Analyst 133:835–845Google Scholar
  157. Weir A, Westerhoff P, Fabricius L, von Goetz N (2012) Titanium dioxide nanoparticles in food and personal care products. Environ Sci Technol 46:2242–2250Google Scholar
  158. Whitmore SE, Lamont RJ (2014) Oral bacteria and cancer. PLoS Pathog 10:e1003933Google Scholar
  159. Williams RC (2000) Offenbacher S (2000) Periodontal medicine: the emergence of a new branch of periodontology. Periodontol 23:9–156Google Scholar
  160. Xi A, Bothun GD (2014) Centrifugation-based assay for examining nanoparticle-lipid membrane binding and disruption. Analyst 139:973–981Google Scholar
  161. Xie Y, He Y, Irwin PL, Jin T, Shi X (2011) Antibacterial activity and mechanism of action of zinc oxide nanoparticles against Campylobacter jejuni. Appl Environ Microbiol 77:2325–2331Google Scholar
  162. Ximénez-Fyvie LA, Haffajee AD, Socransky SS (2000) Comparison of the microbiota of supra- and subgingival plaque in health and periodontitis. J Clin Periodontol 27:648–657Google Scholar
  163. Yamanaka M, Hara K, Kudo J (2005) Bactericidal actions of a silver ion solution on Escherichia coli, studied by energy-filtering transmission electron microscopy and proteomic analysis. Appl Environ Microbiol 71:7589–7593Google Scholar
  164. Yu JX, Li TH (2011) Distinct biological effects of different nanoparticles commonly used in cosmetics and medicine coatings. Cell Biosci 1:19Google Scholar
  165. Zbinden A, Mueller NJ, Tarr PE et al (2012) Streptococcus tigurinus, a novel member of the Streptococcus mitis group, causes invasive infections. J Clin Microbiol 50:2969–2973Google Scholar
  166. Zhang L, Gu FX, Chan JM, Wang AZ (2008) Nanoparticles in medicine: therapeutic applications and developments. Clin Pharmacol Ther 83(5):761–769Google Scholar
  167. Zinkernagel AS, Timmer AM, Pence MA et al (2008) The IL-8 protease SpyCEP/ScpC of group A Streptococcus promotes resistance to neutrophil killing. Cell Host Microbe 4:170–178Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Shams Tabrez Khan
    • 1
    • 2
  • Abdulaziz A. Al-Khedhairy
    • 1
  • Javed Musarrat
    • 3
  1. 1.Department of Zoology, College of ScienceKing Saud UniversityRiyadhSaudi Arabia
  2. 2.Al-Jeraisy Chair for DNA Research, Department of Zoology, College of ScienceKing Saud UniversityRiyadhSaudi Arabia
  3. 3.Department of Agricultural Microbiology, Faculty of Agricultural SciencesAMUAligarhIndia

Personalised recommendations