Indian Journal of Microbiology

, Volume 59, Issue 2, pp 147–153 | Cite as

Antimicrobial Activity of Compounds Containing Silver Nanoparticles and Calcium Glycerophosphate in Combination with Tyrosol

  • José Antonio Santos Souza
  • Debora Barros Barbosa
  • Jackeline Gallo do Amaral
  • Douglas Roberto Monteiro
  • Luiz Fernando Gorup
  • Francisco Nunes de Souza Neto
  • Renan Aparecido Fernandes
  • Gabriela Lopes Fernandes
  • Emerson Rodrigues de Camargo
  • Alessandra Marçal Agostinho
  • Alberto Carlos Botazzo DelbemEmail author
Original research article


Nanocomposites containing antimicrobial agents and calcium phosphates have been developed. Thus, this study assessed the effects of two compounds containing silver nanoparticles (AgNPs) and β-calcium glycerophosphate (CaGP), associated or not with tyrosol (TYR), against planktonic cells and biofilms of Candida albicans and Streptococcus mutans. The nanocompounds were synthesized through chemical and ‘green’ processes and characterized by scanning electron microscopy. The minimum and fractional inhibitory concentrations of each compound were determined for planktonic cells. Next, 24-h single biofilms of C. albicans and S. mutans were treated for 24 h with the nanocompounds alone or in combination with TYR, and the antibiofilm effect was assessed through enumeration of colony forming units. Biofilm data were statistically examined using one-way ANOVA and the Kruskal–Wallis test (α = 0.05). The chemically synthesized nanocompound in combination with TYR demonstrated a synergistic effect against planktonic cells of C. albicans and S. mutans. For the nanocompound obtained through the ‘green’ route associated with TYR, a synergistic effect was observed only against C. albicans. For biofilms, only the combination obtained through the ‘green’ route + TYR demonstrated a synergistic effect against C. albicans. Our results may contribute to the development of oral care products containing AgNPs–CaGP and TYR to combat oral infections.


Metal nanoparticles Polyphosphates Biofilms Candida albicans Streptococcus mutans 



This work was supported by the Coordination for the Improvement of Higher Education Personnel (CAPES, Processes 88881.030445/2013-01 and 88887.068358/2014-00) and the São Paulo Research Foundation (FAPESP, process 2015/00825-5).


  1. 1.
    Struzycka I (2014) The oral microbiome in dental caries. Pol J Microbiol 63:127–135Google Scholar
  2. 2.
    Fragkou S, Balasouli C, Tsuzukibashi O, Argyropoulou A, Menexes G, Kotsanos N, Kalfas S (2016) Streptococcus mutans, Streptococcus sobrinus and Candida albicans in oral samples from caries-free and caries-active children. Eur Arch Paediatr Dent 17:367–375. CrossRefGoogle Scholar
  3. 3.
    Arias LS, Delbem AC, Fernandes RA, Barbosa DB, Monteiro DR (2016) Activity of tyrosol against single and mixed-species oral biofilms. J Appl Microbiol 120:1240–1249. CrossRefGoogle Scholar
  4. 4.
    Samiei M, Farjami A, Dizaj SM, Loftipour F (2016) Nanoparticles for antimicrobial purposes in Endodontics: a systematic review of in vitro studies. Mater Sci Eng C Mater Biol Appl 58:1269–1278. CrossRefGoogle Scholar
  5. 5.
    Noronha VT, Paula AJ, Durán G, Galembeck A, Cogo-Müller K, Franz-Montan M, Durán N (2017) Silver nanoparticles in dentistry. Dent Mater 33:1110–1126. CrossRefGoogle Scholar
  6. 6.
    Otari SV, Pawar SH, Patel SKS, Singh RK, Kim SY, Lee LH, Zhang L, Lee JK (2017) Canna edulis leaf extract-mediated preparation of stabilized silver nanoparticles: characterization, antimicrobial activity, and toxicity studies. J Microbiol Biotechnol 27:731–738. CrossRefGoogle Scholar
  7. 7.
    Manasathien J, Indrapichate K, Intarapichet OK (2012) Antioxidant activity and bioefficacy of pomegranate Punica granatum Linn peel and seed extracts. Glob J Pharmacol 6:131–141. Google Scholar
  8. 8.
    Danelon M, Pessan JP, Souza-Neto FN, de Camargo ER, Delbem AC (2017) Effect to fluoride toothpaste with nano-sized trimetaphosphate on enamel demineralization: an in vitro study. Arch Oral Biol 78:82–87. CrossRefGoogle Scholar
  9. 9.
    Conceição JM, Delbem AC, Danelon M, da Camara DM, Wiegand A, Pessan JP (2015) Fluoride gel supplemented with sodium hexametaphosphate reduces enamel erosive wear in situ. J Dent 43:1255–1260. CrossRefGoogle Scholar
  10. 10.
    Manarelli MM, Delbem ACB, Báez-Quintero LC, de Moraes FRN, Cunha RF, Pessan JP (2017) Fluoride varnishes containing sodium trimetaphosphate reduce enamel demineralization in vitro. Acta Odontol Scand 75:376–378. CrossRefGoogle Scholar
  11. 11.
    McGaughey C, Stowell EC (1977) Effects of polyphosphates on the solubility and mineralization of HA: relevance to a rationale for anticaries activity. J Dent Res 56:579–587. CrossRefGoogle Scholar
  12. 12.
    Fernandes GL, Delbem ACB, do Amaral JG, Gorup LF, Fernandes RA, de Souza-Neto FN, Souza JAS, Monteiro DR, Hunt AMA, Camargo ER, Barbosa DB (2018) Nanosynthesis of silver-calcium glycerophosphate: promising association against oral pathogens. Antibiotics (Basel) 7:E52. CrossRefGoogle Scholar
  13. 13.
    Souza JA, Barbosa DB, Silva AA, do Amaral JG, Gorup LF, de Souza Neto FN, Fernandes RA, Fernandes GL, Camargo ER, Agostinho AM, Delbem AC (2018) Green synthesis of silver nanoparticles combined to calcium glycerophosphate: antimicrobial and antibiofilm activities. Future Microbiol 13:345–357. CrossRefGoogle Scholar
  14. 14.
    Takamiya AS, Monteiro DR, Bernabé DG, Gorup LF, Camargo ER, Gomes-Filho JE, Oliveira SH, Barbosa DB (2016) In vitro and in vivo toxicity evaluation of colloidal silver nanoparticles used in endodontic treatments. J Endod 42:953–960. CrossRefGoogle Scholar
  15. 15.
    Shanmughapriya S, Sornakumari H, Lency A, Kavitha S, Natarajaseenivasan K (2014) Synergistic effect of amphotericin B and tyrosol on biofilm formed by Candida krusei and Candida tropicalis from intrauterine device users. Med Mycol 52:853–861. CrossRefGoogle Scholar
  16. 16.
    Monteiro DR, Feresin LP, Arias LS, Barão VA, Barbosa DB, Delbem AC (2015) Effect of tyrosol on adhesion of Candida albicans and Candida glabrata to acrylic surfaces. Med Mycol 53:656–665. CrossRefGoogle Scholar
  17. 17.
    Kalia VC, Patel SKS, Kang YC, Lee JK (2019) Quorum sensing inhibitors as antipathogens: biotechnological applications. Biotechnol Adv 37:68–90. CrossRefGoogle Scholar
  18. 18.
    Gorup LF, Longo E, Leite ER, Camargo ER (2011) Moderating effect of ammonia on particle growth and stability of quasi-monodisperse silver nanoparticles sunthesized by the Turkevich method. J Colloid Interface Sci 360:355–358. CrossRefGoogle Scholar
  19. 19.
    Wei GX, Bobek LA (2004) In vitro synergic antifungal effect of MUC7 12-mer with histatin-5 12-mer or miconazole. J Antimicrob Chemother 53:750–758. CrossRefGoogle Scholar
  20. 20.
    Miceli MH, Bernardo SM, Lee SA (2009) In vitro analyses of the combination of high-dose doxycycline and antifungal agents against Candida albicans biofilms. Int J Amtimicrob Agents 34:326–332. CrossRefGoogle Scholar
  21. 21.
    Kumari A, Guliani A, Singla R, Yadav R, Yadav SK (2015) Silver nanoparticles synthesized using plant extracts show strong antibacterial activity. IET Nanobiotechnol 9:142–152. CrossRefGoogle Scholar
  22. 22.
    Goudarzi M, Mir N, Mousavi-Kamazani M, Bagheri S, Salavati-Niasari M (2016) Biosynthesis and characterization of silver nanoparticles prepared from two novel natural precursors by facile thermal decomposition methods. Sci Rep 6:32539. CrossRefGoogle Scholar
  23. 23.
    Cordeiro RA, Teixeira CE, Brilhante RS, Castelo-Branco DS, Alencar LP, de Oliveira JS, Monteiro AJ, Bandeira TJ, Sidrim JJ, Moreira JL, Rocha MF (2015) Exogenous tyrosol inhibits planktonic cells and biofilms of Candida species and enhances their susceptibility to antifungals. FEMS Yeast Res 15:fov012. CrossRefGoogle Scholar
  24. 24.
    Rizzello L, Pompa PP (2014) Nanosilver-based antibacterial drugs and devices: mechanisms, methodological draebacks, and guidelines. Chem Soc Rev 43:1501–1518. CrossRefGoogle Scholar
  25. 25.
    Monteiro DR, Arias LS, Fernandes RA, Straioto FG, Barros Barbosa D, Pessan JP, Delbem ACB (2017) Role of tyrosol on Candida albicans, Candida glabrata and Streptococcus mutans biofilms developed on different surfaces. Am J Dent 30:35–39Google Scholar

Copyright information

© Association of Microbiologists of India 2019

Authors and Affiliations

  • José Antonio Santos Souza
    • 1
  • Debora Barros Barbosa
    • 1
  • Jackeline Gallo do Amaral
    • 1
  • Douglas Roberto Monteiro
    • 2
  • Luiz Fernando Gorup
    • 3
  • Francisco Nunes de Souza Neto
    • 4
  • Renan Aparecido Fernandes
    • 5
  • Gabriela Lopes Fernandes
    • 1
  • Emerson Rodrigues de Camargo
    • 4
  • Alessandra Marçal Agostinho
    • 6
  • Alberto Carlos Botazzo Delbem
    • 1
    Email author
  1. 1.Department of Pediatric Dentistry and Public Health, School of DentistrySão Paulo State University (UNESP)AraçatubaBrazil
  2. 2.Graduate Program in Dentistry (GPD – Master’s Degree)University of Western São Paulo (UNOESTE)Presidente PrudenteBrazil
  3. 3.Federal University of Grande DouradosDouradosBrazil
  4. 4.Federal University of São CarlosSão CarlosBrazil
  5. 5.University Center of Adamantina (UNIFAI)AdamantinaBrazil
  6. 6.Michigan State UniversityEast LansingUSA

Personalised recommendations