Skip to main content
Log in

Antimicrobial and antibiofilm activity of silver nanoparticles against Salmonella Enteritidis

  • Food Microbiology - Research Paper
  • Published:
Brazilian Journal of Microbiology Aims and scope Submit manuscript

Abstract

Salmonella enterica serotype Enteritidis is one of the main pathogens associated with foodborne illnesses worldwide. Biofilm formation plays a significant role in the persistence of pathogens in food production environments. Owing to an increase in antimicrobial resistance, there is a growing need to identify alternative methods to control pathogenic microorganisms in poultry environments. Thus, this study aimed to synthesize silver nanoparticles (AgNPs) and evaluate their antibiofilm activity against poultry-origin Salmonella Enteritidis in comparison to a chemical disinfectant. AgNPs were synthesized, characterized, and tested for their minimum inhibitory concentration, minimum bactericidal concentration, and antibiofilm activity against S. Enteritidis strains on polyethylene surfaces. The synthesized AgNPs, dispersed in a liquid medium, were spherical in shape with a mean diameter of 6.2 nm. AgNPs exhibited concentration-dependent bactericidal action. The bacterial reduction was significantly higher with AgNPs (3.91 log10 CFU \(\bullet\) cm−2) than that with sanitizer (2.57 log10 CFU ∙ cm−2). Regarding the time of contact, the bacterial count after a contact time of 30 min was significantly lower than that after 10 min. The AgNPs exhibited antimicrobial and antibiofilm activity for the removal of biofilms produced by S. Enteritidis, demonstrating its potential as an alternative antimicrobial agent. The bactericidal mechanisms of AgNPs are complex; hence, the risk of bacterial resistance is minimal, making nanoparticles a potential alternative for microbial control in the poultry chain.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Availability of data and material

Not applicable.

Code availability

Not applicable.

References

  1. World Health Organization (2020) Food safety. https://www.who.int/news-room/fact-sheets/detail/food-safety Accessed 07 April 2020.

  2. Centers for Diseases Control and Prevention (2021) Salmonella. https://www.cdc.gov/salmonella/index.html Accessed 1 February 2021.

  3. European Food Safety Authority, European Centre for Disease Prevention and Control (2021) The European Union One Health 2019 Zoonoses Report. EFSA J 19:1–286. https://doi.org/10.2903/j.efsa.2021.6406

    Article  Google Scholar 

  4. Food Safety Brazil (2021) Surtos alimentares no Brasil – Dados atualizados em junho de 2018. https://foodsafetybrazil.org/surtos-alimentares-no-brasil-dados-atualizados-junho-de-2018-2 Accessed 21 February 2021.

  5. Center for Disease Control and Prevention – CDC (2011) Making food safer to eat: reducing contamination from the farm to the table. www.cdc.gov/vitalsigns/foodsafety/ Accessed 05 December 2021

  6. Melo ANF, Monte DFM, Pedrosa GTS, Balkey M, Jin Q, Brown E, Allard M, de Oliveira TCRM, Cao G, Magnani M, Macarisin D (2021) Genomic investigation of antimicrobial resistance determinants and virulence factors in Salmonella enterica serovars isolated from contaminated food and human stool samples in Brazil. Int J Food Microbiol 343:109091. https://doi.org/10.1016/j.ijfoodmicro.2021.109091

    Article  CAS  PubMed  Google Scholar 

  7. Galié S, García-Gutiérrez C, Miguélez EM, Villar CJ, Lombó F (2018) Biofilms in the food industry: health aspects and control methods. Front Microbiol 9:1–18. https://doi.org/10.3389/fmicb.2018.00898

    Article  Google Scholar 

  8. Vestby LK, Grønseth T, Simm R, Nesse LL (2020) Bacterial biofilm and its role in the pathogenesis of disease. Antibiotics 9:1–29. https://doi.org/10.3390/antibiotics9020059

    Article  CAS  Google Scholar 

  9. Borges KA, Furian TQ, Souza SN, Menezes R, Tondo EC, Moraes HLS, Salle CTP, Nascimento VP (2018) Biofilm formation capacity of Salmonella serotypes at different temperature conditions. Pesq Vet Bras 38:71–76. https://doi.org/10.1590/1678-5150-PVB-4928

    Article  Google Scholar 

  10. Merino L, Procura F, Trejo FM, Bueno DJ, Golowczyc MA (2019) Biofilm formation by Salmonella sp. in the poultry industry: detection, control and eradication strategies. Food Res Int 119:530–540. https://doi.org/10.1016/j.foodres.2017.11.024

    Article  PubMed  Google Scholar 

  11. Webber B, Oliveira AP, Pottker ES, Daroit L, Levandowski R, Santos LR, Nascimento VP, Rodrigues LB (2019) Salmonella Enteritidis forms biofilm under low temperatures on different food industry surfaces. Cienc Rural 49:1–9. https://doi.org/10.1590/0103-8478cr20181022

    Article  CAS  Google Scholar 

  12. Obe T, Nannapaneni R, Schilling W, Zhang L, Kiess A (2021) Antimicrobial tolerance, biofilm formation, and molecular characterization of Salmonella isolates from poultry processing equipment. J Appl Poult Res 30:100195. https://doi.org/10.1016/j.japr.2021.100195

    Article  CAS  Google Scholar 

  13. Pontin KP, Borges KA, Furian TQ, Carvalho D, Wilsmann DE, Cardoso HRP, Alves AK, Chitolina GZ, Salle CTP, Moraes HLS, do Nascimento VP, (2021) Antimicrobial activity of copper surfaces against biofilm formation by Salmonella Enteritidis and its potential application in the poultry industry. Food Microbiol 94:103645. https://doi.org/10.1016/j.fm.2020.103645

    Article  CAS  PubMed  Google Scholar 

  14. Wang L, Hu C, Shao L (2017) The antimicrobial activity of nanoparticles: present situation and prospects for the future. Int J Nanomedicine 12:1227–1249. https://doi.org/10.2147/ijn.s121956

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Khan I, Saeed K, Khan I (2019) Nanoparticles: properties, applications and toxicities. Arabian J Chem 12:908–931. https://doi.org/10.1016/j.arabjc.2017.05.011

    Article  CAS  Google Scholar 

  16. Khezerlou A, Alizadeh-Sani M, Azizi-Lalabadi M, Ehsani A (2018) Nanoparticles and their antimicrobial properties against pathogens including bacteria, fungi, parasites and viruses. Microb Pathog 123:505–526. https://doi.org/10.1016/j.micpath.2018.08.008

    Article  CAS  PubMed  Google Scholar 

  17. Elez RMMA, Elsohaby I, El-Gazzar N, Tolba HMN, Abdelfatah EN, Abdellatif SS, Mesalam AA, Tahoun ABMB (2021) Antimicrobial resistance of Salmonella Enteritidis and Salmonella Typhimurium isolated from laying hens, table eggs, and humans with respect to antimicrobial activity of biosynthesized silver nanoparticles. Animals 11:3554. https://doi.org/10.3390/ani11123554

    Article  PubMed  PubMed Central  Google Scholar 

  18. Loo YY, Rukayadi Y, Nor-Khaizura MA, Kuan CH, Chieng BW, Nishibuchi M, Radu S (2018) In vitro antimicrobial activity of green synthesized silver nanoparticles against selected Gram-negative foodborne pathogens. Front Microbiol 16:1555. https://doi.org/10.3389/fmicb.2018.01555

    Article  Google Scholar 

  19. El-Gohary FA, Abdel-Hafez LJM, Zakaria AI, Shata RR, Tahoun A, El-Mleeh A, Abo Elfadl EA, Elmahallawy EK (2020) Enhanced antibacterial activity of silver nanoparticles combined with hydrogen peroxide against multidrug-resistant pathogens isolated from dairy farms and beef slaughterhouses in Egypt. Infect Drug Resist 13:3485–3499. https://doi.org/10.2147/idr.s271261

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Redel E, Thomann R, Janiak C (2008) First correlation of nanoparticle size-dependent formation with the ionic liquid anion molecular volume. Inorg Chem 47:14–16. https://doi.org/10.1021/ic702071w

    Article  CAS  PubMed  Google Scholar 

  21. Farina M (2010) Uma introdução à microscopia eletrônica de transmissão. Livraria da Física, São Paulo

    Google Scholar 

  22. Scheeren CW, Machado G, Teixeira SR, Morais J, Domingos JB, Dupont J (2006) Synthesis and characterization of Pt0 nanoparticles in imidazolium ionic liquids. J Phys Chem B 110:13011–20. https://doi.org/10.1021/jp0623037

    Article  CAS  PubMed  Google Scholar 

  23. Mourdikoudis S, Pallares RM, Thanh NTK (2018) Characterization techniques for nanoparticles: comparison and complementarity upon studying nanoparticle properties. Nanoscale 10:12871–12934. https://doi.org/10.1039/c8nr02278j

    Article  CAS  PubMed  Google Scholar 

  24. Duffy LL, Osmond-McLeod MJ, Judy J, King T (2018) Investigation into the antibacterial activity of silver, zinc oxide and copper oxide nanoparticles against poultry-relevant isolates of Salmonella and Campylobacter. Food Contr 92:293–300. https://doi.org/10.1016/j.foodcont.2018.05.008

    Article  CAS  Google Scholar 

  25. Milles AA, Misra SS (1938) The estimation of the bacterial power of the blood. J Hyg 38:732–749. https://doi.org/10.1017/s002217240001158x

    Article  Google Scholar 

  26. Gibson H, Taylor JH, Hall KE, Holah JT (1999) Effectiveness of cleaning techniques used in the food industry in terms of the removal of bacterial bioflms. J Appl Microbiol 87:41–48. https://doi.org/10.1046/j.1365-2672.1999.00790.x

    Article  CAS  PubMed  Google Scholar 

  27. International Organization for Standardization – ISO (2018) Microbiology of food and animal feeding stuffs - horizontal methods for sampling techniques from surfaces using contact plates and swabs, p 11

  28. Rossi DA, Melo RT, Mendonça EP, Monteiro GP (2017) Biofilms of Salmonella and Campylobacter in the poultry industry. In: Manafi M (ed) Poultry Science. IntechOpen, London, pp 93–113

    Google Scholar 

  29. Arnold JW, Silvers S (2000) Comparison of poultry processing equipment surfaces for susceptibility to bacterial attachment and biofilm formation. Poult Sci 79:1215–1221. https://doi.org/10.1093/ps/79.8.1215

    Article  CAS  PubMed  Google Scholar 

  30. Sinde E, Carballo J (2000) Attachment of Salmonella sp. and Listeria monocytogenes to stainless steel, rubber and polytetrafluorethylene: the influence of free energy and the effect of commercial sanitizers. Food Microbiol 17:439–447. https://doi.org/10.1006/fmic.2000.0339

    Article  CAS  Google Scholar 

  31. Zang YT, Li BM, Bing SH, Cao W (2015) Modeling disinfection of plastic poultry transport cages inoculated with Salmonella Enteritidis by slightly acidic electrolyzed water using response surface methodology. Poult Sci 94:2059–2065. https://doi.org/10.3382/ps/pev188

    Article  CAS  PubMed  Google Scholar 

  32. Prestinaci F, Pezzotti P, Pantosti A (2015) Antimicrobial resistance: a global multifaceted phenomenon. Pathog Glob Healt 109(7):309–318. https://doi.org/10.1179/2047773215y.0000000030

    Article  Google Scholar 

  33. Beyth N, Houri-Haddad Y, Domb A, Khan W, Hazan R (2015) Alternative antimicrobial approach: nano-antimicrobial materials. Evid Based Complementary Altern Med 2015:246012. https://doi.org/10.1155/2015/246012

  34. Zewde B, Ambaye A, Stubbs J, Raghavan D (2016) A review of stabilized silver nanoparticles – synthesis, biological properties, characterization, and potential areas of applications. JSM Nanotechnol Nanomed 4:1043

    Google Scholar 

  35. Franci G, Falanga A, Galdiero S, Palomba L, Rai M, Morelli G, Galdiero M (2015) Silver nanoparticles as potential antibacterial agents. Molecules 20:8856–8874. https://doi.org/10.3390/molecules20058856

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Sharma D, Misba L, Khan AU (2019) Antibiotics versus biofilm: an emerging battleground in microbial communities. Antimicrob Resist Infect Control 8:76. https://doi.org/10.1186/s13756-019-0533-3

    Article  PubMed  PubMed Central  Google Scholar 

  37. Ismail AEA, Kotb SAH, Mohamed IMA, Abdel-Mohsein HS (2019) Inhibitory activity of silver nanoparticles and sodium hypochlorite against biofilm produced by Salmonellae isolated from poultry farms. J Adv Vet Anim Res 9:151–160

    Google Scholar 

  38. Malaekeh-Nikouei B, Bazzaz BSF, Mirhadi E, Tajani AS, Khameneh B (2020) The role of nanotechnology in combating biofilm-based antibiotic resistance. J Drug Deliv Sci Technol 60:101880. https://doi.org/10.1016/j.jddst.2020.101880

    Article  CAS  Google Scholar 

  39. Yuan L, Sadiq FA, Wang N, Yang Z, He G (2020) Recent advances in understanding the control of disinfectant-resistant biofilms by hurdle technology in the food industry. Crit Rev Food Sci Nutr 25:1–16. https://doi.org/10.1080/10408398.2020.1809345

    Article  CAS  Google Scholar 

  40. Brazil, Ministry of Agriculture, Livestock and Supply (1998) Portaria SDA/MAPA 210/98. http://sistemasweb.agricultura.gov.br/sislegis/action/detalhaAto.do?method=recuperarTextoAtoTematicaPortalandcodigoTematica=1864168 Accessed 05 June 2019.

  41. Brazil, Ministry of Agriculture, Livestock and Supply (2005) Circular N° 175/2005/CGPE/DIPOA. http://dzetta.com.br/info/wp-content/uploads/2011/06/dzetta-Circular-175-de-16-de-maio-de-2005.pdf Accessed 05 June 05 2019.

  42. Dat NM, Linh VNP, Phuong NTL, Quan LN, Huong NT, Huy LA, Nam HM, Phong MT, Hieu NH (2019) The effects of concentration, contact time, and pH value on antibacterial activity of silver nanoparticles decorated reduced graphene oxide. Mater Technol 34:792–799. https://doi.org/10.1080/10667857.2019.1630898

    Article  Google Scholar 

  43. Union European (2001) NS-EN 13697:2001: Quantitative non-porous surface test for the evaluation of bactericidal and/or fungicidal activity of chemical disinfectants used in food, industrial, domestic and institutional areas Test method and requirements without mechanical action. European Committee for standardization, Brussels, Belgium

    Google Scholar 

  44. Moretro T, Vestby LK, Nesse LL, Hannevik S, Kotlarz K, Lansrud S (2019) Evaluation of efficiency of disinfectants against salmonella from the feed industry. J Appl Microbiol 106:1005–1012. https://doi.org/10.1111/j.1365-2672.2008.04067.x

    Article  Google Scholar 

Download references

Funding

This work was supported by the National Council for Scientific and Technological Development (CNPq) through a scholarship concession to Brunna Dias de Emery.

Author information

Authors and Affiliations

Authors

Contributions

B. D. E., M. I. Q., T. Q. F., C. T. P. S., H. L. S. M., and V. P. N. conceived and designed the experiments. B. D. E., G. Z. C., and M. I. Q. performed experiments. B. D. E., K. A. B., and T. Q. F. analyzed the data. B. D. E., K. A. B., and T. Q. F. prepared the manuscript. All authors critically reviewed and approved the manuscript.

Corresponding author

Correspondence to Karen Apellanis Borges.

Ethics declarations

Ethics approval

Not applicable.

Consent to participate

Not applicable.

Consent for publication

All authors provided consent for the publication of this manuscript.

Competing interests

The authors declare no competing interests.

Additional information

Responsible Editor: Luis Augusto Nero

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dias de Emery, B., Zottis Chitolina, G., Qadir, M.I. et al. Antimicrobial and antibiofilm activity of silver nanoparticles against Salmonella Enteritidis. Braz J Microbiol 54, 285–292 (2023). https://doi.org/10.1007/s42770-022-00868-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42770-022-00868-1

Keywords

Navigation