Abstract
Nisin, a bacteriocin widely used in the food industry, and curcumin, the yellow pigment extracted from turmeric (Curcuma longa L.) stand out among the numerous natural preservatives that have antimicrobial activity. The conversion of these compounds into nanoparticles could be interesting as an alternative to improve technological aspects (such as the low water solubility of curcumin) and to evaluate how synergism could take place in the case of co-encapsulation. The main objective of the present work was to evaluate the combination of nisin (Nis) with nanoencapsulated curcumin (NCur, nanoencapsulated to promote water solubility), as well as the co-encapsulated curcumin and nisin (NCurNis), against the foodborne bacteria Staphylococcus aureus, Escherichia coli and Salmonella Typhimurium. Minimum inhibitory concentration and the minimum bactericidal concentration were evaluated for NCur and Nis, as well as their combination with the fractional inhibitory concentration assay. High effectiveness was found against S. aureus and the combination of both compounds resulted in Nis- nisin; synergism against the same microorganism. The co-encapsulation of curcumin and nisin was carried out based on the synergism tests and the characterization analyses demonstrated that a solid dispersion of the components in the PVP matrix was formed. The inhibitory effect of the curcumin and nisin co-encapsulate was improved when compared to the curcumin nanoparticles or nisin alone.
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Data availability
The datasets used and/or analyzed during the current study are available from the corresponding author upon reasonable request.
Abbreviations
- BHI:
-
Brain heart infusion
- EMB:
-
Eosin methylene blue agar
- ESBL:
-
Extended-spectrum beta-lactamases
- DLS:
-
Dynamic light scattering
- DSC:
-
Differential scanning calorimetry
- Dz:
-
Mean intensity diameter
- FIC:
-
Fractional inhibitory concentration
- FTIR:
-
Fourier transform infrared spectroscopy
- HCl:
-
Hydrochloric acid
- KBr:
-
Potassium bromide
- MBC:
-
Minimum bactericidal concentration
- MFCurNisPVP:
-
Physical mixture of curcumin, nisin, and polyvinylpyrrolidone
- MFCurPVP:
-
Physical mixture of curcumin and polyvinylpyrrolidone
- MHA:
-
Mueller hinton agar
- MHB:
-
Mueller hinton broth
- MIC:
-
Minimum inhibitory concentration
- MRSA:
-
Methicillin-resistant Staphylococcus aureus
- MSSA:
-
Methicillin-susceptible Staphylococcus aureus
- NCur:
-
Nanoencapsulated curcumin
- NCurNis:
-
Co-encapsulated curcumin and nisin
- Nis:
-
Nisin
- PDI:
-
Polydispersity index
- PVP:
-
Polyvinylpyrrolidone
- TEM:
-
Transmission electron microscopy
- TGA:
-
Thermogravimetric analysis
References
Gruskiene R, Kavleiskaja T, Staneviciene R, et al. (2021) Nisin-loaded ulvan particles: preparation and characterization. 10.3390/foods10051007
Almeida HHS, Barros L, Barreira JCM et al (2018) Bioactive evaluation and application of different formulations of the natural colorant curcumin (E100) in a hydrophilic matrix (yogurt ). Food Chem 261:224–232. https://doi.org/10.1016/j.foodchem.2018.04.056
Chawda PJ, Shi J, Xue S, Quek SY (2017) Co-encapsulation of bioactives for food applications. Food Qual Saf 1(4):302–309. https://doi.org/10.1093/fqsafe/fyx028
Chen L, Song Z, Tan SY et al (2020) Application of bacteriocins produced from lactic acid bacteria for microbiological food safety. Curr Topic Lactic Acid Bact Probiotics 6:1–8
CLSI (2012) Performance standards for antimicrobial susceptibility testing; twenty-second informational supplement
da Rosa FC, Nogueira AL, Deretti O (2021) Caracterização de micropartículas de plla contendo curcumina pela técnica de emulsificação/evaporação de solvente/characterization of plla microparticles containing curcumin by solvent emulsification/evaporation technique. Braz J Dev 7(3):28837–28847. https://doi.org/10.34117/bjdv7n3-548
Doern CD (2014) When does 2 plus 2 equal 5? A review of antimicrobial synergy testing. J Clin Microbiol 52:4124–4128. https://doi.org/10.1128/JCM.01121-14
Field D, Begley M, O’Connor PM et al (2012) Bioengineered nisin a derivatives with enhanced activity against both gram positive and gram negative pathogens. PLoS ONE 7:e46884. https://doi.org/10.1371/journal.pone.0046884
Furlanetto A (2020) Síntese de nanoemulsão e nanopartícula de ouro (AuNPs) contendo nisina e seus efeitos sobre os fatores de virulência de Staphylococcus aureus. Universidade Estadual Paulista Julio de Mesquita Filho
Kamaruddin ED, Sriyanti I et al (2017) Synthesis of polyvinylpyrrolidone (PVP)-green tea extract composite nanostructures using electrohydrodynamic spraying technique. IOP Conf Ser Mater Sci Eng 202:1–8. https://doi.org/10.1088/1757-899X/202/1/012043
Karavas E, Ktistis G, Xenakis A, Georgarakis E (2006) Effect of hydrogen bonding interactions on the release mechanism of felodipine from nanodispersions with polyvinylpyrrolidone. Eur J Pharm Biopharm 63:103–114. https://doi.org/10.1016/j.ejpb.2006.01.016
Kaszuba M, McKnight D, Connah MT et al (2008) Measuring sub nanometre sizes using dynamic light scattering. J Nanopart Res 10:823–829. https://doi.org/10.1007/s11051-007-9317-4
Khan I, Oh DH (2016) Integration of nisin into nanoparticles for application in foods. Innov Food Sci Emerg Technol 34:376–384. https://doi.org/10.1016/j.ifset.2015.12.013
Khan WH, Rathod VK (2014) Process intensification approach for preparation of curcumin nanoparticles via solvent-nonsolvent nanoprecipitation using spinning disc reactor. Chem Eng Process 80:1–10. https://doi.org/10.1016/j.cep.2014.03.011
Lemes GF, Marchiore NG, Moreira TFM et al (2017) Enzymatically crosslinked gelatin coating added of bioactive nanoparticles and antifungal agent: effect on the quality of Benitaka grapes. LWT Food Sci Technol 84:175–182. https://doi.org/10.1016/j.lwt.2017.05.050
Leyva-Diaz A, Hernandez-Patlan D, Solis-Cruz B et al (2020) Evaluation of curcumin and copper acetate against salmonella typhimurium infection, intestinal permeability, and cecal microbiota composition in broiler chickens. J Anim Sci Biotechnol. https://doi.org/10.21203/rs.3.rs-42229/v1
Luo L, Wu Y, Liu C et al (2021) Elaboration and characterization of curcumin-loaded soy soluble polysaccharide (SSPS)-based nanocarriers mediated by antimicrobial peptide nisin. Food Chem 336:127669. https://doi.org/10.1016/J.FOODCHEM.2020.127669
Ma S, Moser D, Han F et al (2020) Preparation and antibiofilm studies of curcumin loaded chitosan nanoparticles against polymicrobial biofilms of Candida albicans and Staphylococcus aureus. Carbohydr Polym. https://doi.org/10.1016/j.carbpol.2020.116254
Meral R, Alav A, Karakas CY et al (2019) Effect of electrospun nisin and curcumin loaded nanomats on the microbial quality, hardness and sensory characteristics of rainbow trout fillet. LWT 113:108292. https://doi.org/10.1016/J.LWT.2019.108292
Niaz T, Shabbir S, Noor T et al (2018a) Polyelectrolyte multicomponent colloidosomes loaded with nisin Z for enhanced antimicrobial activity against foodborne resistant pathogens. Front Microbiol 8:1–19. https://doi.org/10.3389/fmicb.2017.02700
Niaz T, Shabbir S, Noor T et al (2018b) Potential of polymer stabilized nano-liposomes to enhance antimicrobial activity of nisin Z against foodborne pathogens. Lwt. https://doi.org/10.1016/j.lwt.2018.05.029
Oyeyemi O, Adegbeyeni O, Oyeyemi I et al (2018) In vitro ovicidal activity of poly lactic acid curcumin-nisin co-entrapped nanoparticle against Fasciola spp. eggs and its reproductive toxicity. J Basic Clin Physiol Pharmacol 29:73–79. https://doi.org/10.1515/jbcpp-2017-0045
Pakbin B, Brück WM, Rossen JWA (2021) Virulence factors of enteric pathogenic Escherichia coli: a review. Int J Mol Sci. https://doi.org/10.3390/ijms22189922
Sharma G, Dang S, Kalia M, Gabrani R (2020) Synergistic antibacterial and anti-biofilm activity of nisin like bacteriocin with curcumin and cinnamaldehyde against ESBL and MBL producing clinical strains. Biofouling 36:710–724. https://doi.org/10.1080/08927014.2020.1804553
Souza JF, Souza ACF, Costa FN (2021) Estudo retrospectivo de surtos de doenças veiculadas por alimentos, na região nordeste e Estado do Maranhão, no período de 2007 a 2019. Res Soc Dev 10(1):e36010111728. https://doi.org/10.33448/rsd-v10i1.11728
Taghavifar S, Afroughi F, SaadatiKeyvan M (2020) Curcumin nanoparticles improved diabetic wounds infected with methicillin-resistant staphylococcus aureus sensitized with HAMLET. Int J Lower Extrem Wounds. https://doi.org/10.1177/1534734620933079
Takundwa BA, Bhagwat P, Pillai S, Ijabadeniyi OA (2021) Antimicrobial efficacy of nisin, oregano and ultrasound against Escherichia coli O157:H7 and Listeria monocytogenes on lettuce. Lwt 139:110522. https://doi.org/10.1016/j.lwt.2020.110522
Tyagi P, Singh M, Kumari H et al (2015) Bactericidal activity of curcumin I is associated with damaging of bacterial membrane. PLoS ONE. https://doi.org/10.1371/journal.pone.0121313
Voronova M, Rubleva N, Kochkina N et al (2018) Preparation and characterization of polyvinylpyrrolidone/cellulose nanocrystals composites. Nanomaterials. https://doi.org/10.3390/nano8121011
World Health Organization (2022) Foodborne diseases. https://www.who.int/health-topics/foodborne-diseases#tab=tab_1. Accessed 12 Jan 2022
Yeluri Jonnala BR, Feehily C, O’Connor PM et al (2021) Assessing the ability of nisin A and derivatives thereof to inhibit gram-negative bacteria from the genus Thermus. J Dairy Sci 104:2632–2640. https://doi.org/10.3168/jds.2020-19350
Zhao X, Zhen Z, Wang X, Guo N (2017) Synergy of a combination of nisin and citric acid against Staphylococcus aureus and Listeria monocytogenes. Food Addit Contam Part A Chem Anal Control Expo Risk Assess 34:2058–2068. https://doi.org/10.1080/19440049.2017.1366076
Acknowledgements
This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code 001. The authors thank the “Central Analítica Multiusuário da UTFPR Campo Mourão” (CAMulti-CM) for the analyses. Authors thank to CNPq (process number 406966/2021-4, Chamada CNPq/MCTI/FNDCT Nº 18/2021—Faixa A—Grupos Emergentes, and process number 310052/2021-1, Chamada CNPq Nº 4/2021—Bolsas de Produtividade em Pesquisa – PQ).
Funding
This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code 001 and CNPq (process number 406966/2021-4, Chamada CNPq/MCTI/FNDCT Nº 18/2021-Faixa A—Grupos Emergentes, and process number 310052/2021-1.
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MBQ: Investigation, Formal analysis, Writing—Original Draft. TFMM: Investigation, Formal analysis, Writing—Original Draft. AO: Investigation, Formal analysis, Writing—Original Draft. ASC: Investigation, Formal analysis, Writing—Original Draft. JLM: Investigation, Formal analysis, Writing—Original Draft. OHG: Conceptualization, Supervision, Writing—Review & Editing. BAAF: Conceptualization, Supervision, Writing—Review & Editing. FVL: Conceptualization, Supervision, Project administration, Funding acquisition, Writing—Review & Editing.
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Quichaba, M.B., Moreira, T.F.M., de Oliveira, A. et al. Biopreservatives against foodborne bacteria: combined effect of nisin and nanoncapsulated curcumin and co-encapsulation of nisin and curcumin. J Food Sci Technol 60, 581–589 (2023). https://doi.org/10.1007/s13197-022-05641-8
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DOI: https://doi.org/10.1007/s13197-022-05641-8