Application of silver nanoparticles in food packages: a review

Emelda Orlando SIMBINE Larissa da Cunha RODRIGUES Judite LAPA-GUIMARÃES Eliana Setsuko KAMIMURA Carlos Humberto CORASSIN Carlos Augusto Fernandes de OLIVEIRA About the authors

Abstract

Silver nanoparticles (AgNPs) are antimicrobial agents that have a wide spectrum of action, including against pathogenic bacteria and spoilage fungi. However, their mechanism of action is not completely clarified. Nowadays, scientific interest on biological synthesis of AgNPs is growing, with emphasis in their extracellular biosynthesis by microbial cells, as it is the most reliable and ecologically correct method for production, yielding no toxic residues. AgNPs may be incorporated to biodegradable and non-biodegradable polymers for the production of food packages with antimicrobial properties, leading to greater safety and longer shelf life. However, it is important to carry out migration tests for new food packages incorporated with AgNPs, based on the effective levels for their inclusion in the packaging materials.

Keywords:
silver nanoparticles; antimicrobial activity; food packaging; polymers

1 Introduction

Microbial contamination of foods is one of the main problems of the food industry, considering the waste of spoiled products and the implications to public health due to foodborne diseases (Carbone et al., 2016Carbone, M., Donia, D. T., Sabbatella, G., & Antiochia, R. (2016). Silver nanoparticles in polymeric matrices for fresh food packaging. Journal of King Saud University - Science, 28(4), 273-279. https://doi.org/10.1016/j.jksus.2016.05.004.
https://doi.org/10.1016/j.jksus.2016.05....
). Therefore, food quality assurance systems applied to production processes are essential to generate products that are free of microbiological hazards. Additionally, post-processing technologies may contribute for the maintenance of food quality during shelf life. Antimicrobial effects may be reached by direct incorporation of biocidal agents in foods or in the space around them (Carbone et al., 2016Carbone, M., Donia, D. T., Sabbatella, G., & Antiochia, R. (2016). Silver nanoparticles in polymeric matrices for fresh food packaging. Journal of King Saud University - Science, 28(4), 273-279. https://doi.org/10.1016/j.jksus.2016.05.004.
https://doi.org/10.1016/j.jksus.2016.05....
). In this context, active packages with antimicrobial properties have been developed for different foods, especially packages with active biocidal substances, which may increase the quality of the product, its shelf life, and prevent spoilage caused by microbial action (Fernández et al., 2010Fernández, A., Picouet, P., & Lloret, E. (2010). Cellulose-silver nanoparticle hybrid materials to control spoilage-related microflora in absorbent pads located in trays of fresh-cut melon. International Journal of Food Microbiology, 142(1–2), 222-228. http://dx.doi.org/10.1016/j.ijfoodmicro.2010.07.001. PMid:20656367.
http://dx.doi.org/10.1016/j.ijfoodmicro....
; Gallocchio et al., 2016Gallocchio, F., Cibin, V., Biancotto, G., Roccato, A., Muzzolon, O., Carmen, L., Simone, B., Manodori, L., Fabrizi, A., Patuzzi, I., & Ricci, A. (2016). Testing nano-silver food packaging to evaluate silver migration and food spoilage bacteria on chicken meat. Food Additives and Contaminants - Part A, 33(6), 1063-1071. http://dx.doi.org/10.1080/19440049.2016.1179794. PMid:27147130.
http://dx.doi.org/10.1080/19440049.2016....
; Mahdi et al., 2012Mahdi, S. S., Vadood, R., & Nourdahr, R. (2012). Study on the antimicrobial effect of nanosilver tray packaging of minced beef at refrigerator temperature. Global Veterinaria, 9(3), 284-289. http://dx.doi.org/10.5829/idosi.gv.2012.9.3.1827.
http://dx.doi.org/10.5829/idosi.gv.2012....
).

The first and most used materials in active packages were organic acids, enzymes, and polymers (biodegradable and non-degradable). Recently, nanoparticles (NPs) of metals or metallic oxides have been introduced with greater advantages compared with organic and inorganic acids, as they are resistant to the most severe processing conditions (Carbone et al., 2016Carbone, M., Donia, D. T., Sabbatella, G., & Antiochia, R. (2016). Silver nanoparticles in polymeric matrices for fresh food packaging. Journal of King Saud University - Science, 28(4), 273-279. https://doi.org/10.1016/j.jksus.2016.05.004.
https://doi.org/10.1016/j.jksus.2016.05....
), such as exposure to high temperatures (Emamifar et al., 2012Emamifar, A., Kadivar, M., Shahedi, M., & Solimanian-Zad, S. (2012). Effect of nanocomposite packaging containing Ag and ZnO on reducing pasteurization temperature of orange juice. Journal of Food Processing and Preservation, 36(2), 104-112. http://dx.doi.org/10.1111/j.1745-4549.2011.00558.x.
http://dx.doi.org/10.1111/j.1745-4549.20...
). Nanotechnology is a promising interdisciplinary science in which new materials are developed in nanoscale, with applications in the fields of medicine, electricity, mechanics, catalysis, photonics, molecular computing, among others (Chen et al., 2016Chen, X., Yan, J. K., & Wu, J. Y. (2016). Characterization and antibacterial activity of silver nanoparticles prepared with a fungal exopolysaccharide in water. Food Hydrocolloids, 53, 69-74. http://dx.doi.org/10.1016/j.foodhyd.2014.12.032.
http://dx.doi.org/10.1016/j.foodhyd.2014...
; Kanmani & Lim, 2013Kanmani, P., & Lim, S. T. (2013). Synthesis and structural characterization of silver nanoparticles using bacterial exopolysaccharide and its antimicrobial activity against food and multidrug resistant pathogens. Process Biochemistry, 48(7), 1099-1106. http://dx.doi.org/10.1016/j.procbio.2013.05.011.
http://dx.doi.org/10.1016/j.procbio.2013...
). The introduction of nanotechnology in the food packaging industry may offer potential solutions for the challenge presented by short shelf life products, improving their quality and keeping them free of microbial adhesion (Emamifar et al., 2012Emamifar, A., Kadivar, M., Shahedi, M., & Solimanian-Zad, S. (2012). Effect of nanocomposite packaging containing Ag and ZnO on reducing pasteurization temperature of orange juice. Journal of Food Processing and Preservation, 36(2), 104-112. http://dx.doi.org/10.1111/j.1745-4549.2011.00558.x.
http://dx.doi.org/10.1111/j.1745-4549.20...
; Qian et al., 2013Qian, Y., Yu, H., He, D., Yang, H., Wang, W., Wan, X., & Wang, L. (2013). Biosynthesis of silver nanoparticles by the endophytic fungus Epicoccum nigrum and their activity against pathogenic fungi. Bioprocess and Biosystems Engineering, 36(11), 1613-1619. http://dx.doi.org/10.1007/s00449-013-0937-z. PMid:23463299.
http://dx.doi.org/10.1007/s00449-013-093...
). Metallic nanoparticles based on magnesium oxide, copper oxide, zinc oxide, cadmium selenite/tellurite, and titanium, silver and gold dioxide, have been studied because of their antimicrobial activity (AbdelRahim et al., 2017AbdelRahim, K., Mahmoud, S. Y., Ali, A. M., Almaary, K. S., Mustafa, A. E. Z. M. A., & Husseiny, S. M. (2017). Extracellular biosynthesis of silver nanoparticles using Rhizopus stolonifer. Saudi Journal of Biological Sciences, 24(1), 208-216. http://dx.doi.org/10.1016/j.sjbs.2016.02.025. PMid:28053592.
http://dx.doi.org/10.1016/j.sjbs.2016.02...
; Almeida et al., 2015Almeida, A. C. S., Franco, A. E. N., Peixoto, F. M., Pessanha, K. L., & Melo, N. R. (2015). Application of nanothecnology in food packaging. Polímeros, 25, 89-97. http://dx.doi.org/10.1590/0104-1428.2069.
http://dx.doi.org/10.1590/0104-1428.2069...
; Echegoyen & Nerín, 2013Echegoyen, Y., & Nerín, C. (2013). Nanoparticle release from nano-silver antimicrobial food containers. Food and Chemical Toxicology, 62, 16-22. http://dx.doi.org/10.1016/j.fct.2013.08.014. PMid:23954768.
http://dx.doi.org/10.1016/j.fct.2013.08....
; Silvestre et al., 2011Silvestre, C., Duraccio, D., & Cimmino, S. (2011). Food packaging based on polymer nanomaterials. Progress in Polymer Science, 36(12), 1766-1782. http://dx.doi.org/10.1016/j.progpolymsci.2011.02.003.
http://dx.doi.org/10.1016/j.progpolymsci...
).

Metallic NPs may be obtained by physical, chemical or biological methods, and antimicrobial activity varies according with the method of synthesis (Durán et al., 2010Durán, N., Marcato, P. D., Conti, R. D., Alves, O. L., Costa, F. T. M., & Brocchi, M. (2010). Potential use of silver nanoparticles on pathogenic bacteria, their toxicity and possible mechanisms of action. Journal of the Brazilian Chemical Society, 21(6), 949-959. http://dx.doi.org/10.1590/S0103-50532010000600002.
http://dx.doi.org/10.1590/S0103-50532010...
). Nowadays, research on biological synthesis of NPs has increased markedly, with emphasis in the microbial production of these compounds, as it is considered the most reliable and ecologically correct method (Wei et al., 2012Wei, X., Luo, M., Li, W., Yang, L., Liang, X., Xu, L., Kong, P., & Liu, H. (2012). Synthesis of silver nanoparticles by solar irradiation of cell-free Bacillus amyloliquefaciens extracts and AgNO3. Bioresource Technology, 103(1), 273-278. http://dx.doi.org/10.1016/j.biortech.2011.09.118. PMid:22019398.
http://dx.doi.org/10.1016/j.biortech.201...
). Among metallic nanoparticles, silver nanoparticles (AgNPs) have been widely studied due to their peculiar properties and their extensive application in the production of biomaterials (AbdelRahim et al., 2017AbdelRahim, K., Mahmoud, S. Y., Ali, A. M., Almaary, K. S., Mustafa, A. E. Z. M. A., & Husseiny, S. M. (2017). Extracellular biosynthesis of silver nanoparticles using Rhizopus stolonifer. Saudi Journal of Biological Sciences, 24(1), 208-216. http://dx.doi.org/10.1016/j.sjbs.2016.02.025. PMid:28053592.
http://dx.doi.org/10.1016/j.sjbs.2016.02...
), and in the food, cosmetics, clothing, and pharmaceutical industries (Chen et al., 2016Chen, X., Yan, J. K., & Wu, J. Y. (2016). Characterization and antibacterial activity of silver nanoparticles prepared with a fungal exopolysaccharide in water. Food Hydrocolloids, 53, 69-74. http://dx.doi.org/10.1016/j.foodhyd.2014.12.032.
http://dx.doi.org/10.1016/j.foodhyd.2014...
; Kanmani & Lim, 2013Kanmani, P., & Lim, S. T. (2013). Synthesis and structural characterization of silver nanoparticles using bacterial exopolysaccharide and its antimicrobial activity against food and multidrug resistant pathogens. Process Biochemistry, 48(7), 1099-1106. http://dx.doi.org/10.1016/j.procbio.2013.05.011.
http://dx.doi.org/10.1016/j.procbio.2013...
). Additionally, when compared with other metals, silver presents the lowest toxicity for animal cells (Berni et al., 2008Berni, E. A. No., Ribeiro, C., & Zucolotto, V. (2008). Síntese de nanopartículas de prata para aplicação na sanitização de embalagens (Comunicado Técnico, No. 99, 4 p.). São Carlos: EMBRAPA. Retrieved from http://agris.fao.org/agris-search/search.do?recordID=BR2008131734
http://agris.fao.org/agris-search/search...
). Therefore, the most recent studies on antimicrobial nanocompounds in food packages are based on AgNPs (Emamifar et al., 2012Emamifar, A., Kadivar, M., Shahedi, M., & Solimanian-Zad, S. (2012). Effect of nanocomposite packaging containing Ag and ZnO on reducing pasteurization temperature of orange juice. Journal of Food Processing and Preservation, 36(2), 104-112. http://dx.doi.org/10.1111/j.1745-4549.2011.00558.x.
http://dx.doi.org/10.1111/j.1745-4549.20...
; Gallocchio et al., 2016Gallocchio, F., Cibin, V., Biancotto, G., Roccato, A., Muzzolon, O., Carmen, L., Simone, B., Manodori, L., Fabrizi, A., Patuzzi, I., & Ricci, A. (2016). Testing nano-silver food packaging to evaluate silver migration and food spoilage bacteria on chicken meat. Food Additives and Contaminants - Part A, 33(6), 1063-1071. http://dx.doi.org/10.1080/19440049.2016.1179794. PMid:27147130.
http://dx.doi.org/10.1080/19440049.2016....
; Martinez-Abad et al., 2012Martinez-Abad, A., Lagaron, J. M., & Ocio, M. J. (2012). Development and characterization of silver-based antimicrobial ethylene-vinyl alcohol copolymer (EVOH) films for food-packaging applications. Journal of Agricultural and Food Chemistry, 60(21), 5350-5359. http://dx.doi.org/10.1021/jf300334z. PMid:22577863.
http://dx.doi.org/10.1021/jf300334z...
). Although AgNPs are listed by the U.S. Food and Drug Administration as generally recognized as safe (GRAS) materials (Emamifar et al., 2012Emamifar, A., Kadivar, M., Shahedi, M., & Solimanian-Zad, S. (2012). Effect of nanocomposite packaging containing Ag and ZnO on reducing pasteurization temperature of orange juice. Journal of Food Processing and Preservation, 36(2), 104-112. http://dx.doi.org/10.1111/j.1745-4549.2011.00558.x.
http://dx.doi.org/10.1111/j.1745-4549.20...
), there is a concern about the potential health effects associated with high intake levels caused by migration of these particles from the packaging to the foods (Claro & Magalhães, 2017Claro, F. C., & Magalhães, W. L. E. (2017). Síntese de nanopartículas de prata em filmes de nanocelulose. Embrapa, 149, 149-152.; Echegoyen & Nerín, 2013Echegoyen, Y., & Nerín, C. (2013). Nanoparticle release from nano-silver antimicrobial food containers. Food and Chemical Toxicology, 62, 16-22. http://dx.doi.org/10.1016/j.fct.2013.08.014. PMid:23954768.
http://dx.doi.org/10.1016/j.fct.2013.08....
; Gallocchio et al., 2016Gallocchio, F., Cibin, V., Biancotto, G., Roccato, A., Muzzolon, O., Carmen, L., Simone, B., Manodori, L., Fabrizi, A., Patuzzi, I., & Ricci, A. (2016). Testing nano-silver food packaging to evaluate silver migration and food spoilage bacteria on chicken meat. Food Additives and Contaminants - Part A, 33(6), 1063-1071. http://dx.doi.org/10.1080/19440049.2016.1179794. PMid:27147130.
http://dx.doi.org/10.1080/19440049.2016....
). Thus, the objective of this paper is to review the available data published in the past 5 years on the mechanisms of action, microbial synthesis, toxicological aspects and antimicrobial properties of AgNPs, as well as their potential applications in the food industry.

2 Mechanisms of action of silver nanoparticles

According to Kanmani & Lim (2013)Kanmani, P., & Lim, S. T. (2013). Synthesis and structural characterization of silver nanoparticles using bacterial exopolysaccharide and its antimicrobial activity against food and multidrug resistant pathogens. Process Biochemistry, 48(7), 1099-1106. http://dx.doi.org/10.1016/j.procbio.2013.05.011.
http://dx.doi.org/10.1016/j.procbio.2013...
, AgNPs have a wide spectrum of antimicrobial activity, including Gram-positive and negative bacteria, fungi, and viruses. It is known that AgNPs are toxic to a large variety of microorganisms (Morones et al., 2005Morones, J. R., Elechiguerra, J. L., Camacho, A., Holt, K., Kouri, J. B., Ramírez, J. T., & Yacaman, M. J. (2005). The bactericidal effect of silver nanoparticles. Nanotechnology, 16(10), 2346-2353. http://dx.doi.org/10.1088/0957-4484/16/10/059. PMid:20818017.
http://dx.doi.org/10.1088/0957-4484/16/1...
) including Escherichia coli, Enterococcus faecalis, Staphylococcus aureus, S. epidermidis, Vibrio cholerae, Pseudomonas aeruginosa, Shigella flexneri, Bacillus anthracis, B. subtilis, B. cereus, Proteus mirabilis, Salmonella enterica typhimurium, Micrococcus luteus, Listeria monocytogenes, and Klebsiella pneumoniae (Almeida et al., 2015Almeida, A. C. S., Franco, A. E. N., Peixoto, F. M., Pessanha, K. L., & Melo, N. R. (2015). Application of nanothecnology in food packaging. Polímeros, 25, 89-97. http://dx.doi.org/10.1590/0104-1428.2069.
http://dx.doi.org/10.1590/0104-1428.2069...
). The bactericidal effect of AgNPs was first quantified by Von Naegelis, using silver ions against algae (Berni et al., 2008Berni, E. A. No., Ribeiro, C., & Zucolotto, V. (2008). Síntese de nanopartículas de prata para aplicação na sanitização de embalagens (Comunicado Técnico, No. 99, 4 p.). São Carlos: EMBRAPA. Retrieved from http://agris.fao.org/agris-search/search.do?recordID=BR2008131734
http://agris.fao.org/agris-search/search...
). However, it is not clear if AgNPs present a specific mechanism of action (Morones et al., 2005Morones, J. R., Elechiguerra, J. L., Camacho, A., Holt, K., Kouri, J. B., Ramírez, J. T., & Yacaman, M. J. (2005). The bactericidal effect of silver nanoparticles. Nanotechnology, 16(10), 2346-2353. http://dx.doi.org/10.1088/0957-4484/16/10/059. PMid:20818017.
http://dx.doi.org/10.1088/0957-4484/16/1...
), or if their antimicrobial activity is only associated with the release of Ag+ ions, their bioactive form (Almeida et al., 2015Almeida, A. C. S., Franco, A. E. N., Peixoto, F. M., Pessanha, K. L., & Melo, N. R. (2015). Application of nanothecnology in food packaging. Polímeros, 25, 89-97. http://dx.doi.org/10.1590/0104-1428.2069.
http://dx.doi.org/10.1590/0104-1428.2069...
; Sobye et al., 2015Sobye, A., Kolding, A., Jorgensen, J. K., Lund, M. K., & Mikkelsen, M. O. (2015). Bactericidal effect of silver nanoparticles: determination of size and shape of triangular silver nanoprisms and spherical silver nanoparticles and their bactericidal effect against Escherichia coli and Bacillus subtilis (pp. 9-76). Aalborg: School of Engineering and Science Nanotechnology.). On the other hand, Sobye et al. (2015)Sobye, A., Kolding, A., Jorgensen, J. K., Lund, M. K., & Mikkelsen, M. O. (2015). Bactericidal effect of silver nanoparticles: determination of size and shape of triangular silver nanoprisms and spherical silver nanoparticles and their bactericidal effect against Escherichia coli and Bacillus subtilis (pp. 9-76). Aalborg: School of Engineering and Science Nanotechnology. proposed different mechanisms by which AgNPs inhibit or reduce the growth and metabolism of bacterial cells, leading to accelerated lysis.

The antimicrobial effect of silver, silver ions, and silver nanoparticles has been studied, aiming to evaluate the mechanism of action against a wide range of bacteria (Pal et al., 2007Pal, S., Tak, Y. K., & Song, J. M. (2007). Does the antibacterial activity of silver nanoparticles depend on the shape of the nanoparticle? A study of the gram-negative bacterium Escherichia coli. The Journal of Biological Chemistry, 73(6), 1712-1720. http://dx.doi.org/10.1128/AEM.02218-06. PMid:17261510.
http://dx.doi.org/10.1128/AEM.02218-06...
). Morones et al. (2005)Morones, J. R., Elechiguerra, J. L., Camacho, A., Holt, K., Kouri, J. B., Ramírez, J. T., & Yacaman, M. J. (2005). The bactericidal effect of silver nanoparticles. Nanotechnology, 16(10), 2346-2353. http://dx.doi.org/10.1088/0957-4484/16/10/059. PMid:20818017.
http://dx.doi.org/10.1088/0957-4484/16/1...
evaluated the bactericidal effect of AgNPs, and identified three main mechanisms of action of the nanoparticles: (1) AgNPs in the range of 1 to 10 nm bound to the surface of the cell membrane and drastically interfere with its functions, such as permeability and respiration; (2) AgNPs are able to penetrate the bacterial cells and damage them, possibly by interacting with compounds containing sulfur and phosphorus, such as DNA; (3) AgNPs release silver ions, which are potentially very reactive and may react with the negatively charged cell membrane, providing an additional contribution to the bactericidal effect of silver nanoparticles.

A study carried out by Sobye et al. (2015)Sobye, A., Kolding, A., Jorgensen, J. K., Lund, M. K., & Mikkelsen, M. O. (2015). Bactericidal effect of silver nanoparticles: determination of size and shape of triangular silver nanoprisms and spherical silver nanoparticles and their bactericidal effect against Escherichia coli and Bacillus subtilis (pp. 9-76). Aalborg: School of Engineering and Science Nanotechnology. demonstrated that, under anaerobiosis conditions, AgNPs do not show bactericidal effect, even at high concentrations. The authors supported the hypothesis that silver ions are not released in the absence of oxygen. Pal et al. (2007)Pal, S., Tak, Y. K., & Song, J. M. (2007). Does the antibacterial activity of silver nanoparticles depend on the shape of the nanoparticle? A study of the gram-negative bacterium Escherichia coli. The Journal of Biological Chemistry, 73(6), 1712-1720. http://dx.doi.org/10.1128/AEM.02218-06. PMid:17261510.
http://dx.doi.org/10.1128/AEM.02218-06...
observed different inhibition effects of AgNPs on E. coli, which activities varied according to the size and shape of particles. However, little is known about the change in AgNPs biological activity caused by the shape of the particle. According to Sobye et al. (2015)Sobye, A., Kolding, A., Jorgensen, J. K., Lund, M. K., & Mikkelsen, M. O. (2015). Bactericidal effect of silver nanoparticles: determination of size and shape of triangular silver nanoprisms and spherical silver nanoparticles and their bactericidal effect against Escherichia coli and Bacillus subtilis (pp. 9-76). Aalborg: School of Engineering and Science Nanotechnology., AgNPs may have different shapes, but the most interesting particles in terms of antimicrobial effect are spherical and triangular, with greater antimicrobial effect of triangular particles than spherical possibly because of their larger contact surface.

3 Biosynthesis of silver nanoparticles and antimicrobial activity

The biological synthesis of AgNPs (involving bacteria, fungi, and biomolecules) has been widely researched, since it is considered as a reliable and ecologically correct method (Durán et al., 2010Durán, N., Marcato, P. D., Conti, R. D., Alves, O. L., Costa, F. T. M., & Brocchi, M. (2010). Potential use of silver nanoparticles on pathogenic bacteria, their toxicity and possible mechanisms of action. Journal of the Brazilian Chemical Society, 21(6), 949-959. http://dx.doi.org/10.1590/S0103-50532010000600002.
http://dx.doi.org/10.1590/S0103-50532010...
; Wei et al., 2012Wei, X., Luo, M., Li, W., Yang, L., Liang, X., Xu, L., Kong, P., & Liu, H. (2012). Synthesis of silver nanoparticles by solar irradiation of cell-free Bacillus amyloliquefaciens extracts and AgNO3. Bioresource Technology, 103(1), 273-278. http://dx.doi.org/10.1016/j.biortech.2011.09.118. PMid:22019398.
http://dx.doi.org/10.1016/j.biortech.201...
). Additionally, biological synthesis does not yield any toxic residues (Husseiny et al., 2015Husseiny, S. M., Salah, T. A., & Anter, H. A. (2015). Biosynthesis of size controlled silver nanoparticles by Fusarium oxysporum, their antibacterial and antitumor activities. Beni-Suef University Journal of Basic and Applied Sciences, 4(3), 225-231. http://dx.doi.org/10.1016/j.bjbas.2015.07.004.
http://dx.doi.org/10.1016/j.bjbas.2015.0...
). Durán et al. (2010)Durán, N., Marcato, P. D., Conti, R. D., Alves, O. L., Costa, F. T. M., & Brocchi, M. (2010). Potential use of silver nanoparticles on pathogenic bacteria, their toxicity and possible mechanisms of action. Journal of the Brazilian Chemical Society, 21(6), 949-959. http://dx.doi.org/10.1590/S0103-50532010000600002.
http://dx.doi.org/10.1590/S0103-50532010...
reported that plant extracts may also be used in metallic nanoparticle production. Microbial synthesis of metallic NPs may be intracellular (Das et al., 2014Das, L. V., Thomas, R., Varghese, R. T., Soniya, E. V., Mathew, J., & Radhakrishnan, E. K. (2014). Extracellular synthesis of silver nanoparticles by the Bacillus strain CS 11 isolated from industrialized area. 3 Biotech, 4(2), 121-126. https://doi.org/10.1007/s13205-013-0130-8.
https://doi.org/10.1007/s13205-013-0130-...
) or extracellular (AbdelRahim et al., 2017AbdelRahim, K., Mahmoud, S. Y., Ali, A. M., Almaary, K. S., Mustafa, A. E. Z. M. A., & Husseiny, S. M. (2017). Extracellular biosynthesis of silver nanoparticles using Rhizopus stolonifer. Saudi Journal of Biological Sciences, 24(1), 208-216. http://dx.doi.org/10.1016/j.sjbs.2016.02.025. PMid:28053592.
http://dx.doi.org/10.1016/j.sjbs.2016.02...
; Das et al., 2014Das, L. V., Thomas, R., Varghese, R. T., Soniya, E. V., Mathew, J., & Radhakrishnan, E. K. (2014). Extracellular synthesis of silver nanoparticles by the Bacillus strain CS 11 isolated from industrialized area. 3 Biotech, 4(2), 121-126. https://doi.org/10.1007/s13205-013-0130-8.
https://doi.org/10.1007/s13205-013-0130-...
; Gopinath & Velusamy, 2013Gopinath, V., & Velusamy, P. (2013). Extracellular biosynthesis of silver nanoparticles using Bacillus sp. GP-23 and evaluation of their antifungal activity towards Fusarium oxysporum. Spectrochimica Acta. Part A: Molecular and Biomolecular Spectroscopy, 106, 170-174. http://dx.doi.org/10.1016/j.saa.2012.12.087. PMid:23376272.
http://dx.doi.org/10.1016/j.saa.2012.12....
; Prakasham et al., 2014Prakasham, R. S., Kumar, B. S., Kumar, Y. S., & Kumar, K. P. (2014). Production and Characterization of Protein Encapsulated Silver Nanoparticles by Marine Isolate Streptomyces parvulus SSNP11. Indian Journal of Microbiology, 54(3), 329-336. http://dx.doi.org/10.1007/s12088-014-0452-1. PMid:24891741.
http://dx.doi.org/10.1007/s12088-014-045...
), yielding NPs of different sizes, shapes and antimicrobial efficacy (Husseiny et al., 2015Husseiny, S. M., Salah, T. A., & Anter, H. A. (2015). Biosynthesis of size controlled silver nanoparticles by Fusarium oxysporum, their antibacterial and antitumor activities. Beni-Suef University Journal of Basic and Applied Sciences, 4(3), 225-231. http://dx.doi.org/10.1016/j.bjbas.2015.07.004.
http://dx.doi.org/10.1016/j.bjbas.2015.0...
).

Several studies have focused on extracellular synthesis of metallic nanoparticles because of its relative simplicity and lower cost compared with intracellular synthesis (Das et al., 2014Das, L. V., Thomas, R., Varghese, R. T., Soniya, E. V., Mathew, J., & Radhakrishnan, E. K. (2014). Extracellular synthesis of silver nanoparticles by the Bacillus strain CS 11 isolated from industrialized area. 3 Biotech, 4(2), 121-126. https://doi.org/10.1007/s13205-013-0130-8.
https://doi.org/10.1007/s13205-013-0130-...
). The mechanisms involved in the extracellular synthesis of nanoparticles using microorganisms have not been completely clarified. However, Das et al. (2014)Das, L. V., Thomas, R., Varghese, R. T., Soniya, E. V., Mathew, J., & Radhakrishnan, E. K. (2014). Extracellular synthesis of silver nanoparticles by the Bacillus strain CS 11 isolated from industrialized area. 3 Biotech, 4(2), 121-126. https://doi.org/10.1007/s13205-013-0130-8.
https://doi.org/10.1007/s13205-013-0130-...
postulated that the synthesis is related to the presence of nitrate reductase enzymes released by the microorganisms, which are responsible for the bio-reduction of metallic ions and metallic nanoparticles. This phenomenon may be evidenced by the color change using spectrophotometry (Elbeshehy et al., 2015Elbeshehy, E. K. F., Elazzazy, A. M., & Aggelis, G. (2015). Silver nanoparticles synthesis mediated by new isolates of Bacillus spp., nanoparticle characterization and their activity against Bean Yellow Mosaic Virus and human pathogens. Frontiers in Microbiology, 6, 1-13. http://dx.doi.org/10.3389/fmicb.2015.00453. PMid:26029190.
http://dx.doi.org/10.3389/fmicb.2015.004...
). Taking into account the accessibility and easy genetic modification, bacteria are the most promising candidates to AgNPs synthesis (Wei et al., 2012Wei, X., Luo, M., Li, W., Yang, L., Liang, X., Xu, L., Kong, P., & Liu, H. (2012). Synthesis of silver nanoparticles by solar irradiation of cell-free Bacillus amyloliquefaciens extracts and AgNO3. Bioresource Technology, 103(1), 273-278. http://dx.doi.org/10.1016/j.biortech.2011.09.118. PMid:22019398.
http://dx.doi.org/10.1016/j.biortech.201...
; Elbeshehy et al., 2015Elbeshehy, E. K. F., Elazzazy, A. M., & Aggelis, G. (2015). Silver nanoparticles synthesis mediated by new isolates of Bacillus spp., nanoparticle characterization and their activity against Bean Yellow Mosaic Virus and human pathogens. Frontiers in Microbiology, 6, 1-13. http://dx.doi.org/10.3389/fmicb.2015.00453. PMid:26029190.
http://dx.doi.org/10.3389/fmicb.2015.004...
; Kanmani & Lim, 2013Kanmani, P., & Lim, S. T. (2013). Synthesis and structural characterization of silver nanoparticles using bacterial exopolysaccharide and its antimicrobial activity against food and multidrug resistant pathogens. Process Biochemistry, 48(7), 1099-1106. http://dx.doi.org/10.1016/j.procbio.2013.05.011.
http://dx.doi.org/10.1016/j.procbio.2013...
; Singh et al., 2013bSingh, R., Wagh, P., Wadhwani, S., Gaidhani, S., Kumbhar, A., Bellare, J., & Chopade, B. A. (2013b). Synthesis, optimization, and characterization of silver nanoparticles from Acinetobacter calcoaceticus and their enhanced antibacterial activity when combined with antibiotics. International Journal of Nanomedicine, 8, 4277-4290. http://dx.doi.org/10.2147/IJN.S48913. PMid:24235826.
http://dx.doi.org/10.2147/IJN.S48913...
).

3.1 Biosynthesis of AgNPs by bacterial species

The main genera of bacteria that exhibit effective synthesis of AgNPs include Bacillus spp. (Das et al., 2014Das, L. V., Thomas, R., Varghese, R. T., Soniya, E. V., Mathew, J., & Radhakrishnan, E. K. (2014). Extracellular synthesis of silver nanoparticles by the Bacillus strain CS 11 isolated from industrialized area. 3 Biotech, 4(2), 121-126. https://doi.org/10.1007/s13205-013-0130-8.
https://doi.org/10.1007/s13205-013-0130-...
; Elbeshehy et al., 2015Elbeshehy, E. K. F., Elazzazy, A. M., & Aggelis, G. (2015). Silver nanoparticles synthesis mediated by new isolates of Bacillus spp., nanoparticle characterization and their activity against Bean Yellow Mosaic Virus and human pathogens. Frontiers in Microbiology, 6, 1-13. http://dx.doi.org/10.3389/fmicb.2015.00453. PMid:26029190.
http://dx.doi.org/10.3389/fmicb.2015.004...
; Gopinath & Velusamy, 2013Gopinath, V., & Velusamy, P. (2013). Extracellular biosynthesis of silver nanoparticles using Bacillus sp. GP-23 and evaluation of their antifungal activity towards Fusarium oxysporum. Spectrochimica Acta. Part A: Molecular and Biomolecular Spectroscopy, 106, 170-174. http://dx.doi.org/10.1016/j.saa.2012.12.087. PMid:23376272.
http://dx.doi.org/10.1016/j.saa.2012.12....
; Wei et al., 2012Wei, X., Luo, M., Li, W., Yang, L., Liang, X., Xu, L., Kong, P., & Liu, H. (2012). Synthesis of silver nanoparticles by solar irradiation of cell-free Bacillus amyloliquefaciens extracts and AgNO3. Bioresource Technology, 103(1), 273-278. http://dx.doi.org/10.1016/j.biortech.2011.09.118. PMid:22019398.
http://dx.doi.org/10.1016/j.biortech.201...
), Streptomyces spp. (Manikprabhu & Lingappa, 2013Manikprabhu, D., & Lingappa, K. (2013). Antibacterial activity of silver nanoparticles against methicillin-resistant staphylococcus aureus synthesized using model streptomyces sp. pigment by photo-irradiation method. Journal of Pharmacy Research, 6(2), 255-260. http://dx.doi.org/10.1016/j.jopr.2013.01.022.
http://dx.doi.org/10.1016/j.jopr.2013.01...
; Mohanta & Behera, 2014Mohanta, Y. K., & Behera, S. K. (2014). Biosynthesis, characterization and antimicrobial activity of silver nanoparticles by Streptomyces sp. SS2. Bioprocess and Biosystems Engineering, 37(11), 2263-2269. http://dx.doi.org/10.1007/s00449-014-1205-6. PMid:24842223.
http://dx.doi.org/10.1007/s00449-014-120...
; Prakasham et al., 2014Prakasham, R. S., Kumar, B. S., Kumar, Y. S., & Kumar, K. P. (2014). Production and Characterization of Protein Encapsulated Silver Nanoparticles by Marine Isolate Streptomyces parvulus SSNP11. Indian Journal of Microbiology, 54(3), 329-336. http://dx.doi.org/10.1007/s12088-014-0452-1. PMid:24891741.
http://dx.doi.org/10.1007/s12088-014-045...
) Acinetobacter spp. (Singh et al., 2013bSingh, R., Wagh, P., Wadhwani, S., Gaidhani, S., Kumbhar, A., Bellare, J., & Chopade, B. A. (2013b). Synthesis, optimization, and characterization of silver nanoparticles from Acinetobacter calcoaceticus and their enhanced antibacterial activity when combined with antibiotics. International Journal of Nanomedicine, 8, 4277-4290. http://dx.doi.org/10.2147/IJN.S48913. PMid:24235826.
http://dx.doi.org/10.2147/IJN.S48913...
), and Pseudomonas spp. (Gopinath et al., 2017Gopinath, V., Priyadarshini, S., Loke, M. F., Arunkumar, J., Marsili, E., MubarakAli, D., Velusamy, P., & Vadivelu, J. (2017). Biogenic synthesis, characterization of antibacterial silver nanoparticles and its cell cytotoxicity. Arabian Journal of Chemistry, 10(8), 1107-1117. http://dx.doi.org/10.1016/j.arabjc.2015.11.011.
http://dx.doi.org/10.1016/j.arabjc.2015....
; Peiris et al., 2017Peiris, M. K., Gunasekara, C. P., Jayaweera, P. M., Arachchi, N. D. H., & Fernando, N. (2017). Biosynthesized silver nanoparticles: Are they effective antimicrobials? Memorias do Instituto Oswaldo Cruz, 112(8), 537-543. http://dx.doi.org/10.1590/0074-02760170023. PMid:28767978.
http://dx.doi.org/10.1590/0074-027601700...
). Bacterial strains used for AgNPs synthesis were mainly isolated in samples of soil sediment contaminated by heavy metals (Das et al., 2014Das, L. V., Thomas, R., Varghese, R. T., Soniya, E. V., Mathew, J., & Radhakrishnan, E. K. (2014). Extracellular synthesis of silver nanoparticles by the Bacillus strain CS 11 isolated from industrialized area. 3 Biotech, 4(2), 121-126. https://doi.org/10.1007/s13205-013-0130-8.
https://doi.org/10.1007/s13205-013-0130-...
; Elbeshehy et al., 2015Elbeshehy, E. K. F., Elazzazy, A. M., & Aggelis, G. (2015). Silver nanoparticles synthesis mediated by new isolates of Bacillus spp., nanoparticle characterization and their activity against Bean Yellow Mosaic Virus and human pathogens. Frontiers in Microbiology, 6, 1-13. http://dx.doi.org/10.3389/fmicb.2015.00453. PMid:26029190.
http://dx.doi.org/10.3389/fmicb.2015.004...
; Mohanta & Behera, 2014Mohanta, Y. K., & Behera, S. K. (2014). Biosynthesis, characterization and antimicrobial activity of silver nanoparticles by Streptomyces sp. SS2. Bioprocess and Biosystems Engineering, 37(11), 2263-2269. http://dx.doi.org/10.1007/s00449-014-1205-6. PMid:24842223.
http://dx.doi.org/10.1007/s00449-014-120...
), and marine sediments (Manivasagan et al., 2013Manivasagan, P., Venkatesan, J., Senthilkumar, K., Sivakumar, K., & Kim, S. K. (2013). Biosynthesis, antimicrobial and cytotoxic effect of silver nanoparticles using a novel Nocardiopsis sp. MBRC-1. BioMed Research International, 2013, 287638. http://dx.doi.org/10.1155/2013/287638. PMid:23936787.
http://dx.doi.org/10.1155/2013/287638...
; Prakasham et al., 2014Prakasham, R. S., Kumar, B. S., Kumar, Y. S., & Kumar, K. P. (2014). Production and Characterization of Protein Encapsulated Silver Nanoparticles by Marine Isolate Streptomyces parvulus SSNP11. Indian Journal of Microbiology, 54(3), 329-336. http://dx.doi.org/10.1007/s12088-014-0452-1. PMid:24891741.
http://dx.doi.org/10.1007/s12088-014-045...
). Table 1 presents the outcomes from recent studies on the bacterial biosynthesis of AgNPs, size and shape of AgNPs produced, as well as the microbial species tested for their minimum inhibitory concentration.

Table 1
Antimicrobial effect of silver nanoparticles synthesized by bacterial strains.

Kanmani & Lim (2013)Kanmani, P., & Lim, S. T. (2013). Synthesis and structural characterization of silver nanoparticles using bacterial exopolysaccharide and its antimicrobial activity against food and multidrug resistant pathogens. Process Biochemistry, 48(7), 1099-1106. http://dx.doi.org/10.1016/j.procbio.2013.05.011.
http://dx.doi.org/10.1016/j.procbio.2013...
synthesized bacterial AgNPs by direct reduction of silver nitrite by the exopolysaccharide, and demonstrated their antibacterial and antifungal activity with different susceptibilities of bacterial species in the following order: P. aeruginosa > E.coli and K. pneumonia > L. monocytogenes. The inhibition zone observed for bacterial species was achieved at 2 mg/mL AgNPs, while fungal zone of inhibition ranged between 0.2 to 2 mg/mL, with greater susceptibility of Aspergillus spp. than Penicillium spp. AgNPs derived from Acinetobacter spp. biosynthesis using an extract of free cells of the microorganism had antimicrobial activity against Gram-positive and negative bacteria (Singh et al., 2013bSingh, R., Wagh, P., Wadhwani, S., Gaidhani, S., Kumbhar, A., Bellare, J., & Chopade, B. A. (2013b). Synthesis, optimization, and characterization of silver nanoparticles from Acinetobacter calcoaceticus and their enhanced antibacterial activity when combined with antibiotics. International Journal of Nanomedicine, 8, 4277-4290. http://dx.doi.org/10.2147/IJN.S48913. PMid:24235826.
http://dx.doi.org/10.2147/IJN.S48913...
). Wei et al. (2012)Wei, X., Luo, M., Li, W., Yang, L., Liang, X., Xu, L., Kong, P., & Liu, H. (2012). Synthesis of silver nanoparticles by solar irradiation of cell-free Bacillus amyloliquefaciens extracts and AgNO3. Bioresource Technology, 103(1), 273-278. http://dx.doi.org/10.1016/j.biortech.2011.09.118. PMid:22019398.
http://dx.doi.org/10.1016/j.biortech.201...
produced bacterial AgNPs from Bacillus amyloliquefaciens by solar irradiation, and these nanoparticles presented antimicrobial effects, with B. subtilis being more susceptible (0.009 mg/mL) than E. coli. Gopinath & Velusamy (2013)Gopinath, V., & Velusamy, P. (2013). Extracellular biosynthesis of silver nanoparticles using Bacillus sp. GP-23 and evaluation of their antifungal activity towards Fusarium oxysporum. Spectrochimica Acta. Part A: Molecular and Biomolecular Spectroscopy, 106, 170-174. http://dx.doi.org/10.1016/j.saa.2012.12.087. PMid:23376272.
http://dx.doi.org/10.1016/j.saa.2012.12....
synthetized AgNPs using Bacillus spp. GP-23, and observed effective antifungal activity against Fusarium oxysporum at 0.008 mg/mL.

Bacillus spp. strains isolated from soil samples contaminated with heavy metals were highly efficient for intracellular and extracellular synthesis of AgNPs (spherical, 42-92 nm) (Das et al., 2014Das, L. V., Thomas, R., Varghese, R. T., Soniya, E. V., Mathew, J., & Radhakrishnan, E. K. (2014). Extracellular synthesis of silver nanoparticles by the Bacillus strain CS 11 isolated from industrialized area. 3 Biotech, 4(2), 121-126. https://doi.org/10.1007/s13205-013-0130-8.
https://doi.org/10.1007/s13205-013-0130-...
). Elbeshehy et al. (2015)Elbeshehy, E. K. F., Elazzazy, A. M., & Aggelis, G. (2015). Silver nanoparticles synthesis mediated by new isolates of Bacillus spp., nanoparticle characterization and their activity against Bean Yellow Mosaic Virus and human pathogens. Frontiers in Microbiology, 6, 1-13. http://dx.doi.org/10.3389/fmicb.2015.00453. PMid:26029190.
http://dx.doi.org/10.3389/fmicb.2015.004...
identified new strains of Bacillus (B. pumilus, B. persicus, and B. licheniformis) that were efficient in the AgNPs extracellular synthesis. AgNPs produced by B. licheniformis presented strong antibacterial effect against Gram-negative bacteria (E. coli, K. pneumoniae, S. sonnei, P. aeruginosa), followed by Gram-positive ones (S. epidermidis, S. aureus - methicillin- resistant strain - and S. bovis). Significant antifungal effects were also observed against A. flavus and C. albicans ATCC 1021.

AgNPs produced by Streptomyces albidoflavus were evaluated by Prakasham et al. (2012)Prakasham, R. S., Buddana, S. K., Yannam, S. K., & Guntuku, G. S. (2012). Characterization of silver nanoparticles synthesized by using marine isolate Streptomyces albidoflavus. Journal of Microbiology and Biotechnology, 22(5), 614-621. http://dx.doi.org/10.4014/jmb.1107.07013. PMid:22561854.
http://dx.doi.org/10.4014/jmb.1107.07013...
by determining the inhibition zones against bacterial species. The author observed high antibacterial effects against K. pneumonia (36 mm), followed by M. luteus (28 mm), and B. subtilis (24 mm), and lower effect against E. coli (22 mm). On the other hand, Mohanta & Behera (2014)Mohanta, Y. K., & Behera, S. K. (2014). Biosynthesis, characterization and antimicrobial activity of silver nanoparticles by Streptomyces sp. SS2. Bioprocess and Biosystems Engineering, 37(11), 2263-2269. http://dx.doi.org/10.1007/s00449-014-1205-6. PMid:24842223.
http://dx.doi.org/10.1007/s00449-014-120...
developed the extracellular biosynthesis of AgNPs using Streptomyces sp. SS2 isolated from soil sediment samples, and demonstrated potential antimicrobial activity of AgNPs against E. coli, B. subtilis, S. epidermis, V. cholerae, and S. aureus. The largest and the smallest zone of inhibition were observed against V. cholerae and B. subtilis, respectively.

Prakasham et al. (2014)Prakasham, R. S., Kumar, B. S., Kumar, Y. S., & Kumar, K. P. (2014). Production and Characterization of Protein Encapsulated Silver Nanoparticles by Marine Isolate Streptomyces parvulus SSNP11. Indian Journal of Microbiology, 54(3), 329-336. http://dx.doi.org/10.1007/s12088-014-0452-1. PMid:24891741.
http://dx.doi.org/10.1007/s12088-014-045...
characterized AgNPs obtained from extracellular synthesis by strains of actinomycetes (Streptomyces parvulus SSNP11) isolated from samples of marine sediment. The AgNPs had effective antibacterial activity against Gram-negative and positive bacteria, including P. putida, K. pneumoniae, B. subtilis, and S. typhi. Manivasagan et al. (2013)Manivasagan, P., Venkatesan, J., Senthilkumar, K., Sivakumar, K., & Kim, S. K. (2013). Biosynthesis, antimicrobial and cytotoxic effect of silver nanoparticles using a novel Nocardiopsis sp. MBRC-1. BioMed Research International, 2013, 287638. http://dx.doi.org/10.1155/2013/287638. PMid:23936787.
http://dx.doi.org/10.1155/2013/287638...
studied the biosynthesis of AgNPs (spherical, average size 45 ± 0.15 nm) by Nocardiopsis sp. MBRC-1 isolated from samples of marine sediment. The resulting particles had significant antimicrobial effects against several microorganisms including bacteria (E. coli, B. subtilis, E. hirae, P. aeruginosa, S. flexneri, and S. aureus) and fungi (A. niger, A. brasiliensis, A. fumigates, and C. albicans).

Peiris et al. (2017)Peiris, M. K., Gunasekara, C. P., Jayaweera, P. M., Arachchi, N. D. H., & Fernando, N. (2017). Biosynthesized silver nanoparticles: Are they effective antimicrobials? Memorias do Instituto Oswaldo Cruz, 112(8), 537-543. http://dx.doi.org/10.1590/0074-02760170023. PMid:28767978.
http://dx.doi.org/10.1590/0074-027601700...
produced AgNPs using Pseudomonas aeruginosa ATCC 27853, and demonstrated that the nanoparticles were effective against Gram-negative and positive bacteria (E. coli ATCC 25922, S. aureus ATCC 25923, P. aeruginosa ATCC 27853, S. typhimurium, Acinetobacter) as well as fungi (C. albicans). Gopinath et al. (2017)Gopinath, V., Priyadarshini, S., Loke, M. F., Arunkumar, J., Marsili, E., MubarakAli, D., Velusamy, P., & Vadivelu, J. (2017). Biogenic synthesis, characterization of antibacterial silver nanoparticles and its cell cytotoxicity. Arabian Journal of Chemistry, 10(8), 1107-1117. http://dx.doi.org/10.1016/j.arabjc.2015.11.011.
http://dx.doi.org/10.1016/j.arabjc.2015....
obtained AgNPs by biogenic extracellular synthesis using the bacterium P. putida MVP2. The AgNPs were efficient against Gram-positive and negative bacteria, including S. aureus, E. coli, B. cereus, P. aeruginosa, and H. pylori. AgNPs produced by biosynthesis using the acidophilic actinobacterium Streptacidiphilus durhamensis HGG16n had high antimicrobial effect against P. aeruginosa, S. aureus, and P. mirabilis, followed by E. coli, K. pneumoniae, and B. subtilis (Buszewski et al., 2018Buszewski, B., Railean-Plugaru, V., Pomastowski, P., Rafińska, K., Szultka-Mlynska, M., Golinska, P., Wypij, M., Laskowski, D., & Dahm, H. (2018). Antimicrobial activity of biosilver nanoparticles produced by a novel Streptacidiphilus durhamensis strain. Journal of Microbiology, Immunology, and Infection, 51(1), 45-54. http://dx.doi.org/10.1016/j.jmii.2016.03.002. PMid:27103501.
http://dx.doi.org/10.1016/j.jmii.2016.03...
).

In summary, low levels of AgNPs synthesized by bacterial species presented strong antimicrobial activity effect against S. aureus, P. aeruginosa, B. subtilis, E. coli, although higher concentrations were required to become effective against other important pathogenic microorganisms including L. monocytogenes and S. typhimurium.

3.2 Biosynthesis of AgNPs by fungi species

There are several reports demonstrating the biosynthesis of AgNPs by fungi species, mostly of them related to the use of endophytic fungi (those isolated from parts of plants) (Devi & Joshi, 2015Devi, L. S., & Joshi, S. R. (2015). Ultrastructures of silver nanoparticles biosynthesized using endophytic fungi. Journal of Microscopy and Ultrastructure, 3(1), 29-37. http://dx.doi.org/10.1016/j.jmau.2014.10.004. PMid:30023179.
http://dx.doi.org/10.1016/j.jmau.2014.10...
; Qian et al., 2013Qian, Y., Yu, H., He, D., Yang, H., Wang, W., Wan, X., & Wang, L. (2013). Biosynthesis of silver nanoparticles by the endophytic fungus Epicoccum nigrum and their activity against pathogenic fungi. Bioprocess and Biosystems Engineering, 36(11), 1613-1619. http://dx.doi.org/10.1007/s00449-013-0937-z. PMid:23463299.
http://dx.doi.org/10.1007/s00449-013-093...
; Singh et al., 2017Singh, T., Jyoti, K., Patnaik, A., Singh, A., Chauhan, R., & Chandel, S. (2017). Biosynthesis, characterization and antibacterial activity of silver nanoparticles using an endophytic fungal supernatant of Raphanus sativus. Journal of Genetic Engineering and Biotechnology, 15(1), 31-39. http://dx.doi.org/10.1016/j.jgeb.2017.04.005. PMid:30647639.
http://dx.doi.org/10.1016/j.jgeb.2017.04...
; Sogra Fathima & Balakrishnan, 2014Sogra Fathima, B., & Balakrishnan, R. M. (2014). Biosynthesis and optimization of silver nanoparticles by endophytic fungus Fusarium solani. Materials Letters, 132, 428-431. http://dx.doi.org/10.1016/j.matlet.2014.06.143.
http://dx.doi.org/10.1016/j.matlet.2014....
). The main genera of fungi reported as efficient in extracellular biosynthesis of AgNPs include Fusarium spp. (Balakumaran et al., 2015Balakumaran, M. D., Ramachandran, R., & Kalaichelvan, P. T. (2015). Exploitation of endophytic fungus, Guignardia mangiferae for extracellular synthesis of silver nanoparticles and their in vitro biological activities. Microbiological Research, 178, 9-17. http://dx.doi.org/10.1016/j.micres.2015.05.009. PMid:26302842.
http://dx.doi.org/10.1016/j.micres.2015....
; Husseiny et al., 2015Husseiny, S. M., Salah, T. A., & Anter, H. A. (2015). Biosynthesis of size controlled silver nanoparticles by Fusarium oxysporum, their antibacterial and antitumor activities. Beni-Suef University Journal of Basic and Applied Sciences, 4(3), 225-231. http://dx.doi.org/10.1016/j.bjbas.2015.07.004.
http://dx.doi.org/10.1016/j.bjbas.2015.0...
; Sogra Fathima & Balakrishnan, 2014Sogra Fathima, B., & Balakrishnan, R. M. (2014). Biosynthesis and optimization of silver nanoparticles by endophytic fungus Fusarium solani. Materials Letters, 132, 428-431. http://dx.doi.org/10.1016/j.matlet.2014.06.143.
http://dx.doi.org/10.1016/j.matlet.2014....
), Aspergillus (Balakumaran et al., 2015Balakumaran, M. D., Ramachandran, R., & Kalaichelvan, P. T. (2015). Exploitation of endophytic fungus, Guignardia mangiferae for extracellular synthesis of silver nanoparticles and their in vitro biological activities. Microbiological Research, 178, 9-17. http://dx.doi.org/10.1016/j.micres.2015.05.009. PMid:26302842.
http://dx.doi.org/10.1016/j.micres.2015....
; Devi & Joshi, 2015Devi, L. S., & Joshi, S. R. (2015). Ultrastructures of silver nanoparticles biosynthesized using endophytic fungi. Journal of Microscopy and Ultrastructure, 3(1), 29-37. http://dx.doi.org/10.1016/j.jmau.2014.10.004. PMid:30023179.
http://dx.doi.org/10.1016/j.jmau.2014.10...
; Ninganagouda et al., 2013Ninganagouda, S., Rathod, V., Jyoti, H., Singh, D., Prema, K., & Manzoor-Ul-Haq, S. (2013). Aspergillus flavus and their antimicrobial activity. International Journal of Pharma and Bio Sciences, 4(2), 222-229. Retrieved from https://www.researchgate.net/publication/236943633%0AEXTRACELLULAR
https://www.researchgate.net/publication...
), and Penicllium (Balakumaran et al., 2015Balakumaran, M. D., Ramachandran, R., & Kalaichelvan, P. T. (2015). Exploitation of endophytic fungus, Guignardia mangiferae for extracellular synthesis of silver nanoparticles and their in vitro biological activities. Microbiological Research, 178, 9-17. http://dx.doi.org/10.1016/j.micres.2015.05.009. PMid:26302842.
http://dx.doi.org/10.1016/j.micres.2015....
; Devi & Joshi, 2015Devi, L. S., & Joshi, S. R. (2015). Ultrastructures of silver nanoparticles biosynthesized using endophytic fungi. Journal of Microscopy and Ultrastructure, 3(1), 29-37. http://dx.doi.org/10.1016/j.jmau.2014.10.004. PMid:30023179.
http://dx.doi.org/10.1016/j.jmau.2014.10...
; Ma et al., 2017Ma, L., Su, W., Liu, J. X., Zeng, X. X., Huang, Z., Li, W., Liu, Z. C., & Tang, J. X. (2017). Optimization for extracellular biosynthesis of silver nanoparticles by Penicillium aculeatum Su1 and their antimicrobial activity and cytotoxic effect compared with silver ions. Materials Science and Engineering C, 77, 963-971. http://dx.doi.org/10.1016/j.msec.2017.03.294. PMid:28532117.
http://dx.doi.org/10.1016/j.msec.2017.03...
; Singh et al., 2013aSingh, D., Rathod, V., Ninganagouda, S., Herimath, J., & Kulkarni, P. (2013a). Biosynthesis of silver nanoparticle by endophytic fungi Pencillium sp. isolated from Curcuma longa (turmeric) and its antibacterial activity against pathogenic gram negative bacteria. Journal of Pharmacy Research, 7(5), 448-453. http://dx.doi.org/10.1016/j.jopr.2013.06.003.
http://dx.doi.org/10.1016/j.jopr.2013.06...
). AgNPs produced by fungal biosynthesis have antimicrobial properties against a wide range of pathogenic microorganisms, including fungi, Gram-positive and negative bacteria, as shown in Table 2.

Table 2
Antimicrobial effect of silver nanoparticles synthesized by fungus strains.

Gade et al. (2013)Gade, A., Gaikwad, S., Duran, N., & Rai, M. (2013). Screening of different species of Phoma for the synthesis of silver nanoparticles. Biotechnology and Applied Biochemistry, 60(5), 482-493. http://dx.doi.org/10.1002/bab.1141. PMid:23848561.
http://dx.doi.org/10.1002/bab.1141...
studied the ability of 18 species in the genus Phoma spp. to produce AgNPs, and concluded that all of them were efficient in terms of AgNPs biosynthesis. In general, the process yielded spherical nanoparticles, except for the species P. sorghina MTCC-2096, which produced AgNPs in the shape of nanorods. Sogra Fathima & Balakrishnan (2014)Sogra Fathima, B., & Balakrishnan, R. M. (2014). Biosynthesis and optimization of silver nanoparticles by endophytic fungus Fusarium solani. Materials Letters, 132, 428-431. http://dx.doi.org/10.1016/j.matlet.2014.06.143.
http://dx.doi.org/10.1016/j.matlet.2014....
studied the extracellular biosynthesis and optimization of AgNPs, using the endophytic fungus Fusarium solani. These authors obtained AgNPs of different shapes, with the predominance of 10-nm, spherical AgNPs. Husseiny et al. (2015)Husseiny, S. M., Salah, T. A., & Anter, H. A. (2015). Biosynthesis of size controlled silver nanoparticles by Fusarium oxysporum, their antibacterial and antitumor activities. Beni-Suef University Journal of Basic and Applied Sciences, 4(3), 225-231. http://dx.doi.org/10.1016/j.bjbas.2015.07.004.
http://dx.doi.org/10.1016/j.bjbas.2015.0...
demonstrated that the AgNPs (spherical and uniformly distributed) synthesized by Fusarium oxysporum were effective against S. aureus and E. coli. Ninganagouda et al. (2013)Ninganagouda, S., Rathod, V., Jyoti, H., Singh, D., Prema, K., & Manzoor-Ul-Haq, S. (2013). Aspergillus flavus and their antimicrobial activity. International Journal of Pharma and Bio Sciences, 4(2), 222-229. Retrieved from https://www.researchgate.net/publication/236943633%0AEXTRACELLULAR
https://www.researchgate.net/publication...
reported AgNPs extracellular biosynthesis by Aspergillus flavus, which were efficient against the Gram-negative bacteria tested, P. aeruginosa, E. coli and K. pneumonia.

Regarding the antifungal properties of AgNPs from fungal biosynthesis, Qian et al. (2013)Qian, Y., Yu, H., He, D., Yang, H., Wang, W., Wan, X., & Wang, L. (2013). Biosynthesis of silver nanoparticles by the endophytic fungus Epicoccum nigrum and their activity against pathogenic fungi. Bioprocess and Biosystems Engineering, 36(11), 1613-1619. http://dx.doi.org/10.1007/s00449-013-0937-z. PMid:23463299.
http://dx.doi.org/10.1007/s00449-013-093...
observed a high extracellular biosynthesis of AgNPs by the endophytic fungus Epicoccum nigrum isolated from Phellodendron amurense. The antifungal activities of the AgNPs obtained were demonstrated against 9 fungus strains (Candida albicans ATCC 90028, C. parapsilosis ATCC 22019, C. tropicalis JLCC 31384, C.krusei ATCC 6258, Cryptococcus neoformans IFM 45687, A. fumigatus IFM 40808, A.flavus IFM 55648, F. Solani JLCC 30866, and Sporothrix schenckii JLCC 32757). Studies demonstrated that endophytic fungi (Aspergillus tamarii PFL2, Aspergillus niger PFR6 and Penicllium ochrochloron PFR8) isolated from the ethno medicinal plant Potentilla fulgens L. also show the ability to synthetize AgNPs (Devi & Joshi, 2014Devi, L. S., & Joshi, S. R. (2014). Evaluation of the antimicrobial potency of silver nanoparticles biosynthesized by using an endophytic fungus, Cryptosporiopsis ericae PS4. Journal of Microbiology (Seoul, Korea), 52(8), 667-674. http://dx.doi.org/10.1007/s12275-014-4113-1. PMid:24994011.
http://dx.doi.org/10.1007/s12275-014-411...
, 2015Devi, L. S., & Joshi, S. R. (2015). Ultrastructures of silver nanoparticles biosynthesized using endophytic fungi. Journal of Microscopy and Ultrastructure, 3(1), 29-37. http://dx.doi.org/10.1016/j.jmau.2014.10.004. PMid:30023179.
http://dx.doi.org/10.1016/j.jmau.2014.10...
). Cryptosporiopsis ericae PS4 was also efficient for extracellular biosynthesis of AgNPs, which were effective against pathogenic microorganisms, including S. aureus MTCC96, S. enteric MTCC735, E. coli MTCC730, E. faecalis MTCC2729, and C. albicans MTCC 183 (Devi & Joshi, 2014Devi, L. S., & Joshi, S. R. (2014). Evaluation of the antimicrobial potency of silver nanoparticles biosynthesized by using an endophytic fungus, Cryptosporiopsis ericae PS4. Journal of Microbiology (Seoul, Korea), 52(8), 667-674. http://dx.doi.org/10.1007/s12275-014-4113-1. PMid:24994011.
http://dx.doi.org/10.1007/s12275-014-411...
). Chen et al. (2016)Chen, X., Yan, J. K., & Wu, J. Y. (2016). Characterization and antibacterial activity of silver nanoparticles prepared with a fungal exopolysaccharide in water. Food Hydrocolloids, 53, 69-74. http://dx.doi.org/10.1016/j.foodhyd.2014.12.032.
http://dx.doi.org/10.1016/j.foodhyd.2014...
produced AgNPs using an exopolysaccharide obtained by means of fermentation of a medicinal fungus and AgNO3 in distilled water. These nanoparticles showed antimicrobial effect against Gram-positive and negative bacteria.

The aqueous extract of the mycelium of Rhizopus stolonifer demonstrated to be effective in the biosynthesis of spherical) AgNPs (diameter: 9.46 ± 2.64 nm) (AbdelRahim et al., 2017AbdelRahim, K., Mahmoud, S. Y., Ali, A. M., Almaary, K. S., Mustafa, A. E. Z. M. A., & Husseiny, S. M. (2017). Extracellular biosynthesis of silver nanoparticles using Rhizopus stolonifer. Saudi Journal of Biological Sciences, 24(1), 208-216. http://dx.doi.org/10.1016/j.sjbs.2016.02.025. PMid:28053592.
http://dx.doi.org/10.1016/j.sjbs.2016.02...
). The AgNPs produced by the fungus Cordyceps sinensis (Berk.) Sacc Cs-HK1, presented antimicrobial activity against E. coli (1.6 mg/mL) and S. aureus (0.8 mg/mL) (Chen et al., 2016Chen, X., Yan, J. K., & Wu, J. Y. (2016). Characterization and antibacterial activity of silver nanoparticles prepared with a fungal exopolysaccharide in water. Food Hydrocolloids, 53, 69-74. http://dx.doi.org/10.1016/j.foodhyd.2014.12.032.
http://dx.doi.org/10.1016/j.foodhyd.2014...
). Singh et al. (2017)Singh, T., Jyoti, K., Patnaik, A., Singh, A., Chauhan, R., & Chandel, S. (2017). Biosynthesis, characterization and antibacterial activity of silver nanoparticles using an endophytic fungal supernatant of Raphanus sativus. Journal of Genetic Engineering and Biotechnology, 15(1), 31-39. http://dx.doi.org/10.1016/j.jgeb.2017.04.005. PMid:30647639.
http://dx.doi.org/10.1016/j.jgeb.2017.04...
reported the extracellular biosynthesis of spherical AgNPs (diameter: 4-30 nm) using the supernatant of an endophytic fungus (Alternaria spp) isolated from Raphanus sativus, which showed antimicrobial properties against pathogenic bacteria (methicillin-resistant B. subtilis, S. aureus, E. coli and S. marcescens). The endophytic fungus Pencillium spp. isolated from the leaves of Curcuma longa was efficient in the extracellular biosynthesis of spherical AgNPs (diameter: 25 nm), which was effective against several pathogens, especially P. aeruginosa and K. pneumoniae (Singh et al., 2013aSingh, D., Rathod, V., Ninganagouda, S., Herimath, J., & Kulkarni, P. (2013a). Biosynthesis of silver nanoparticle by endophytic fungi Pencillium sp. isolated from Curcuma longa (turmeric) and its antibacterial activity against pathogenic gram negative bacteria. Journal of Pharmacy Research, 7(5), 448-453. http://dx.doi.org/10.1016/j.jopr.2013.06.003.
http://dx.doi.org/10.1016/j.jopr.2013.06...
).

Balakumaran et al. (2015)Balakumaran, M. D., Ramachandran, R., & Kalaichelvan, P. T. (2015). Exploitation of endophytic fungus, Guignardia mangiferae for extracellular synthesis of silver nanoparticles and their in vitro biological activities. Microbiological Research, 178, 9-17. http://dx.doi.org/10.1016/j.micres.2015.05.009. PMid:26302842.
http://dx.doi.org/10.1016/j.micres.2015....
isolated 13 species of endophytic fungi in 9 different samples of plant leaves, and observed that only 6 fungi (A. niger, Aspergillus spp., Colletotrichum spp., F. oxysporum, Guignardia spp., and Penicillium spp.) were able to produce AgNPs by extracellular biosynthesis. In particular, Guignardia spp., isolated from Citrus spp., showed the best results for extracellular biosynthesis of AgNPs that were effective against several Gram-negative and Gram-positive bacterial species, including E. coli ATCC 8739, Proteus mirabilis MTCC 425, P. aeruginosa ATCC 27853, S. aureus ATCC 29736, E. faecalis ATCC 29212 and B. subtilis ATCC 6633. AgNPs produced by the fungus Penicillium aculeatum Su1 also presented antimicrobial activity against Gram-negative and positive bacteria and fungi at levels of 0.05-0.2 mg/mL, with greatest effect on C. albicans, followed by P. aeruginosa, B. subtilis, S. aureus and E. coli (Ma et al., 2017Ma, L., Su, W., Liu, J. X., Zeng, X. X., Huang, Z., Li, W., Liu, Z. C., & Tang, J. X. (2017). Optimization for extracellular biosynthesis of silver nanoparticles by Penicillium aculeatum Su1 and their antimicrobial activity and cytotoxic effect compared with silver ions. Materials Science and Engineering C, 77, 963-971. http://dx.doi.org/10.1016/j.msec.2017.03.294. PMid:28532117.
http://dx.doi.org/10.1016/j.msec.2017.03...
).

4 Application of silver nanoparticles in food packaging

Many of the packages used in the food industry are made of petroleum-based plastics. When compared with other materials (paper, glass, wood, metals and ceramic), plastic packages have advantages in terms of physical-mechanic characteristics, such as weight, flexibility, mechanical resistance, and physical-chemical and biological characteristics related to quality, health protection and safety (Claro & Magalhães, 2017Claro, F. C., & Magalhães, W. L. E. (2017). Síntese de nanopartículas de prata em filmes de nanocelulose. Embrapa, 149, 149-152.). These features provide to plastic materials excellent conditions to produce active packages obtained by the addition of nanocompounds with antimicrobial properties. According to Almeida et al. (2015)Almeida, A. C. S., Franco, A. E. N., Peixoto, F. M., Pessanha, K. L., & Melo, N. R. (2015). Application of nanothecnology in food packaging. Polímeros, 25, 89-97. http://dx.doi.org/10.1590/0104-1428.2069.
http://dx.doi.org/10.1590/0104-1428.2069...
, packages with nanotechnological applications have better physical-chemical properties, reduced hydrophilic characteristics, better biodegradability, and increased value-added. Active packages make up a new generation of food packages obtained by the incorporation of metallic nanoparticles to polymer films (Emamifar et al., 2012Emamifar, A., Kadivar, M., Shahedi, M., & Solimanian-Zad, S. (2012). Effect of nanocomposite packaging containing Ag and ZnO on reducing pasteurization temperature of orange juice. Journal of Food Processing and Preservation, 36(2), 104-112. http://dx.doi.org/10.1111/j.1745-4549.2011.00558.x.
http://dx.doi.org/10.1111/j.1745-4549.20...
).

The advantage of silver antimicrobial agents is that they can be easily incorporated to several materials, such as plastics and textiles, making them useful in wide spectrum applications, maintaining their antimicrobial activity in situ, in which traditional antimicrobial agents would be unstable (Almeida et al., 2015Almeida, A. C. S., Franco, A. E. N., Peixoto, F. M., Pessanha, K. L., & Melo, N. R. (2015). Application of nanothecnology in food packaging. Polímeros, 25, 89-97. http://dx.doi.org/10.1590/0104-1428.2069.
http://dx.doi.org/10.1590/0104-1428.2069...
). According to Carbone et al. (2016)Carbone, M., Donia, D. T., Sabbatella, G., & Antiochia, R. (2016). Silver nanoparticles in polymeric matrices for fresh food packaging. Journal of King Saud University - Science, 28(4), 273-279. https://doi.org/10.1016/j.jksus.2016.05.004.
https://doi.org/10.1016/j.jksus.2016.05....
, AgNPs may be incorporated to non-degradable (polyethylene, polyvinyl chloride, vinyl alcohol) and biodegradable polymers (cellulose, starch, chitosan, agarose) to produce food packages, as presented in Table 3.

Table 3
Antimicrobial effect of silver nanoparticles (AgNP) incorporated to food packages.

Emamifar et al. (2012)Emamifar, A., Kadivar, M., Shahedi, M., & Solimanian-Zad, S. (2012). Effect of nanocomposite packaging containing Ag and ZnO on reducing pasteurization temperature of orange juice. Journal of Food Processing and Preservation, 36(2), 104-112. http://dx.doi.org/10.1111/j.1745-4549.2011.00558.x.
http://dx.doi.org/10.1111/j.1745-4549.20...
evaluated the inhibition effect of packages impregnated with Ag and ZnO nanoparticles on Lactobacillus plantarum in orange juice, and observed that the bacterium was inhibited in the product stored at 4 °C. However, the silver nanoparticle presented the greatest antimicrobial activity, compared with the ZnO nanoparticle, in juices stored for up to 112 days. Panea et al. (2014)Panea, B., Ripoll, G., González, J., Fernández-Cuello, Á., & Albertí, P. (2014). Effect of nanocomposite packaging containing different proportions of ZnO and Ag on chicken breast meat quality. Journal of Food Engineering, 123, 104-112. http://dx.doi.org/10.1016/j.jfoodeng.2013.09.029.
http://dx.doi.org/10.1016/j.jfoodeng.201...
demonstrated the antimicrobial effect of nanocomposite packages of chicken breast containing different ZnO and Ag ratios. However, the authors observed that the meat sensory attributes were slightly affected by the package, with increased cereal odor and tenderness after 10 days of storage, although no differences were found in color and appearance of the product after 21 days of storage.

Fernández et al. (2010)Fernández, A., Picouet, P., & Lloret, E. (2010). Cellulose-silver nanoparticle hybrid materials to control spoilage-related microflora in absorbent pads located in trays of fresh-cut melon. International Journal of Food Microbiology, 142(1–2), 222-228. http://dx.doi.org/10.1016/j.ijfoodmicro.2010.07.001. PMid:20656367.
http://dx.doi.org/10.1016/j.ijfoodmicro....
stored fresh melon cuts in plastic films based on cellulose incorporated with spherical AgNP (5 and 35 nm diameters), and obtained low counts of yeasts, mesophilic and psychrophilic bacteria, when compared with the control films (without AgNP). Beigmohammadi et al. (2016)Beigmohammadi, F., Peighambardoust, S. H., Hesari, J., Azadmard-Damirchi, S., Peighambardoust, S. J., & Khosrowshahi, N. K. (2016). Antibacterial properties of LDPE nanocomposite films in packaging of UF cheese. Lebensmittel-Wissenschaft + Technologie, 65, 106-111. http://dx.doi.org/10.1016/j.lwt.2015.07.059.
http://dx.doi.org/10.1016/j.lwt.2015.07....
developed low density polyethylene (LDPE) package films incorporated with Ag, copper oxide (CuO), and zinc oxide (ZnO), and found a reduction in coliform counts of ultra-filtered cheese stored at 4 ± 0.5 °C for 4 weeks.

Azlin-Hasim et al. (2015)Azlin-Hasim, S., Cruz-Romero, M. C., Morris, M. A., Cummins, E., & Kerry, J. P. (2015). Effects of a combination of antimicrobial silver low density polyethylene nanocomposite films and modified atmosphere packaging on the shelf life of chicken breast fillets. Food Packaging and Shelf Life, 4, 26-35. http://dx.doi.org/10.1016/j.fpsl.2015.03.003.
http://dx.doi.org/10.1016/j.fpsl.2015.03...
studied the effect of the combination between LDPE film package with AgNPs and modified atmosphere in the shelf life of chicken breast fillets. Two films were developed with the incorporation of AgNPs in the polymer (0.5 and 1% polymer weight, w/w), and tested for their antimicrobial activity against several bacterial species. Compared with the control film (without AgNPs), bacterial growth in the nanocomposite Ag/LDPE film was significantly inhibited until day 6 (up to 22.5% reduction), which significantly increased the shelf life of the chicken breast fillet. Kuuliala et al. (2015)Kuuliala, L., Pippuri, T., Hultman, J., Auvinen, S. M., Kolppo, K., Nieminen, T., Karp, M., Björkroth, J., Kuusipalo, J., & Jääskeläinen, E. (2015). Preparation and antimicrobial characterization of silver-containing packaging materials for meat. Food Packaging and Shelf Life, 6, 53-60. http://dx.doi.org/10.1016/j.fpsl.2015.09.004.
http://dx.doi.org/10.1016/j.fpsl.2015.09...
also developed LDPE package films containing AgNPs to protect fresh pork sirloin stored at 6 °C for 28 days. The antimicrobial effect of the films against the bacteria associated with meat spoilage was determined, including Leuconostoc gelidum subsp. gasicomitatum (LMG 18811T), Lactobacillus sakei (23K), Lactococcus piscium (MKFS47), Carnobacterium divergens (DSMZ 20623T) and Hafnia alvei (DSM30163). In the in vitro study of the films, they were effective against L. piscium, B. thermosphacta, H. alvei, L. sakei and C. divergens. However, the AgNPs films did not affect the microbial growth in the packed samples of pork sirloin during storage, when compared with the control. This finding was attributed to the different dynamics in silver ion release on meat surfaces, or to the interaction between silver and amino acids.

5 Toxicological aspects of silver nanoparticles

In spite of all the advantages related to the use of AgNPs, one possible constraint in the use of nanoparticles in food packages is their migration to the food, leading to potential toxicity problems (Panea et al., 2014Panea, B., Ripoll, G., González, J., Fernández-Cuello, Á., & Albertí, P. (2014). Effect of nanocomposite packaging containing different proportions of ZnO and Ag on chicken breast meat quality. Journal of Food Engineering, 123, 104-112. http://dx.doi.org/10.1016/j.jfoodeng.2013.09.029.
http://dx.doi.org/10.1016/j.jfoodeng.201...
). Echegoyen & Nerín (2013)Echegoyen, Y., & Nerín, C. (2013). Nanoparticle release from nano-silver antimicrobial food containers. Food and Chemical Toxicology, 62, 16-22. http://dx.doi.org/10.1016/j.fct.2013.08.014. PMid:23954768.
http://dx.doi.org/10.1016/j.fct.2013.08....
assessed Ag migration in three types of containers available in the USA, including polypropylene plastic bags and polyolefin containers. Ag migration was tested using two simulated food conditions using ethanol (50% v/v) and acetic acid (3% v/v) at 40 °C for 10 days and 70 °C for 2 h. The authors demonstrated the migration of Ag from the package to the liquid, which was greater in acetic acid at 40 °C for 10 days. However, total Ag migration was below the maximum migration limits determined by European regulations. Jokar & Abdul Rahman (2014)Jokar, M., & Abdul Rahman, R. (2014). Study of silver ion migration from melt-blended and layered-deposited silver polyethylene nanocomposite into food simulants and apple juice. Food Additives & Contaminants. Part A, Chemistry, Analysis, Control, Exposure & Risk Assessment, 31(4), 734-742. http://dx.doi.org/10.1080/19440049.2013.878812. PMid:24392748.
http://dx.doi.org/10.1080/19440049.2013....
assessed the Ag+ migration in simulated food conditions (distilled water, 3% acetic acid, 10% ethanol) and in apple juice stored at 4 and 40 °C for 30 days. The migrated AG from package to the acetic acid solution and apple juice was higher than in ethanol and distilled water, indicating that acidity promotes Ag+ release by the polymers due to their dissolution.

Recent studies have investigated the effects of AgNPs in vivo and in vitro (Garcia et al., 2016Garcia, T., Lafuente, D., Blanco, J., Sánchez, D. J., Sirvent, J. J., Domingo, J. L., & Gómez, M. (2016). Oral subchronic exposure to silver nanoparticles in rats. Food and Chemical Toxicology, 92, 177-187. http://dx.doi.org/10.1016/j.fct.2016.04.010. PMid:27090107.
http://dx.doi.org/10.1016/j.fct.2016.04....
). AgNPs may accumulate in several organs, including the liver, kidneys, testicles, and brain (Bagheri-Abassi et al., 2015Bagheri-Abassi, F., Alavi, H., Mohammadipour, A., Motejaded, F., & Ebrahimzadeh-Bideskan, A. (2015). The effect of silver nanoparticles on apoptosis and dark neuron production in rat hippocampus. Iranian Journal of Basic Medical Sciences., 18(7), 644-648. PMid:26351553.; Garcia et al., 2016Garcia, T., Lafuente, D., Blanco, J., Sánchez, D. J., Sirvent, J. J., Domingo, J. L., & Gómez, M. (2016). Oral subchronic exposure to silver nanoparticles in rats. Food and Chemical Toxicology, 92, 177-187. http://dx.doi.org/10.1016/j.fct.2016.04.010. PMid:27090107.
http://dx.doi.org/10.1016/j.fct.2016.04....
). Garcia et al. (2016)Garcia, T., Lafuente, D., Blanco, J., Sánchez, D. J., Sirvent, J. J., Domingo, J. L., & Gómez, M. (2016). Oral subchronic exposure to silver nanoparticles in rats. Food and Chemical Toxicology, 92, 177-187. http://dx.doi.org/10.1016/j.fct.2016.04.010. PMid:27090107.
http://dx.doi.org/10.1016/j.fct.2016.04....
demonstated that the oral exposure of Sprague Dawley adult rats to subchornic doses of AgNPs led to an accumulation of Ag in differnt tissues at doses of 50, 100 and 200 mg/kg/day. Moreover, high doses of AgNPs can cause hepatotoxic (El Mahdy et al., 2015El Mahdy, M. M., Eldin, T. A. S., Aly, H. S., Mohammed, F. F., & Shaalan, M. I. (2015). Evaluation of hepatotoxic and genotoxic potential of silver nanoparticles in albino rats. Experimental and Toxicologic Pathology, 67(1), 21-29. http://dx.doi.org/10.1016/j.etp.2014.09.005. PMid:25446800.
http://dx.doi.org/10.1016/j.etp.2014.09....
), neurotoxic (Bagheri-Abassi et al., 2015Bagheri-Abassi, F., Alavi, H., Mohammadipour, A., Motejaded, F., & Ebrahimzadeh-Bideskan, A. (2015). The effect of silver nanoparticles on apoptosis and dark neuron production in rat hippocampus. Iranian Journal of Basic Medical Sciences., 18(7), 644-648. PMid:26351553.), and genotoxic effects (El Mahdy et al., 2015El Mahdy, M. M., Eldin, T. A. S., Aly, H. S., Mohammed, F. F., & Shaalan, M. I. (2015). Evaluation of hepatotoxic and genotoxic potential of silver nanoparticles in albino rats. Experimental and Toxicologic Pathology, 67(1), 21-29. http://dx.doi.org/10.1016/j.etp.2014.09.005. PMid:25446800.
http://dx.doi.org/10.1016/j.etp.2014.09....
; Patlolla et al., 2015Patlolla, A. K., Hackett, D., & Tchounwou, P. B. (2015). Genotoxicity study of silver nanoparticles in bone marrow cells of Sprague-Dawley rats. Food and Chemical Toxicology, 85, 52-60. http://dx.doi.org/10.1016/j.fct.2015.05.005. PMid:26032631.
http://dx.doi.org/10.1016/j.fct.2015.05....
). However, the possibility of migration of such toxic levels from active packages to foods is very low, although possible toxicological effects of AGNPs levels in foods as a consequence of migration from packages have not been assessed so far.

Li et al. (2018)Li, W., Li, L., Zhang, H., Yuan, M., & Qin, Y. (2018). Evaluation of PLA nanocomposite films on physicochemical and microbiological properties of refrigerated cottage cheese. Journal of Food Processing and Preservation, 42(1), 1-9. http://dx.doi.org/10.1111/jfpp.13362.
http://dx.doi.org/10.1111/jfpp.13362...
evaluated the migration of AgNPs of poly (lactic acid) (PLA) matrix impregnated with TiO2 + AgNPs in Yunnan cottage cheese. The authors observed that the Ag ions migration (0.02 mg/kg) into the food increased with storage time. However, the total Ag migration was lower than the maximum migration limits (10 mg/Kg) determined by European regulations for food contact material. Chi et al. (2018)Chi, H., Xue, J., Zhang, C., Chen, H., Li, L., & Qin, Y. (2018). High pressure treatment for improving water vapour barrier properties of poly (lactic acid)/Ag nanocomposite films. Polymers, 10(9), 1-11. http://dx.doi.org/10.3390/polym10091011. PMid:30960936.
http://dx.doi.org/10.3390/polym10091011...
studied the migration behavior of AgNPs from the PLA films in the presence of 50% (v/v) ethanol as a food simulant. The author reported that high pressure treatment at 200 to 400 MPa reduced the migration of AgNPs from the films. The amounts of AgNPs migrated were 0.354 and 0.409 mg/Kkg for treatment at 200 to 400 MPa, respectively. Thus, the author conclude that the PLA films treated by high pressure were safe and suitable for contact with foodstuffs.

6 Conclusions

Silver nanoparticles are potential antimicrobial agents against a wide range of microorganisms, including highly pathogenic Gram-positive and Gram-negative bacteria and fungi. Biological synthesis of AgNPs is considered the most correct and reliable method to obtain these particles. The use of bacteria and fungi has been widely explored for extracellular biosynthesis of AgNPs, demonstrating to be efficient and promising. Polymers are the main materials tested for impregnation with AgNPs to produce active food packages. However, it is important to carry out migration tests when a new package based on AgNP is produced. Additionally, further studies are necessary to determine the effective levels for AgNP inclusion in food packages.

  • Practical Application: One of the main objectives of the food industry is to increase the shelf life of foodstuffs by using appropriate methods of microbial control in processes and products. In this context, results listed in the present review on the application of silver nanoparticles (AgNPs) in food packages offer new perspectives to prevent microbial spoilage and increase shelf life. However, AgNPs should be produced by ecologically correct methods, and the results from different studies regarding their antimicrobial effects should be critically evaluated before using these materials in food packages.

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Publication Dates

  • Publication in this collection
    27 June 2019
  • Date of issue
    Oct-Dec 2019

History

  • Received
    14 Nov 2018
  • Accepted
    29 Mar 2019
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