Elsevier

Food Control

Volume 123, May 2021, 107768
Food Control

Low levels of silver in food packaging materials may have no functional advantage, instead enhance microbial spoilage of food through hormetic effect

https://doi.org/10.1016/j.foodcont.2020.107768Get rights and content

Highlights

  • Evaluated food packaging materials with claims on antimicrobial silver technology.

  • ICP-OES based determination showed nominal levels of silver in packaging material.

  • Low levels of silver had no functional advantage in improving shelf-life of food.

  • Sub-lethal levels of silver showed hormesis by inducing mild oxidative stress.

  • Bacterial viability and biofilm formation increased at sub-lethal levels of silver.

Abstract

Recently there has been an influx of silver infused food packaging materials that claim to enhance the shelf-life of stored food. We tested commercially available normal plastic packing material (S1) and two packing materials (S2 and S3) which claimed to contain silver to enhance shelf-life of stored food for the presence of silver and its antibacterial performance. Microwave assisted acid digestion of the plastic material and ICP-OES analysis confirmed the presence of silver in S2 (103 μg/g) and S3 (74 μg/g) but not in S1. Migration studies showed that 12–14% of silver incorporated into the plastic could leach into milk (used as a food simulant). Shelf-life studies conducted using milk showed that in comparison to normal plastic materials (S1), those containing silver (S2 and S3) had no functional advantage but slightly enhanced the microbial growth. Further studies showed that sub-lethal concentration of silver generates reactive oxygen species (ROS) within bacterial cells (Escherichia coli ATCC 25922 and Staphylococcus aureus ATCC 25923) accompanied by increased cell proliferation and biofilm formation suggestive of a hormetic effect. In short, these studies showed that the incorporation of silver at low concentration in packaging materials may not provide a functional advantage, but mitigate the migration of silver into the stored food products at sub-lethal concentration and may induce bacterial hormesis and accelerate food spoilage.

Introduction

Metallic silver has been widely applied in medical, personal care and food contact materials due to its wide-spectrum antimicrobial properties, stability and relatively low cost. Additionally, the thermal stability of metallic silver and the possibility of blending it with polymeric matrices make it an ideal antimicrobial agent for preparing food packaging materials. The metallic silver incorporated into the polymer matrix releases Ag+ ions into the surrounding medium. Highly reactive Ag+ ions induces multiple damages in microbial cells to keep food safe from pathogenic and spoilage microorganisms. In the recent past, there has been a renewed interest in silver incorporated food packaging materials because of the advent of silver nanotechnology. Nanomaterials of silver are the most frequently used because of their unique physical and antimicrobial properties (Vance et al., 2015). While silver offers advantages in terms of its stability, durability (Kumar & Münstedt, 2005) and wide range of antimicrobial activity (George, Tay, Phue, Gardner, & Sukumaran, 2019; Toh, Faure, Mohd Amin, Hay, & George, 2017) to make it an ideal antimicrobial agent to be used in plastics meant for food packaging, its safety to human and environment is questionable (George et al., 2012, 2014; Kaweeteerawat, Na Ubol, Sangmuang, Aueviriyavit, & Maniratanachote, 2017). This is particularly of concern as previous studies have shown that nanosilver incorporated into packaging materials could migrate into food (Huang et al., 2011).

Migration of plastics or components of packaging materials to the stored food has been identified as a potential health hazard because of the possible consumer exposure during consumption of food (Chaudhry & Castle, 2011; Cushen, Kerry, Morris, Cruz-Romero, & Cummins, 2013). Therefore, regulatory agencies around the world have mandated specifications on the allowable amount of migration of packaging material components to the stored food. While, there are standardized protocols to determine the migration of plastics and other additives to food (Commission regulation (EU) no. 10/2011), the instrumentation and know-how on identifying migration of metallic additives and nanomaterials and their degradation products to the stored food are largely under developed (O'Brien & Cummins, 2008). Furthermore, the functional advantage of incorporating food packaging products with antimicrobial agents should be evaluated against its potential risk to human health. Data on the functional advantage of silver in food packaging products and their potential health risks are required for informed regulatory decision making on the market rights of such products.

Most of the existing studies have evaluated the toxic effects of silver at relatively high doses while the health and environmental risk originating from low doses of silver remains largely elusive. Studies have shown that a sub-lethal concentration of silver could cause proliferation in bacterial cells by adaptive mechanisms, a process known as hormesis (Iavicoli, Leso, Fontana, & Calabrese, 2018). It is important to investigate whether the application of a sub-lethal concentration of silver in food packaging systems could migrate in the food matrixes and initiate an increase in bacterial population rather than showing antimicrobial properties. This is because, induction of oxidative stress is regarded as one of the mechanisms of silver toxicity (Chairuangkitti et al., 2013) and sub-lethal concentrations of ROS have shown to stimulate the expression of defence mechanisms in bacteria at enzymatic, transcriptional or genetic level leading to hormesis (Cap, Váchová, & Palkova, 2012; Tkachenko, 2018).

In this study, we investigated the possible migration of silver from commercially available food packaging materials into milk (food simulant) and compared the functional properties of food packaging materials with and without silver by conducting shelf-life studies. Contrary to our expectations, milk stored in silver incorporated packaging material had higher bacterial count. We hypothesized and showed that sub-lethal concentrations of silver could mediate hormesis in bacteria. The results from our studies, indeed suggest that sub-lethal levels of silver incorporated in food packaging material may have no functional advantage but, on the contrary lead to increased microbial activity.

Section snippets

Test materials

Three types of plastic bags, a normal polyethylene (PE) plastic (S1) (Home Proud Brand; Malaysia) and two high density polyethylene (HDPE) plastic bags with claims of containing silver (S2) (Komax Brand; South Korea) and S3 (Humming Bio; South Korea) intended for food storage were purchased from commercial suppliers in Singapore. The packaging materials for testing were handled under strict aseptic conditions to avoid any external contamination and were kept under the UV light (inside biosafety

IDL and MDL were detected for silver using ICP-OES where MDL value was the highest for vinegar

The measured IDL for silver using ICP-OES was identified to be 0.6 μg/L. Since we were interested in detecting silver present in different matrices, determination of the MDL was also essential. MDL is the minimum concentration of analyte in a sample that can be determined and reported to be different from the blank with 99% level of confidence. MDL determined for water, vinegar and milk samples are 6, 10, and 1 μg/L, respectively. Among the tested food simulants, we noticed that the MDL value

Conclusion

Based on our findings, we could infer that the level of silver in the tested food packaging materials is extremely low to impart any antimicrobial effect and improve the shelf-life of the stored food. On the contrary, as observed in this study, the nominal level of silver could induce bacterial hormesis leading to an accelerated spoilage of food and increased chances of health risks. Besides, the migration of silver to food contribute to a potential danger of unintended exposure of consumers.

CRediT author statement

Saji George: Design of study, overall coordination, supervision and guidance on progression and interpretation of data, manuscript writing. Ling Li Teo: Detection of IDL and MDL, optimization of conditions for ICP-OES. Satwik Majumder: Dose response studies using AgNO3 to determine bacterial hormesis, measurement of ROS and biofilm assay, interpretation of data, manuscript writing, manuscript review/editing. Wan Lin Chew: Preparation of materials, ICP-OES studies. Gek Hoon Khoo: Overall design

Declaration of interests

The authors (Saji George, Ling Li Teo, Satwik Majumder, Wan Lin Chew, Gek Hoon Khoo) declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgement

SG acknowledges institutional funding (FYP and CDP) from Nanyang Polytechnic, MOE 2012-TIF-1-G-067 and Canada Research Chair CRC/George/X-coded/248991 for supporting this work..

References (35)

  • G.I. Borge et al.

    Growth and toxin profiles of Bacillus cereus isolated from different food sources

    International Journal of Food Microbiology

    (2001)
  • M. Cap et al.

    Reactive oxygen species in the signaling and adaptation of multicellular microbial communities

    Oxidative medicine and cellular longevity

    (2012)
  • no. 10/2011: Plastic materials and articles intended to come into contact with food

    (2011)
  • A.L. Dale et al.

    Modeling nanosilver transformations in freshwater sediments

    Environmental Science & Technology

    (2013)
  • P.N. Danese et al.

    The outer membrane protein, antigen 43, mediates cell-to-cell interactions within Escherichia coli biofilms

    Molecular Microbiology

    (2000)
  • S. George et al.

    Differential effect of solar light in increasing the toxicity of silver and titanium dioxide nanoparticles to a fish cell line and zebrafish embryos

    Environmental Science & Technology

    (2014)
  • S. George et al.

    Surface defects on plate-shaped silver nanoparticles contribute to its hazard potential in a fish gill cell line and zebrafish embryos

    ACS Nano

    (2012)
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