Low levels of silver in food packaging materials may have no functional advantage, instead enhance microbial spoilage of food through hormetic effect
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)
- et al.
Silver nanoparticles induce toxicity in a549 cells via ros-dependent and ros-independent pathways
Toxicology in Vitro
(2013) - et al.
Food applications of nanotechnologies: An overview of opportunities and challenges for developing countries
Trends in Food Science & Technology
(2011) - et al.
Migration and exposure assessment of silver from a PVC nanocomposite
Food Chemistry
(2013) - et al.
Possibilities of gutta-percha–centered infection in endodontically treated teeth: An in vitro study
Journal of Endodontics
(2010) - et al.
Effect of tissue fluids on hydrophobicity and adherence of Enterococcus faecalis to dentin
Journal of Endodontics
(2007) - et al.
Extending life span by increasing oxidative stress
Free Radical Biology and Medicine
(2011) - et al.
Microbial shelf-life of high-pressure-homogenised milk
International Dairy Journal - INT DAIRY J
(2007) - et al.
Exploring the redox balance inside gram-negative bacteria with redox-sensitive GFP
Free Radical Biology and Medicine
(2016) - et al.
Chinese consumer demand for food safety attributes in milk products
Food Policy
(2008) - Agri-Food and Veterinary Authority of Singapore (AVA). In Microbiological standard for food , in: Sale of food Act...