Impact of photodynamic inactivation on microbial safety in foods

Keywords: antimicrobial treatment, curcumin, food preservation, food safety, green technology, photodynamic, photosensitiser, reactive oxygen species.

The key element in achieving good health and sustaining life is access to nutritious and safe food. According to the World Health Organization, over 200 different diseases with severity ranging from diarrhoea to cancers can be caused by unsafe food consumption, which contains harmful microorganisms or chemical substances.¹ Food safety is generally influenced by the growing world population, climate change, and globalisation of food trade. Therefore, it contributes greatly to global food and nutrition security, as well as to national economies.

Food industry traditionally uses conventional thermal-based processing such as dry-heating and steam-heating to reduce the microbial contamination of foods caused by vegetative cells, spores, and biofilms. However, this practice sometimes suffers from undesirable impacts on flavour, nutritional composition, and texture of treated foods.² Various non-thermal processing technologies such as ultraviolet light, irradiation, ultrasound, ozonation, cold plasma, pulsed electric field, and high hydrostatic pressure have been introduced to the food industry to reduce the microbial load while retaining the natural colour, flavour and nutrition. Nevertheless, the wide application of some of these non-thermal decontamination technologies is limited by strict processing conditions, expensive equipment, high energy consumption, and the emergence of microbial resistance.³

One of the recently introduced non-thermal decontamination technologies to the food industry is photodynamic treatment, which is also known as photosensitisation. For several decades, photodynamic treatment has been investigated and used for medical and dental purposes to treat tumour/cancerous cells and as antibacterial/antibiofilm treatment. Reactive oxygen species (ROS) are produced during the photodynamic treatment, which only requires the presence of oxygen, a photosensitiser, and light (at photosensitiser’s λ_max). Photosensitisers become excited on illumination and generate cytotoxic ROS through subsequent de-excitation and collision with the surrounding oxygen molecules⁴ (Fig. 1). The produced ROS exhibit a multi-target attack towards different intracellular components of microorganisms present in the food, such as their proteins, lipids, and nucleic acids, resulting in cellular death. Therefore, because of direct and non-selective oxidative damage to essential biomolecules required for cell integrity and function, there is also a low probability of the emergence of microbial resistance using photodynamic treatment.⁵ Another advantage of this treatment is being chemical free that is in line with the growing demand for ‘clean label’ food products.

Fig. 1.  A schematic overview of the photodynamic process.⁶

Generally, photosensitisers can be endogenous such as porphyrins, which already exist within some fungal and bacterial cells, or exogenous such as curcumin, chlorophyll, and riboflavin isolated from plant material (Fig. 2). However, the poor water solubility of some potent photosensitisers such as curcumin can limit the wide application of the treatment on different food products. This can be overcome with the aid of encapsulation technology using hydrocolloids isolated from natural resources. This results in better bonding of the photosensitiser with microbial cells and better accumulation in the vicinity of target cells and therefore an enhanced photodynamic antimicrobial effect. Furthermore, another feature of this photodynamic treatment is its low energy requirement and no toxic by-products or residue generation,⁵ thus making it a safe and eco-compatible technology.

Fig. 2.  Examples of natural photosensitisers: (a) riboflavin, (b) chlorophyllin A, (c) hypericin, (d) curcumin, (e) aloe-emodin.⁷

In 2004, Lukšien and colleagues explored the application of innovative and promising photodynamic inactivation for microbial food safety. The authors reported a complete in vitro photoinactivation of common food crop spoilage fungi, namely Rhizopus oryzae, Aspergillus flavus, Trichothecium roseum, and Fusarium avenaceum, using hematoporphyrin dimethyl ether as a photosensitiser.⁸ Further studies have since shown the efficiency of photodynamic treatment in inactivating a wide variety of food spoilage and pathogenic microorganisms (i.e. vegetative cells, spores, biofilms) such as Listeria monocytogenes, Salmonella enterica,⁹ Vibrio parahaemolyticus,¹⁰ Enterococcus faecalis,¹¹ Pseudomonas fluorescens, Shigella flexneri,¹² Staphylococcus aureus,¹³ Bacillus cereus,¹⁴ Candida albicans, Aspergillus niger, Penicillium griseofulvum, Fusarium oxysporum, Zygosaccharomyces bailii,¹⁵ Aspergillus flavus,¹⁶ and Botrytis cinerea.¹⁷

Several studies have shown that photodynamic treatment has the potential to be applied on a variety of food products including fruits and vegetables, seeds and grains, meat and aquatic products, and juices. This also has the advantage of minimal influence on nutritional and sensorial properties compared to conventional thermal processing technologies. A few examples of decontamination efficiency of photodynamic treatment of various food matrices include reducing the population of V. parahaemolyticus on cooked oysters,¹⁸ of L. monocytogenes on smoked salmon¹⁹ and on fresh-cut pears,²⁰ of E. coli on fresh-cut pineapple,²¹ of Staph. saprophyticus on fresh dough sheet,²² of P. fluorescens on Minas Frescal cheese,²³ of A. flavus on maize kernel and flour²⁴ and on peanuts,²⁵ and of Botrytis cinerea on apples.²⁶ The use of photodynamic treatment in disinfecting the water in fish farming was also suggested by Wohllebe and colleagues. The authors successfully decontaminated the water containing larvae (of human pathogenic parasites) using low concentrations of chlorophyll acid²⁷ before introducing the fish. They further suggested chlorophyll-mediated photodynamic treatment as a practical and inexpensive treatment for controlling ectoparasites such as Ichthyophthirius mulftifiliis in fish.²⁸

Furthermore, encouraged by promising antimicrobial efficacy of this treatment, photodynamic-mediated food packaging films have been recently investigated. The photosensitiser is embedded in the film forming matrix to add the antimicrobial activity to the food packaging material. Examples of photodynamically active food packaging are riboflavin-incorporated chitosan-based film as a salmon packaging material, with the ability to reduce L. monocytogenes, V. parahaemolyticus and Shewanella baltica populations,²⁹ carbon nitride-incorporated konjac glucomannan-based film as a cherry tomato packaging material with the ability to inhibit E. coli and Staph. aureus growth,³⁰ curcumin-incorporated cellulose laurate-based film as a pork packaging material with the ability to reduce Staph. aureus population,³¹ β-cyclodextrin/curcumin complex-incorporated 2,3-dialdehyde cellulose-based film as a salmon packaging material with the ability to inactivate L. monocytogenes, V. parahaemolyticus, and Shew. putrefaciens,³² and aloe emodin-incorporated poly(3-hydroxybutyrate-co-3-hydroxyvalerate)-based film as a packaging material for fresh-cut papaya, pork belly and pork bologna with the ability to inactivate E. coli.³³ It is also possible that the photosensitiser-incorporated food packaging material may improve the shelf life of the products by being exposed to artificial lighting in the retail stores. However, this needs further investigation.

In general, various studies have shown the efficiency of photodynamic treatment as a naturally based, cost effective, clean label and eco-friendly decontamination technique. The key benefit of this technology is that it is a non-thermal process and retains the nutritional and organoleptic qualities of food. It is easily scalable and can be implemented in the food industry as it can operate using an existing conveyor system. It does not require expensive equipment and the materials used such as curcumin and visible light are already approved and being used in the food industry. It is effective against a wide range of food related microorganisms including viruses, bacteria, yeasts, and moulds.

Besides the diverse applications of photodynamic treatment in post-harvest and processed foods from plant or animal sources it has applications in decontamination of fruit and vegetable washing water, making it attractive for adoption by industry. It can also be investigated as an antibacterial, antifungal, and possibly pesticide treatment for the photosensitiser to be applied directly on fresh produce and be photoactivated with the aid of artificial lighting for example in greenhouses, where the intensity of light and time of exposure can be controlled. However, the efficiency of the treatment is dependent on the processing conditions such as photosensitiser concentration, light dose, and wavelength, as well as the food matrix properties. Optimising and validating the treatment conditions, including photosensitiser formulation and illumination dosage, are the future challenges to effectively implementing the treatment in the food industry to replace the conventional decontamination techniques, while maintaining similar or higher decontamination efficiency.

Data sharing is not applicable as no new data were generated or analysed during this study.

The authors declare no conflicts of interest.

This research did not receive any specific funding.