Spray-drying microencapsulation of synergistic antioxidant mushroom extracts and their use as functional food ingredients
Introduction
Mushrooms are widely appreciated all over the world for their nutritional properties (Kalač, 2009). They have a low fat content but are rich in water, minerals, proteins, fibres and carbohydrates (Heleno et al., 2012, Kalač, 2009, Reis et al., 2012, Reis et al., 2011). Besides their nutritional value, it has been demonstrated that mushrooms have health promoting benefits (Palacios et al., 2011). They are effective as anti-inflammatory (Ma, Chen, Dong, & Lu, 2013), antitumor (Heleno et al., 2014), antibacterial (Alves et al., 2012) and antioxidant agents (Reis et al., 2011), extending their potential use as functional foods and applications in the biomedical field.
During natural cellular metabolism, reactive oxygen (ROS), nitrogen (RNS) and sulphur (RSS) species are produced (Carocho & Ferreira, 2013), ROS being the most abundant (Ferreira, Barros, & Abreu, 2009). When high concentrations of these species are present, an oxidative stress is generated. If in excess, ROS may oxidise and damage cellular lipids, proteins and DNA, leading to their modification and inhibition of normal functions (Ferreira et al., 2009). Given this scenario, the organism develops defence mechanisms such as endogenous defences, including enzymatic reactions such as the production of superoxide dismutase (SOD), catalase (CAT), glutathione peroxidase (GSH-Px) and glutathione reductase; or non-enzymatic reactions, resulting in species such as glutathione (GSH), α-tocopherol (vitamin E), ascorbic acid (vitamin C) and lipoic acid (Carocho and Ferreira, 2013, Ferreira et al., 2009). Both mechanisms are able to provide cells protection against excessive levels of free radicals (Carocho & Ferreira, 2013).
The exogenous antioxidant defence promoters can be ingested as part of the daily diet to help fight against high ROS contents. Therefore, mushrooms can play an important role since they contain diverse phenolic compounds, known to be excellent antioxidants due to their capacity for capturing free radicals by electron transferring, and to the excellent redox properties of the phenolic hydroxyls groups (Ferreira et al., 2009).
Apart from their instability at high temperatures, and in the presence of oxygen and light, some mushroom extracts are characterised by a strong odour and flavour. One way to ensure their viability as functional food ingredients is to proceed with their microencapsulation, providing protection against oxidation and masking their odour and flavour (Ersus and Yurdagel, 2007, Fang and Bhandari, 2010). Despite the numerous available microencapsulation possibilities, spray-drying is still one of the most widely used processes to encapsulate food ingredients (Fang & Bhandari, 2010). Among the main advantages of this technique are its easy industrialisation and the possibility of continuous production. Nevertheless, prolonged contact with high temperatures can compromise the bioactive properties of the mushroom extracts, and should be avoided.
Among several possibilities, maltodextrin (MD), a hydrolysed starch, offers advantages as a microencapsulation material (Gharsallaoui, Roudaut, Chambin, Voilley, & Saurel, 2007). It is a low cost material with a neutral aroma and flavour, high water solubility and low viscosity at high solids content, being able to provide effective protection against oxidation (Ersus and Yurdagel, 2007, Saéns et al., 2009).
Microencapsulation can be applied to protect bioactive natural extracts and some examples calling up this thematic can be found in literature (Dias, Ferreira, & Barreiro, 2015). Nevertheless, these studies are mainly related to the development of the microencapsulation process and do not proceed with the implementation of a final application as a functional food. (Ersus and Yurdagel, 2007, Kha et al., 2010, Saéns et al., 2009, Silva et al., 2013, Wu et al., 2014). In fact, and according to the current research, the examples dealing with the full process development are scarcer. In this context, Çam, Içyer, and Erdoğna (2014) tested the incorporation of microencapsulated Punica granatum L., an extract from pomegranate, in ice creams, and Martins et al. (2014) studied the incorporation of Rubus ulmifolius Schoot (Rosaceae), a species of wild blackberry, microencapsulated in alginate microparticles in yogurt. The obtained results, rather preliminary, are encouraging interest in the development of foods enriched with natural extracts that are often referred as health promoters (Ramalingum & Mahomoodally, 2014).
In this work, extracts of two mushroom species, Suillus luteus (L.: Fries) and Cooprinopsis atramentaria (Bull.) were investigated for their synergistic antioxidant effects and a promising combination of both (in similar proportions) was chosen to be microencapsulated by spray-drying using maltodextrin as the encapsulating material. The obtained powders were characterised by Scanning Electron Microscopy (SEM) (to inspect morphology and particle size) and for their antioxidant activity (free radicals scavenging activity and reducing power). Encapsulation yield and efficiency were also estimated. As a final step in this work, the produced microspheres were incorporated into cottage cheese samples and their antioxidant activity, nutritional value and colour were determined and compared with the counterparts, using extracts in the free form and a control (sample with no added extracts).
Section snippets
Standards and reagents
For antioxidant tests, 2,2-dipheny-1-picrylhydrazyl (DPPH) was obtained from Alfa Aesar (Ward Hill, MA, USA). For chromatographic analysis, HPLC-grade acetonitrile was purchased from Fisher Scientific (Lisbon, Portugal). The standards, such as fatty acids methyl ester (FAME) reference standard mixture 37 (standard 47885-U), β-carotene (98%) and trolox (6-hydroxy-2,5,7,8-tetramethylchroman-2-carboxylic acid), were purchased from Sigma (St. Louis, MO, USA), along with formic acid. Maltodextrin
Synergistic effects between mushroom extracts
The results of the antioxidant activity (measured by the DPPH radical scavenging activity, reducing power and inhibition of β-carotene bleaching assays) of the free extracts, S. luteus (Sl) and C. atramentaria (Ca), and of the prepared mixtures (Sl:Ca 1:2, 1:1 and 2:1, w/w) are shown in Table 1. Comparing the two individualised mushrooms extracts, the lower EC50 values were obtained for Sl extracts, indicating that this mushroom has a higher antioxidant activity than Ca. This tendency was also
Conclusions
In this work, the antioxidant activity of Sl and Ca extracts was evaluated and it was observed that their combination results in synergistic effects. The spray-drying of the extracts using an extract/maltodextrin ratio of 1/20 and an inlet temperature of 170 °C resulted in good encapsulation yield (around 50%) and efficiency (43.5–62.6%.).
The microencapsulated extracts with maltodextrin did not lose antioxidant activity, and the combination Sl:Ca (1:1) was shown to be the best as it revealed
Competing interests
The authors declare no competing financial interest.
Acknowledgement
Financial support was provided by FCT/MEC and FEDER under Programme PT2020 (LSRE: Project UID/EQU/50020/2013and CIMO: PEst-OE/AGR/UI0690/2014) and QREN, ON2 and FEDER (Project NORTE-07-0162-FEDER-000050 and NORTE-07-0124-FEDER-000014). G. Ruphuy thanks Universidad de Costa Rica (UCR) and Ministerio de Ciencia, Tecnología y Telecomunicaciones de Costa Rica (MICITT) for her scholarship and L. Barros FCT for her contract (Compromisso para a Ciência 2008). A special thanks to Cargill for having
References (24)
- et al.
Foeniculum vulgare Mill. As natural conservation enhacer and health promoter by incorporation in cottage cheese
Journal of Functional Foods
(2015) - et al.
Pomegranate peel phenolics: Microencapsulation, storage stability and potential ingredient for functional food development
LWT-Food Science and Technology
(2014) - et al.
A review on antioxidants, prooxidants and related controversy: natural and synthetic compounds, screening and analysis methodologies and future perspectives
Food and Chemical Toxicology
(2013) - et al.
Microencapsulation of anthocyanin pigments of black carrot (Daucuscorota L.) by spray drier
Journal of Food Engineering
(2007) - et al.
Encapsulation of polyphenols – a review
Food Science & Technology
(2010) - et al.
Applications of spray-drying in microencapsulation of food ingredients: An overview
Food Research International
(2007) - et al.
Cytotoxicity of coprinopsis atramentaria extract, organic acids and their synthesized methylated and glucuronate derivatives
Food Research International
(2014) Chemical composition and nutritional value of European species of wild growing mushrooms: A review
Food Chemistry
(2009)- et al.
Effects of spray drying conditions on the physicochemical and antioxidant properties of the Gac (Momordica cochinchinensis) fruit aril powder
Journal of Food Engineering
(2010) - et al.
Anti-inflammatory and anticancer activities of extracts and compounds from the mushroom Inonotus obliquus
Food Chemistry
(2013)
Antioxidant properties of phenolic compounds occurring in edible mushrooms
Food Chemistry
Chemical composition and nutritional value of the most widely appreciated cultivated mushrooms: an inter-species comparative study
Food and Chemical Toxicology
Cited by (56)
Design of functional foods with targeted health functionality and nutrition by using microencapsulation technologies
2022, Food Structure Engineering and Design for Improved Nutrition, Health and Well-beingUmami Ingredient: Flavor enhancer from shiitake (Lentinula edodes) byproducts
2020, Food Research InternationalCitation Excerpt :HD extract spray drying, using maltodextrin as a carrier agent, provided a yield of 60 ± 0.03%, which is considered good for the scale used (laboratory). This result was superior to that reported by Francisco et al. (2018) and Ribeiro et al. (2015) for mushroom extract spray drying. Yield is affected by the amount of material deposited on the wall of the equipment, droplets and powder can stick on the walls and cyclone, reducing the amount of product collected at the end of the process (Wang & Langrish, 2009).
Bioactive compounds profile, enzyme inhibitory and antioxidant activities of water extracts from five selected medicinal plants
2020, Industrial Crops and ProductsRecovery and partial purification of fibrinolytic protease from Pleurotus ostreatus and P. eryngii and cytotoxic and antioxidant activity of their extracts
2024, Preparative Biochemistry and BiotechnologyMushroom β-glucans: application and innovation for food industry and immunotherapy
2023, Applied Microbiology and Biotechnology