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Edible flowers. Benefits and risks pertaining to their consumption
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Commentary
Edible flowers. Benefits and risks pertaining to their consumption Ewa Matyjaszczyka,∗, Maria Śmiechowskab a b
Institute of Plant Protection, National Research Institute, ul Władysława Węgorka 20; 60-318, Poznań, Poland Gdynia Maritime University, ul. Morska 81-87, 81-225, Gdynia, Poland
ARTICLE INFO
ABSTRACT
Keywords: Edible flowers Benefits Risk Hazard Food safety Impurities
Background: Recently, a new trend as well as fashion has been observed of fresh flowers consumption. Edible flowers are served in fashionable restaurants and are popular topic of different magazine articles making an excellent illustration opportunity. However, contrary to the common belief that whatever natural is safe, flowers may pose risk to consumers. Scope and approach: The paper presents consumer attitudes towards edible flowers, explaining what characteristics attract consumers towards them. The beneficial compounds most commonly occurring in edible flowers are described as well as impurities external to the flower-bearing plant. Key findings and conclusion: The benefits of edible flowers consumption are nutritional and bioactive properties. The hazardous compounds may come from the plant or from the different levels of food chain. The two most important groups of external impurities occurring in edible flowers are bacteria and chemical compounds. Hazardous bacteria may come both from agricultural production and the food chain, while the sources of chemical impurities are mostly agricultural production and the environment. Relevant safety requirements and guidelines are scarce.
1. Introduction
1.1. Consumer attitudes and behaviour towards edible flowers
Herb flowers have been used in phytotherapy for centuries. Fresh flowers from the earliest times were used primarily to decorate and aromatise the rooms. Recently, a new trend has been observed consisting in the widespread use of mainly fresh flowers for consumption. The main task of plants in nature is to grow fruits and seeds. Flowers may therefore contain repellents or poisonous substances produced by the plant to prevent their loss (Dusemund, Rietjens, Cartus, Schaefer, & Lampen, 2017; Egebjerg et al., 2018; Pinela, Carvalho, & Ferreira, 2017). It is worth noting that not all flowers used in herbal medicine are edible. Some of them contain substances that act very strongly on the human body and can be poisonous (Akinmoladun, Olaleye, & Farombi, 2014; Kristanc & Kreft, 2016). The present paper attempts a narrative review of scientific articles about edible flowers and highlights the benefits and risks associated with their consumption. We focus on edible flowers, i.e., those which consumption is safe for people. Therefore the plant toxins naturally present in flowers are not discussed here. Only hazards, external to the flower-producing plant, are presented.
The interest in edible flowers is the result of the search for new, natural food products. Consumers are increasingly choosing food products containing natural ingredients due to concerns about the adverse health effects of synthetic compounds. Edible flowers (Table 1) bring interesting elements to culinary and dietary habits. Flowers can be used in various forms and shapes. Edible flowers are usually fresh. If treated, the treatment should not cause their destruction. The recent research show that to prolong the shelf life of edible flowers both high hydrostatic pressure technology and food irradiation technology may be used. Satisfactory results were also obtained by applying freeze drying, which has the advantage of being non-destructive towards bioactive compounds present in edible flowers. The use of osmotic dehydration and application of edible protective coatings are also currently tested (Fernandes, Saraiva, Pereira, Casal, & Ramalhosa, 2019). Consumers perceive flowers by their attractive appearance, size, shape, taste, smell and colour. From the studies of Kelly, Behe, Biernbaum, and Poff (2001a) it appears that consumers prefer yellow, orange and blue flowers. Benvenuti et al. (2016) conducted sensory evaluation studies of flowers. Consumers assessed features such as
∗
Corresponding author. E-mail addresses: [email protected] (E. Matyjaszczyk), [email protected] (M. Śmiechowska).
https://doi.org/10.1016/j.tifs.2019.07.017 Received 4 March 2019; Received in revised form 9 July 2019; Accepted 19 July 2019 0924-2244/ © 2019 Published by Elsevier Ltd.
Please cite this article as: Ewa Matyjaszczyk and Maria Śmiechowska, Trends in Food Science & Technology, https://doi.org/10.1016/j.tifs.2019.07.017
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Table 1 Flowers most often used as food and their applications. Source: Own elaboration based on: Kalemba-Drożdż (2016): Kwiaty jadalne [Edible flowers]; Mlcek and Rop (2011): Fresh edible flowers of ornamental plants - A new source of nutraceutical foods; Benvenuti, Bortolotti, and Maggini (2016): Antioxidant power, anthocyanin content and organoleptic performance of edible flowers. Flower plants Black elder Pansy Cornflower Chrysanthemum Zucchini Chicory Pumpkin Sweet violet Phlox Forsythia Freesia Fuchsia Hawthorn Hibiscus Dead-nettle Jasmine Coneflower Clover Lavender Common poppy Hollyhock Common marigold Nasturtium Impatiens Forget-me-not Starflower Petunia Primrose Peony Rose Chamomile Sunflower Daisy Orchid Strawberry Evening primrose Cherry Heather
Application in nutrition Sambucus nigra L. Viola tricolor L. Centaurea cyanus L. Dendranthema spp (Chrysanthemum spp.) Cucurbita pepo convar giromontiina Greb. Cichorium intybus L. Cucurbita pepo L. Viola odorata L. Phlox L. Forsythia Vah Freesia Eckl. ex Klatt Fuchsia L. Crataegus L. Hibiscus L. Lamium L. Jasminum L. Echinacea Moench Trifolium L. Lavandula L. Papaver rhoeas L. Alcea L. Calendula off. L. Tropaeolum L. Impatiens L Myosotis L. Borago off. L. Petunia Juss. Primula L. Paeonia L. Rosa L. Matricaria L. Helianthus L. Bellis L. Orchis L. Fragaria L. Oenothera L. Cerasus Mill. Calluna vulgaris L
Decoration Decoration Decoration Decoration
of of of of
dishes, desserts, salads, juices, drinks dishes and desserts, salads dishes and desserts dishes and desserts
Dishes, pancakes, crisps Dishes, desserts, salads Dishes, pancakes, crisps Decoration of dishes and desserts, ice cream and drinks Decoration of dishes and desserts, ice cream and drinks Decoration of dishes and salads, drinks Decoration of dishes and desserts, ice cream and drinks Decoration of desserts, ice cream and drinks Decoration of dishes and desserts, ice cream, juices Decoration of dishes, desserts and drinks Decoration of cakes, desserts, ice cream and drinks Decoration of dishes, herbal teas Decoration of dishes, cake additive, salads Decoration of dishes and desserts, ice cream and drinks Decoration of dishes and desserts, ice cream and drinks Decoration of dishes and desserts, herbal teas Decoration of dishes and desserts, salads, juice Decoration of dishes, salads Decoration of dishes and desserts, salads Decoration of dishes, salads Decoration of dishes, salads Decoration of dishes, salads Decoration of dishes and desserts, salads Decoration of dishes and desserts, drinks Decoration of dishes and desserts, ice cream, drinks, juices Decoration of dishes and desserts, drinks, juices Decoration of dishes, salads, herbal teas Decoration of dishes, salads Decoration of dishes, desserts, salads Decoration of dishes and desserts, ice cream Decoration of dishes and desserts, salads, herbal teas Decoration of dishes and desserts, ice cream Decoration of dishes and desserts, ice cream, drinks Decoration of dishes and desserts, drinks
spices, sweetness, smell, softness and bitterness. The consumers decidedly preferred A. houstorianum, B. semperflorens, V. vittrockiana i T. majus due to their tastiness. Results of the study of Kelly, Behe, Biernbaum, and Poff (2001b) performed in USA show that consumers rate edible flowers attributes such as taste, texture and appearance highly. Nationality has an influence on the behaviour and attitudes of consumers towards edible flowers. Research conducted in Taiwan by Chen and Wei (2017) showed that consumers there indicate that curiosity, aroma and health properties have the greatest impact on the attitude towards edible flowers. The aroma also indirectly affects the attitude to the consumption of edible flowers through specific perceptual curiosity. Zimowski (2014) indicates that aroma is one of the most important features of edible flowers. Odour is often a distinctive feature for a given species of flowers (Kaneko et al., 2017). Even varieties of the same species differ in the olfactory bouquet. An example may be rose flowers, which for many varieties smell faintly or do not smell at all, and among those that smell, there are noticeable differences in the type of smell. In many cases, modern varieties of many garden plants, once valued for their scent, today smell less intense. The reason for this seems to be the directional breeding selection, which at the expense of the smell led to obtaining plants with larger, more impressive and durable flowers.
According to the study conducted in Brazil, consumers treat edible flowers as “unknown foods” (Rodrigues et al., 2017). In the study, consumers were asked to express their opinion on foods with edible flowers and the natural yoghurt with flowers was presented for evaluation. The results showed a very positive attitude to both situations, and consumers associated food products containing flowers with “health benefits”, while yoghurt with flowers was considered an innovative product. Flowers were perceived as a surprising and unexpected addition to yoghurt. 1.2. Edible flowers as a source of bioactive substances The introduction of flowers for consumption triggered questions about the value of edible flowers. Apart from adding fresh and exotic aroma, delicate taste and attractive appearance, do they also provide health benefits for the consumer? The answer to this question are the results of research on the composition of active substances isolated from edible flowers. These studies showed the richness of bioactive compounds contained in flowers. Polyphenols and their antioxidant properties are among the most frequently tested compounds. Pires et al. (2018) defined phenol profiles in flower extracts (Dahlia mignon, Rosa damascena, Calendula officinalis L. and Centaurea cyanus L.) and assessed their bioactive potential, including antioxidant, antiproliferative and antibacterial abilities. The highest concentration of 2
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detected. The yellow oranges contained more carotenoids, while the red oranges contained more anthocyanins. The correlation between the content of violaxanthin, zeta-carotene and lutein and the index of yellow colour intensity was proved. In addition to the above mentioned bioactive compounds, edible flowers also contain vitamins and minerals. Vitamins A, C and E were detected in flower petals (Mlcek, Rop 2011). The relatively high content of vitamin C was determined in flower petals of nasturtium, rose and hibiscus (Garzón & Wrolstad, 2009; Özcan 2002). In turn, tocopherols were identified in petals of Rosa canina L., Dahlia mignon, Calendula officinalis L. and Centaurea cyanus L. (Pires, Dias, Barros, & Ferreira, 2017). There are very few studies on the content of mineral compounds in edible flowers. In tests carried out in Brazil, the content of As, Ca, Cd, Co, Cr, Cu, Fe, Mg, Mn, Mo, Na, Ni, P and Zn in rose petals Rosa spp. was determined (dos Santos et al., 2018).
Table 2 Impurities in edible flowers registered in the European Union rapid alert system for food and feed (RASFF) in the years 2004–2018. Flower
Country of origin
Food safety issue
Year
Cornflower blossoms Magosa flower (Azadirachta indica) Chamomile flower Tilia flowers Tilia tomentosa flowers Hibiscus flowers
Albania Thailand
Salmonella Salmonella Stanley
2018 2017
Egypt Bulgaria Albania Egypt
Rat droppings N,N-diethyl-meta-toluamide Dimethoate Infested with insects and moulds, rodent excrements
2016 2015 2014 2008
Sulphite unauthorised
2005
Salmonella Mbandaka Salmonella Hadar
2005 2004
Cinnamon and Sri Lanka cinnamon tree flowers (Cinnamomum verum) Fresh edible flower Thailand Dried marigold Egypt flowers/ Calendula officinalis
1.3. Safety issues of edible flowers’ consumption As stressed earlier, some flowers may contain harmful compounds produced by the plant. In this chapter, however, safety is discussed in the context of external impurities only. Safety issues regarding edible flowers have been already registered in the European Union Rapid Alert System for Food and Feed (RASFF), see Table 2. The main problems are related to the presence of bacteria (Salmonella spp.) or chemical compounds like dimethoate (insecticide), diethyl-meta-toluamide (insect repellent) and sulfites. RASFF data prove that due attention should be paid to the suitable growing, preservation, transport and storage of edible flowers. There is also the need to create awareness regarding the safety of this group of food products among actors on different levels of production chain, as well as the consumers. The microbiological impurities of edible flowers noted so far in RASFF are all related to the presence of different serotypes of Salmonella (see Table 2). Different types of growing as well as harvesting and processing conditions can open the way for bacteria to get onto and into the plant material, including flowers. It may happen before harvest, but it is more likely to happen afterwards (Erickson, 2012; Hirneisen, Sharma, & Knie, 2012). The plants on the field or in the glasshouse may be contaminated through soil, fertilizers or irrigation, especially if watered with surface water (Fornefeld et al., 2017). After the harvest, the contamination can occur through numerous routes during food processing, transport, distribution and preparation. For example, by water and ice used to wash, chill or pack, by contaminated surfaces used for food processing, by food workers not observing the proper hygienic measures, etc. (CDC How Food Gets Contaminated; EFSA, 2018 Zoonotic diseases). The microbial impurities are of concern as edible flowers are mostly consumed fresh and often served in combination with foods such as salads, desserts and cakes, that may constitute a good growth medium for bacteria. Considering data regarding vegetables (de Oliveira, Decol, & Tondo, 2018; Liu et al., 2017) it is not unlikely that some edible flowers may be able to support growth of pathogenic bacteria (including Salmonella) and consequently allow an increase in their concentration during the supply phases. In addition some dishes decorated with edible flowers most certainly are able to support growth of pathogenic bacteria. Considering their use and application edible flowers may be therefore a matter of concern for cross-contamination. The majority of edible flowers are used for decoration. In line with that, there is a possibility they are not consumed at all, and become leftovers. However in case of cross-contamination this does not eliminate the microbial risk. On the other hand, as far as chemical impurities are concerned, the risk related to edible flowers consumption may differ significantly depending on consumer behaviour. What are the possible reasons for the presence of chemical compounds in edible flowers? At least part of them are pesticide residues coming from agricultural production. On different stages of their
phenolic compounds was found in marigolds. Extracts and infusions of rose petals showed the highest antioxidant activity, which may have resulted from the presence of quercetin and kaempferol derivatives. Many publications concern the results of research on the composition and health benefits of different rose varieties. Rose oil in many parts of the world, such as Bulgaria, Turkey, India and Iran, is used to obtain essential oil, rose water, syrup, liqueur and other products. The most important properties of rose oil include diuretic, sedative, anti-migraine, antiseptic and antibacterial effects (Schmitzer, MikulicPetkovsek, & Stampar, 2019). Research conducted by Lia et al. (2014) on the total phenolic content and antioxidative abilities of 51 edible and wild flowers showed that the wrinkled rose (Rosa rugosa Thunb.), wavyleaf sea-lavender (Limonium sinuatum L.), sweet osmanthus (Osmanthus fragrans), stripped pelargonium (Pelargonium hortorum L.) and spicy jatropha (Jatropha integerrima Jacq.) are characterized by the highest content of homogentisic acid, cyanidin-3-glucoside, protocatechuic acid, catechin, gallic acid and epicatechin. In other studies, it was shown that out of the 23 studied Chinese flowers Osmanthus fragrans (Thunb.) Lour, Paeonia lactiflora Pall and Rosa rugosa Thunb (violet) were characterized by the strongest antioxidant activity before or after in vitro digestion, suggesting that these flowers are important natural sources in the prevention of oxidative stress diseases (Chen et al., 2015). Most researchers emphasize that edible flowers are characterized by a high content of antioxidative polyphenols. Research conducted by Chen, Chen, Xiao, and Fu (2018) showed that the wrinkled rose (Rosa rugosa Thunb.), wavyleaf sea-lavender (Limonium sinuatum L.), Chinese quince (Chaenomeles sinensis (Thouin) Koehne), sweet osmanthus (Osmanthus fragrans), giant crepe-myrtle (Lagetstroemia speciose L.) and rosemary (Rosmarinus officinalis L.) showed the strongest antioxidant activity among the 30 tested flowers and these flowers contained the highest total phenols (TPC) and total flavonoids (TFC). Researchers suggest that flower extracts can be used as functional foods in the prevention of chronic diseases. Colour plays a very important role in food and nutrition and is an important organoleptic property of edible flowers (Śmiechowska & Dmowski, 2014, pp. 343–359). The colour of flowers primarily depends on the content of carotenoids and anthocyanins. In edible flowers, the increased content of anthocyanins is mostly positively correlated with higher levels of total flavonoids (Friedman et al., 2010). No research on the dependence of the colour of flowers on the content of bioactive substances has been conducted thus far. However, in the study of carotenoids content in fruits (Ben Abdelaali et al., 2018) a significant dependence of the colour on the content of bioactive compounds was 3
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development, plants are endangered by various harmful organisms. If chemical products are used to control insects, weeds and fungi then pesticide residues are detected in the final product. Detection of pesticide residues is a natural consequence of making use of them. Therefore, pesticide residues are regularly monitored in crops and in food (Mojsak, Kaczyński, & Łozowicka, 2018; Rutkowska, Łozowicka, & Kaczyński, 2018). If pesticide residues are detected within legal limits, it means if their amounts do not exceed maximum residue levels (MRL), the food is safe. Such result would be of course not reported in RASFF. In case of edible flowers it is, however, not unlikely that if the pesticides are used to protect plants, the residues may exceed MRL. There are two different reasons for that, depending if the flowers come from ornamental plants or from plants that are produced for food. In case of most plants produced for food, the agricultural production process is not focused on the flower to be eaten. The development of flower into the fruit or seed takes some time. Within that time plant protection product applied prior to flowering have chance to decompose. The timing of application recommended in the label of plan protection product takes this gap into account. If the flower is harvested, that gives less time for any chemical protection products used in the agricultural production process to decompose. Logically, it means that residues of pesticides in the flowers may be higher than permitted. There are of course some plants like cauliflower or broccoli where flower is the main edible plant part and in their case this safety issue is not relevant. However, cauliflower and broccoli are usually counted among vegetables, and despite being flowers are rarely referred to as “edible flowers”. Sometimes edible flowers come from plants that are typically grown for ornamental purposes. Orchids or chrysanthemums may serve as an example here. Ornamental plants are produced for their beauty and are usually grown with great care to avoid any pest damages. In case of ornamental plants even the slightest visible damage of leaves or flowers may mean that the crop has no market value. Therefore, there are fertilisation programmes and available pesticides to ensure that they look beautiful. The products used in the process of agricultural production must be applied in the way safe for the workers, for soil and for non-target species (for example bees) (Matyjaszczyk, 2017). However, normally MRLs are not an issue in ornamental plants as those plants are not intended for human consumption. It may happen, that even if ornamental plants are produced with due respect to all appropriate rules and chemical protection is applied following minutely the label, the flowers may still contain chemical substances of different kind in the amounts not suitable for food products. The efficient plant protection products consisting of natural compounds are not always available (Matyjaszczyk, 2018). Therefore, ornamental plants produced for yield of flowers to be consumed by humans should be grown separately from ornamental plants grown for ornamental purposes. They should be also fertilized and protected in the manner that the final product meets all safety criteria regarding human consumption. We can assume as much, just by applying logical approach. However, the devil is in the details. Namely, how those ornamental plants should be taken care of? What products should be used for their protection? In what doses? The recommendations on how to use plant protection products are given in the product label, which is approved by the responsible authority. However, only common recommendations following the intended use are available on the label. The ornamental plants as such are considered to be “minor crop” owing to the fact that due to the limited area they are not in the focus of the attention of agrochemical companies. The production of flowers of ornamental plants intended for human consumption is a margin of margin. No chemical company is interested in registration of such use and performing necessary laboratory tests. Consequently, the recommendations regarding the protection of edible flowers are as a rule not available. It is therefore not unlikely that in the absence of guidelines for edible flowers, farmers may follow the label recommendations regarding plants for ornamental use, thus exceeding
the safety limits. Some edible flowers come from wild plants, collected from wild stands. Contamination of flowers with similar but poisonous relatives growing in the neighbourhood is therefore not unlikely. In the case of wild plants, especially those that come from an area that is not in agricultural use, there may be a concern of chemical impurities absorbed from soil or from air. High concentration of heavy metals in soil is a recognised problem in certain areas (Superville et al., 2017). It is also known that heavy metals, for example cadmium, are absorbed by plants and safety concerns may arise after those plants are consumed by humans (Matyjaszczyk & Schumann, 2018). Another matter of concern are impurities in the air, among others those that come from automotive or from industrial pollution (Omasa, Tobe, & Kondo, 2002). Therefore, in case of edible flowers coming from wild plants the place of their harvest may influence the safety of their consumption. In terms of legal rules the problem of pesticide and heavy metal residues in edible flowers was recognised in some regions. For example in the European Union an MRL group “Herbs and edible flowers” (code number 0256000) with a sub-group “basil and edible flowers” (code number 0256080) is established and therefore unambiguous rules regarding maximum levels of pesticide and heavy metal residues in edible flowers are set. The risk for humans can be calculated as a function of hazard and exposure (EFSA, 2018). If hazard is defined as chemical impurities in edible flowers, in turn exposure can be calculated considering the data on the amount of pesticides or heavy metals and the edible flower consumption data. As consumption of flowers is rarely significant in terms of volume, the risk in most cases is not likely to be very high. Anyway, the risk is worth stressing, especially among frequent consumers. Source: Years 2015-2018 own search, earlier Fernandes, Casalb, Pereiraa, Saraivac, and Ramalhosaa (2017): Edible flowers: A review of the nutritional, antioxidant, antimicrobial properties and effects on human health. 2. Conclusions Edible flowers are gaining more and more popularity among the consumers, cooks and confectioners. They are appreciated for their sensory values, such as taste and aroma and evoke positive aesthetic impressions. Edible flowers also provide bioactive compounds in the form of polyphenols, vitamins and minerals. Each food product must, however, be primarily safe for the consumer and in the case of edible flowers there are no clear legal regulations such as a list of flowers allowed for consumption, growing conditions, harvest dates, storage conditions and substances authorized for use in the protection of edible flowers. The RASFF data show that microbial contamination and the presence of chemical residues make it necessary to pay special attention to the proper cultivation, preservation, transport and storage of edible flowers. It is also necessary to increase awareness of the safety of this group of food products among entities operating at different levels of the production chain, as well as consumers. References Akinmoladun, A. C., Olaleye, M. T., & Farombi, E. O. (2014). Cardiotoxicity and cardioprotective effects of african medicinal plants. In V. Kuete (Ed.). Toxicological survey of african medicinal plants., 2014Elsevier Inchttps://www.sciencedirect.com/book/ 9780128000182/toxicological-survey-of-african-medicinal-plants, Accessed date: 25 August 2018. Ben Abdelaali, S., Rodrigo, E., Saddoud, O., Zacarías, L., Rabeh, M., & Messaoud, M. (2018). Carotenoids and colour diversity of traditional and emerging Tunisian orange cultivars (Citrus sinensis (L.) Osbeck). Scientia Horticulturae, 227, 296–304. Benvenuti, S., Bortolotti, E., & Maggini, R. (2016). Antioxidant power, anthocyanin content and organoleptic performance of edible flowers. Scientia Horticulturae, 199, 170–177. CDC How Food Gets Contaminated The food production chain. https://www.cdc.gov/ foodsafety/production-chain.html, Accessed date: 18 December 2018. Chen, G.-L., Chen, S.-G., Xiao, Y., & Fu, N.-L. (2018). Antioxidant capacities and total
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Commentary
Edible flowers. Benefits and risks pertaining to their consumption Ewa Matyjaszczyka,∗, Maria Śmiechowskab a b
Institute of Plant Protection, National Research Institute, ul Władysława Węgorka 20; 60-318, Poznań, Poland Gdynia Maritime University, ul. Morska 81-87, 81-225, Gdynia, Poland
ARTICLE INFO
ABSTRACT
Keywords: Edible flowers Benefits Risk Hazard Food safety Impurities
Background: Recently, a new trend as well as fashion has been observed of fresh flowers consumption. Edible flowers are served in fashionable restaurants and are popular topic of different magazine articles making an excellent illustration opportunity. However, contrary to the common belief that whatever natural is safe, flowers may pose risk to consumers. Scope and approach: The paper presents consumer attitudes towards edible flowers, explaining what characteristics attract consumers towards them. The beneficial compounds most commonly occurring in edible flowers are described as well as impurities external to the flower-bearing plant. Key findings and conclusion: The benefits of edible flowers consumption are nutritional and bioactive properties. The hazardous compounds may come from the plant or from the different levels of food chain. The two most important groups of external impurities occurring in edible flowers are bacteria and chemical compounds. Hazardous bacteria may come both from agricultural production and the food chain, while the sources of chemical impurities are mostly agricultural production and the environment. Relevant safety requirements and guidelines are scarce.
1. Introduction
1.1. Consumer attitudes and behaviour towards edible flowers
Herb flowers have been used in phytotherapy for centuries. Fresh flowers from the earliest times were used primarily to decorate and aromatise the rooms. Recently, a new trend has been observed consisting in the widespread use of mainly fresh flowers for consumption. The main task of plants in nature is to grow fruits and seeds. Flowers may therefore contain repellents or poisonous substances produced by the plant to prevent their loss (Dusemund, Rietjens, Cartus, Schaefer, & Lampen, 2017; Egebjerg et al., 2018; Pinela, Carvalho, & Ferreira, 2017). It is worth noting that not all flowers used in herbal medicine are edible. Some of them contain substances that act very strongly on the human body and can be poisonous (Akinmoladun, Olaleye, & Farombi, 2014; Kristanc & Kreft, 2016). The present paper attempts a narrative review of scientific articles about edible flowers and highlights the benefits and risks associated with their consumption. We focus on edible flowers, i.e., those which consumption is safe for people. Therefore the plant toxins naturally present in flowers are not discussed here. Only hazards, external to the flower-producing plant, are presented.
The interest in edible flowers is the result of the search for new, natural food products. Consumers are increasingly choosing food products containing natural ingredients due to concerns about the adverse health effects of synthetic compounds. Edible flowers (Table 1) bring interesting elements to culinary and dietary habits. Flowers can be used in various forms and shapes. Edible flowers are usually fresh. If treated, the treatment should not cause their destruction. The recent research show that to prolong the shelf life of edible flowers both high hydrostatic pressure technology and food irradiation technology may be used. Satisfactory results were also obtained by applying freeze drying, which has the advantage of being non-destructive towards bioactive compounds present in edible flowers. The use of osmotic dehydration and application of edible protective coatings are also currently tested (Fernandes, Saraiva, Pereira, Casal, & Ramalhosa, 2019). Consumers perceive flowers by their attractive appearance, size, shape, taste, smell and colour. From the studies of Kelly, Behe, Biernbaum, and Poff (2001a) it appears that consumers prefer yellow, orange and blue flowers. Benvenuti et al. (2016) conducted sensory evaluation studies of flowers. Consumers assessed features such as
∗
Corresponding author. E-mail addresses: [email protected] (E. Matyjaszczyk), [email protected] (M. Śmiechowska).
https://doi.org/10.1016/j.tifs.2019.07.017 Received 4 March 2019; Received in revised form 9 July 2019; Accepted 19 July 2019 0924-2244/ © 2019 Published by Elsevier Ltd.
Please cite this article as: Ewa Matyjaszczyk and Maria Śmiechowska, Trends in Food Science & Technology, https://doi.org/10.1016/j.tifs.2019.07.017
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Table 1 Flowers most often used as food and their applications. Source: Own elaboration based on: Kalemba-Drożdż (2016): Kwiaty jadalne [Edible flowers]; Mlcek and Rop (2011): Fresh edible flowers of ornamental plants - A new source of nutraceutical foods; Benvenuti, Bortolotti, and Maggini (2016): Antioxidant power, anthocyanin content and organoleptic performance of edible flowers. Flower plants Black elder Pansy Cornflower Chrysanthemum Zucchini Chicory Pumpkin Sweet violet Phlox Forsythia Freesia Fuchsia Hawthorn Hibiscus Dead-nettle Jasmine Coneflower Clover Lavender Common poppy Hollyhock Common marigold Nasturtium Impatiens Forget-me-not Starflower Petunia Primrose Peony Rose Chamomile Sunflower Daisy Orchid Strawberry Evening primrose Cherry Heather
Application in nutrition Sambucus nigra L. Viola tricolor L. Centaurea cyanus L. Dendranthema spp (Chrysanthemum spp.) Cucurbita pepo convar giromontiina Greb. Cichorium intybus L. Cucurbita pepo L. Viola odorata L. Phlox L. Forsythia Vah Freesia Eckl. ex Klatt Fuchsia L. Crataegus L. Hibiscus L. Lamium L. Jasminum L. Echinacea Moench Trifolium L. Lavandula L. Papaver rhoeas L. Alcea L. Calendula off. L. Tropaeolum L. Impatiens L Myosotis L. Borago off. L. Petunia Juss. Primula L. Paeonia L. Rosa L. Matricaria L. Helianthus L. Bellis L. Orchis L. Fragaria L. Oenothera L. Cerasus Mill. Calluna vulgaris L
Decoration Decoration Decoration Decoration
of of of of
dishes, desserts, salads, juices, drinks dishes and desserts, salads dishes and desserts dishes and desserts
Dishes, pancakes, crisps Dishes, desserts, salads Dishes, pancakes, crisps Decoration of dishes and desserts, ice cream and drinks Decoration of dishes and desserts, ice cream and drinks Decoration of dishes and salads, drinks Decoration of dishes and desserts, ice cream and drinks Decoration of desserts, ice cream and drinks Decoration of dishes and desserts, ice cream, juices Decoration of dishes, desserts and drinks Decoration of cakes, desserts, ice cream and drinks Decoration of dishes, herbal teas Decoration of dishes, cake additive, salads Decoration of dishes and desserts, ice cream and drinks Decoration of dishes and desserts, ice cream and drinks Decoration of dishes and desserts, herbal teas Decoration of dishes and desserts, salads, juice Decoration of dishes, salads Decoration of dishes and desserts, salads Decoration of dishes, salads Decoration of dishes, salads Decoration of dishes, salads Decoration of dishes and desserts, salads Decoration of dishes and desserts, drinks Decoration of dishes and desserts, ice cream, drinks, juices Decoration of dishes and desserts, drinks, juices Decoration of dishes, salads, herbal teas Decoration of dishes, salads Decoration of dishes, desserts, salads Decoration of dishes and desserts, ice cream Decoration of dishes and desserts, salads, herbal teas Decoration of dishes and desserts, ice cream Decoration of dishes and desserts, ice cream, drinks Decoration of dishes and desserts, drinks
spices, sweetness, smell, softness and bitterness. The consumers decidedly preferred A. houstorianum, B. semperflorens, V. vittrockiana i T. majus due to their tastiness. Results of the study of Kelly, Behe, Biernbaum, and Poff (2001b) performed in USA show that consumers rate edible flowers attributes such as taste, texture and appearance highly. Nationality has an influence on the behaviour and attitudes of consumers towards edible flowers. Research conducted in Taiwan by Chen and Wei (2017) showed that consumers there indicate that curiosity, aroma and health properties have the greatest impact on the attitude towards edible flowers. The aroma also indirectly affects the attitude to the consumption of edible flowers through specific perceptual curiosity. Zimowski (2014) indicates that aroma is one of the most important features of edible flowers. Odour is often a distinctive feature for a given species of flowers (Kaneko et al., 2017). Even varieties of the same species differ in the olfactory bouquet. An example may be rose flowers, which for many varieties smell faintly or do not smell at all, and among those that smell, there are noticeable differences in the type of smell. In many cases, modern varieties of many garden plants, once valued for their scent, today smell less intense. The reason for this seems to be the directional breeding selection, which at the expense of the smell led to obtaining plants with larger, more impressive and durable flowers.
According to the study conducted in Brazil, consumers treat edible flowers as “unknown foods” (Rodrigues et al., 2017). In the study, consumers were asked to express their opinion on foods with edible flowers and the natural yoghurt with flowers was presented for evaluation. The results showed a very positive attitude to both situations, and consumers associated food products containing flowers with “health benefits”, while yoghurt with flowers was considered an innovative product. Flowers were perceived as a surprising and unexpected addition to yoghurt. 1.2. Edible flowers as a source of bioactive substances The introduction of flowers for consumption triggered questions about the value of edible flowers. Apart from adding fresh and exotic aroma, delicate taste and attractive appearance, do they also provide health benefits for the consumer? The answer to this question are the results of research on the composition of active substances isolated from edible flowers. These studies showed the richness of bioactive compounds contained in flowers. Polyphenols and their antioxidant properties are among the most frequently tested compounds. Pires et al. (2018) defined phenol profiles in flower extracts (Dahlia mignon, Rosa damascena, Calendula officinalis L. and Centaurea cyanus L.) and assessed their bioactive potential, including antioxidant, antiproliferative and antibacterial abilities. The highest concentration of 2
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detected. The yellow oranges contained more carotenoids, while the red oranges contained more anthocyanins. The correlation between the content of violaxanthin, zeta-carotene and lutein and the index of yellow colour intensity was proved. In addition to the above mentioned bioactive compounds, edible flowers also contain vitamins and minerals. Vitamins A, C and E were detected in flower petals (Mlcek, Rop 2011). The relatively high content of vitamin C was determined in flower petals of nasturtium, rose and hibiscus (Garzón & Wrolstad, 2009; Özcan 2002). In turn, tocopherols were identified in petals of Rosa canina L., Dahlia mignon, Calendula officinalis L. and Centaurea cyanus L. (Pires, Dias, Barros, & Ferreira, 2017). There are very few studies on the content of mineral compounds in edible flowers. In tests carried out in Brazil, the content of As, Ca, Cd, Co, Cr, Cu, Fe, Mg, Mn, Mo, Na, Ni, P and Zn in rose petals Rosa spp. was determined (dos Santos et al., 2018).
Table 2 Impurities in edible flowers registered in the European Union rapid alert system for food and feed (RASFF) in the years 2004–2018. Flower
Country of origin
Food safety issue
Year
Cornflower blossoms Magosa flower (Azadirachta indica) Chamomile flower Tilia flowers Tilia tomentosa flowers Hibiscus flowers
Albania Thailand
Salmonella Salmonella Stanley
2018 2017
Egypt Bulgaria Albania Egypt
Rat droppings N,N-diethyl-meta-toluamide Dimethoate Infested with insects and moulds, rodent excrements
2016 2015 2014 2008
Sulphite unauthorised
2005
Salmonella Mbandaka Salmonella Hadar
2005 2004
Cinnamon and Sri Lanka cinnamon tree flowers (Cinnamomum verum) Fresh edible flower Thailand Dried marigold Egypt flowers/ Calendula officinalis
1.3. Safety issues of edible flowers’ consumption As stressed earlier, some flowers may contain harmful compounds produced by the plant. In this chapter, however, safety is discussed in the context of external impurities only. Safety issues regarding edible flowers have been already registered in the European Union Rapid Alert System for Food and Feed (RASFF), see Table 2. The main problems are related to the presence of bacteria (Salmonella spp.) or chemical compounds like dimethoate (insecticide), diethyl-meta-toluamide (insect repellent) and sulfites. RASFF data prove that due attention should be paid to the suitable growing, preservation, transport and storage of edible flowers. There is also the need to create awareness regarding the safety of this group of food products among actors on different levels of production chain, as well as the consumers. The microbiological impurities of edible flowers noted so far in RASFF are all related to the presence of different serotypes of Salmonella (see Table 2). Different types of growing as well as harvesting and processing conditions can open the way for bacteria to get onto and into the plant material, including flowers. It may happen before harvest, but it is more likely to happen afterwards (Erickson, 2012; Hirneisen, Sharma, & Knie, 2012). The plants on the field or in the glasshouse may be contaminated through soil, fertilizers or irrigation, especially if watered with surface water (Fornefeld et al., 2017). After the harvest, the contamination can occur through numerous routes during food processing, transport, distribution and preparation. For example, by water and ice used to wash, chill or pack, by contaminated surfaces used for food processing, by food workers not observing the proper hygienic measures, etc. (CDC How Food Gets Contaminated; EFSA, 2018 Zoonotic diseases). The microbial impurities are of concern as edible flowers are mostly consumed fresh and often served in combination with foods such as salads, desserts and cakes, that may constitute a good growth medium for bacteria. Considering data regarding vegetables (de Oliveira, Decol, & Tondo, 2018; Liu et al., 2017) it is not unlikely that some edible flowers may be able to support growth of pathogenic bacteria (including Salmonella) and consequently allow an increase in their concentration during the supply phases. In addition some dishes decorated with edible flowers most certainly are able to support growth of pathogenic bacteria. Considering their use and application edible flowers may be therefore a matter of concern for cross-contamination. The majority of edible flowers are used for decoration. In line with that, there is a possibility they are not consumed at all, and become leftovers. However in case of cross-contamination this does not eliminate the microbial risk. On the other hand, as far as chemical impurities are concerned, the risk related to edible flowers consumption may differ significantly depending on consumer behaviour. What are the possible reasons for the presence of chemical compounds in edible flowers? At least part of them are pesticide residues coming from agricultural production. On different stages of their
phenolic compounds was found in marigolds. Extracts and infusions of rose petals showed the highest antioxidant activity, which may have resulted from the presence of quercetin and kaempferol derivatives. Many publications concern the results of research on the composition and health benefits of different rose varieties. Rose oil in many parts of the world, such as Bulgaria, Turkey, India and Iran, is used to obtain essential oil, rose water, syrup, liqueur and other products. The most important properties of rose oil include diuretic, sedative, anti-migraine, antiseptic and antibacterial effects (Schmitzer, MikulicPetkovsek, & Stampar, 2019). Research conducted by Lia et al. (2014) on the total phenolic content and antioxidative abilities of 51 edible and wild flowers showed that the wrinkled rose (Rosa rugosa Thunb.), wavyleaf sea-lavender (Limonium sinuatum L.), sweet osmanthus (Osmanthus fragrans), stripped pelargonium (Pelargonium hortorum L.) and spicy jatropha (Jatropha integerrima Jacq.) are characterized by the highest content of homogentisic acid, cyanidin-3-glucoside, protocatechuic acid, catechin, gallic acid and epicatechin. In other studies, it was shown that out of the 23 studied Chinese flowers Osmanthus fragrans (Thunb.) Lour, Paeonia lactiflora Pall and Rosa rugosa Thunb (violet) were characterized by the strongest antioxidant activity before or after in vitro digestion, suggesting that these flowers are important natural sources in the prevention of oxidative stress diseases (Chen et al., 2015). Most researchers emphasize that edible flowers are characterized by a high content of antioxidative polyphenols. Research conducted by Chen, Chen, Xiao, and Fu (2018) showed that the wrinkled rose (Rosa rugosa Thunb.), wavyleaf sea-lavender (Limonium sinuatum L.), Chinese quince (Chaenomeles sinensis (Thouin) Koehne), sweet osmanthus (Osmanthus fragrans), giant crepe-myrtle (Lagetstroemia speciose L.) and rosemary (Rosmarinus officinalis L.) showed the strongest antioxidant activity among the 30 tested flowers and these flowers contained the highest total phenols (TPC) and total flavonoids (TFC). Researchers suggest that flower extracts can be used as functional foods in the prevention of chronic diseases. Colour plays a very important role in food and nutrition and is an important organoleptic property of edible flowers (Śmiechowska & Dmowski, 2014, pp. 343–359). The colour of flowers primarily depends on the content of carotenoids and anthocyanins. In edible flowers, the increased content of anthocyanins is mostly positively correlated with higher levels of total flavonoids (Friedman et al., 2010). No research on the dependence of the colour of flowers on the content of bioactive substances has been conducted thus far. However, in the study of carotenoids content in fruits (Ben Abdelaali et al., 2018) a significant dependence of the colour on the content of bioactive compounds was 3
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development, plants are endangered by various harmful organisms. If chemical products are used to control insects, weeds and fungi then pesticide residues are detected in the final product. Detection of pesticide residues is a natural consequence of making use of them. Therefore, pesticide residues are regularly monitored in crops and in food (Mojsak, Kaczyński, & Łozowicka, 2018; Rutkowska, Łozowicka, & Kaczyński, 2018). If pesticide residues are detected within legal limits, it means if their amounts do not exceed maximum residue levels (MRL), the food is safe. Such result would be of course not reported in RASFF. In case of edible flowers it is, however, not unlikely that if the pesticides are used to protect plants, the residues may exceed MRL. There are two different reasons for that, depending if the flowers come from ornamental plants or from plants that are produced for food. In case of most plants produced for food, the agricultural production process is not focused on the flower to be eaten. The development of flower into the fruit or seed takes some time. Within that time plant protection product applied prior to flowering have chance to decompose. The timing of application recommended in the label of plan protection product takes this gap into account. If the flower is harvested, that gives less time for any chemical protection products used in the agricultural production process to decompose. Logically, it means that residues of pesticides in the flowers may be higher than permitted. There are of course some plants like cauliflower or broccoli where flower is the main edible plant part and in their case this safety issue is not relevant. However, cauliflower and broccoli are usually counted among vegetables, and despite being flowers are rarely referred to as “edible flowers”. Sometimes edible flowers come from plants that are typically grown for ornamental purposes. Orchids or chrysanthemums may serve as an example here. Ornamental plants are produced for their beauty and are usually grown with great care to avoid any pest damages. In case of ornamental plants even the slightest visible damage of leaves or flowers may mean that the crop has no market value. Therefore, there are fertilisation programmes and available pesticides to ensure that they look beautiful. The products used in the process of agricultural production must be applied in the way safe for the workers, for soil and for non-target species (for example bees) (Matyjaszczyk, 2017). However, normally MRLs are not an issue in ornamental plants as those plants are not intended for human consumption. It may happen, that even if ornamental plants are produced with due respect to all appropriate rules and chemical protection is applied following minutely the label, the flowers may still contain chemical substances of different kind in the amounts not suitable for food products. The efficient plant protection products consisting of natural compounds are not always available (Matyjaszczyk, 2018). Therefore, ornamental plants produced for yield of flowers to be consumed by humans should be grown separately from ornamental plants grown for ornamental purposes. They should be also fertilized and protected in the manner that the final product meets all safety criteria regarding human consumption. We can assume as much, just by applying logical approach. However, the devil is in the details. Namely, how those ornamental plants should be taken care of? What products should be used for their protection? In what doses? The recommendations on how to use plant protection products are given in the product label, which is approved by the responsible authority. However, only common recommendations following the intended use are available on the label. The ornamental plants as such are considered to be “minor crop” owing to the fact that due to the limited area they are not in the focus of the attention of agrochemical companies. The production of flowers of ornamental plants intended for human consumption is a margin of margin. No chemical company is interested in registration of such use and performing necessary laboratory tests. Consequently, the recommendations regarding the protection of edible flowers are as a rule not available. It is therefore not unlikely that in the absence of guidelines for edible flowers, farmers may follow the label recommendations regarding plants for ornamental use, thus exceeding
the safety limits. Some edible flowers come from wild plants, collected from wild stands. Contamination of flowers with similar but poisonous relatives growing in the neighbourhood is therefore not unlikely. In the case of wild plants, especially those that come from an area that is not in agricultural use, there may be a concern of chemical impurities absorbed from soil or from air. High concentration of heavy metals in soil is a recognised problem in certain areas (Superville et al., 2017). It is also known that heavy metals, for example cadmium, are absorbed by plants and safety concerns may arise after those plants are consumed by humans (Matyjaszczyk & Schumann, 2018). Another matter of concern are impurities in the air, among others those that come from automotive or from industrial pollution (Omasa, Tobe, & Kondo, 2002). Therefore, in case of edible flowers coming from wild plants the place of their harvest may influence the safety of their consumption. In terms of legal rules the problem of pesticide and heavy metal residues in edible flowers was recognised in some regions. For example in the European Union an MRL group “Herbs and edible flowers” (code number 0256000) with a sub-group “basil and edible flowers” (code number 0256080) is established and therefore unambiguous rules regarding maximum levels of pesticide and heavy metal residues in edible flowers are set. The risk for humans can be calculated as a function of hazard and exposure (EFSA, 2018). If hazard is defined as chemical impurities in edible flowers, in turn exposure can be calculated considering the data on the amount of pesticides or heavy metals and the edible flower consumption data. As consumption of flowers is rarely significant in terms of volume, the risk in most cases is not likely to be very high. Anyway, the risk is worth stressing, especially among frequent consumers. Source: Years 2015-2018 own search, earlier Fernandes, Casalb, Pereiraa, Saraivac, and Ramalhosaa (2017): Edible flowers: A review of the nutritional, antioxidant, antimicrobial properties and effects on human health. 2. Conclusions Edible flowers are gaining more and more popularity among the consumers, cooks and confectioners. They are appreciated for their sensory values, such as taste and aroma and evoke positive aesthetic impressions. Edible flowers also provide bioactive compounds in the form of polyphenols, vitamins and minerals. Each food product must, however, be primarily safe for the consumer and in the case of edible flowers there are no clear legal regulations such as a list of flowers allowed for consumption, growing conditions, harvest dates, storage conditions and substances authorized for use in the protection of edible flowers. The RASFF data show that microbial contamination and the presence of chemical residues make it necessary to pay special attention to the proper cultivation, preservation, transport and storage of edible flowers. It is also necessary to increase awareness of the safety of this group of food products among entities operating at different levels of the production chain, as well as consumers. References Akinmoladun, A. C., Olaleye, M. T., & Farombi, E. O. (2014). Cardiotoxicity and cardioprotective effects of african medicinal plants. In V. Kuete (Ed.). Toxicological survey of african medicinal plants., 2014Elsevier Inchttps://www.sciencedirect.com/book/ 9780128000182/toxicological-survey-of-african-medicinal-plants, Accessed date: 25 August 2018. Ben Abdelaali, S., Rodrigo, E., Saddoud, O., Zacarías, L., Rabeh, M., & Messaoud, M. (2018). Carotenoids and colour diversity of traditional and emerging Tunisian orange cultivars (Citrus sinensis (L.) Osbeck). Scientia Horticulturae, 227, 296–304. Benvenuti, S., Bortolotti, E., & Maggini, R. (2016). Antioxidant power, anthocyanin content and organoleptic performance of edible flowers. Scientia Horticulturae, 199, 170–177. CDC How Food Gets Contaminated The food production chain. https://www.cdc.gov/ foodsafety/production-chain.html, Accessed date: 18 December 2018. Chen, G.-L., Chen, S.-G., Xiao, Y., & Fu, N.-L. (2018). Antioxidant capacities and total
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