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Composition and functionality of bee pollen: A review
Journal Pre-proof Composition and functionality of bee pollen: A review Mamta Thakur, Vikas Nanda
PII:
S0924-2244(19)31021-0
DOI:
https://doi.org/10.1016/j.tifs.2020.02.001
Reference:
TIFS 2736
To appear in:
Trends in Food Science & Technology
Received Date: 16 November 2019 Revised Date:
5 January 2020
Accepted Date: 3 February 2020
Please cite this article as: Thakur, M., Nanda, V., Composition and functionality of bee pollen: A review, Trends in Food Science & Technology (2020), doi: https://doi.org/10.1016/j.tifs.2020.02.001. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2020 Published by Elsevier Ltd.
Authors’ Contribution Statement Mamta Thakur has framed the article structure; searched, complied and interpreted the literature and written the manuscript. Professor Vikas Nanda has technically reviewed and edited the manuscript. Both authors contributed critically to the final revised form of the manuscript.
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Composition and functionality of bee pollen: A review
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Running head: Bee pollen: Composition & functionality
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Mamta Thakur* and Vikas Nanda
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Department of Food Engineering and Technology
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Sant Longowal Institute of Engineering and Technology (Deemed-to-be-University), Longowal -
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148106 (Punjab) India
7 8 9 10 11 12 13 14 15 16 *
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Corresponding Author:
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Mamta Thakur
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Department of Food Engineering and Technology
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Sant Longowal Institute of Engineering and Technology (Deemed-to-be-University)
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Longowal - 148106 (Punjab) India
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E-mail: [email protected]
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ORCID: 0000-0002-6052-6819 1
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Abstract
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Background
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The food industry today is returning to natural foods after emphasizing the processed products
27
due to the higher consumer demand for foods which are well recognized by healthy nutrients.
28
Bee pollen is known as a natural superfood due to its indispensable nutritional and medicinal
29
properties. However, the physico-chemical and nutritional properties of bee pollen are
30
ambiguous which vary greatly due to the difference of botanical and geographical origin.
31
Scope and approach
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The current study, therefore, presents an updated overview by critically reviewing the literature
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for chemical constituents (sugars, amino acids, fatty acids, minerals, vitamins, and phenolic
34
compounds) of bee pollen since 2009 from more than 20 nations of the world. The functional
35
properties of different plant-derived bee pollen and their food applications are also discussed for
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the first time.
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Key findings and conclusions
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As per the systematic review of above 100 studies, the bee pollen contains average 54.22%
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(18.50-84.25%) carbohydrates, 21.30% (4.50-40.70%) proteins, 5.31% (0.41-13.50%) lipids,
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8.75% (0.15-31.26%) fibre, 2.91% (0.50-7.75%) ash, 13.41 g/100g (2.77-28.49 g/100g) glucose,
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15.36 g/100g (4.9-33.48 g/100g) fructose, 4.25 g/100g (0.05-9.02 g/100g) sucrose, 4951.61
42
mg/kg (3.06-13366.60 mg/kg) potassium, 4157.86 mg/kg (234.40-9587.00 mg/kg) phosphorus,
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1751.22 mg/kg (1.09-5752.19 mg/kg) calcium, 1246.99 mg/kg (44.00-4680.53 mg/kg)
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magnesium, 46.97 mg/kg (0.10-105.80 mg/kg) zinc, 197.41 mg/kg (2.60-1180.00 mg/kg) iron,
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and 30.59 mg GAE/g (0.69-213.20 mg GAE/g) total phenolic content. Bee pollen, based on its
46
functional properties can be recommended as a natural food ingredient in several processed food 2
47
products. Further, the present paper strongly focuses to investigate the mono-floral bee pollen
48
from different geographical regions and related safety issues to establish the global pollen quality
49
and safety standards in coming years.
50
Keywords: Bee pollen; essential amino and ω-3 fatty acids; B-complex vitamins; polyphenols;
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functional properties; food applications
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1. Introduction
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Recently, the bee pollen has demonstrated great attention in food processing as it is a
54
paragon of wholesome nutrients (Sattler et al., 2015; Thakur & Nanda, 2018a). It contains
55
mainly lipids, proteins, and micronutrients essential for honeybees whereas it exhibits the
56
nutraceutical potential for humans, thereby preventing several diseases (de Melo & Almeida-
57
Muradian, 2010; Komosinska-Vassev, Olczyk, Kafmierczak, Mencner, & Olczyk, 2015). For the
58
heightened application of bee pollen, its comprehensive characterization based on physico-
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chemical, nutritional, and functional characteristics as per floral and geographical source is need
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of the hour.
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Basically, the pollen is the microscopic structure like grains, found in the anther of
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stamen in the angiosperms (Steven, 2014). Worker honeybees during visits attract the hundreds
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to thousands of pollen grains using weak electrostatic field generated between flower (negatively
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charged) and bee body (positively charged) (Clarke, Morley, & Robert, 2017). The pollen grains
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are agglutinated using the several combs and hairs of bee’s hind legs which are moistened with
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salivary secretions and nectar to form a pellet of size 1.4-4 mm i.e. characteristically distinct
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from wind pollen (Saavedra, Rojas, & Delgado, 2013). Thus bees carry the pollen as pellets
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using the pollen basket and stored inside the alveoli for further consumption to fulfill the
69
requirements for protein and to synthesize the jelly in their food glands (Di Pasquale et al., 3
70
2013). The bee colony can collect 50-250 g of pollen per day or 15-40 kg per year (Komosinska-
71
Vassev, Olczyk, Kafmierczak, Mencner, & Olczyk, 2015).
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Bee pollen, also known as apicultural or bee-collected or corbicular pollen can be
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harvested with the help of trap, fixed at the entrance of beehives. While returning home, the
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pollen is lost from the hind legs and collected in the collection tray of the trap (Fig. 1). The
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nutrient-dense pollen thus collected is high in moisture content and its properties initiate to
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degrade after the collection. Therefore, the bee pollen must be consumed either fresh or quickly
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dried carefully to retain the nutrients (Denisow & Denisow-Pietrzyk, 2016; Kieliszek et al.,
78
2018). The plant sources of bee pollen, as determined by palynological analysis strongly affect
79
its nutritional, physico-chemical, and functional properties (da Silva et al., 2014; Nogueira,
80
Iglesias, Feás, & Estevinho, 2012; Yang et al., 2013; Thakur & Nanda, 2018a). The pollen
81
pellets from unique botanical taxon or the ones having single predominant pollen at > 90%
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frequency or containing no accessory pollen at > 60% frequency are considered as mono-floral
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(Barth et al., 2010). However, in case of inadequate flora surrounding the hive, the honeybee will
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visit the flower of other botanical sources and thus the microscopic pollen grains are mixed,
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resulting in the pellet known as multi-floral pollen when there is no predominance and may
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present accessory pollen varying from 15-45% (Barth et al., 2010). The flower from plant
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species affects the color of pollen grain ranging from white or creamish white and yellow to
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orange, red, green, gray and dark brown. The physico-chemical, functional and sensory
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properties are usually fixed for mono-floral pollen of a particular botanical origin whereas the
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multi-floral pollen loads vary in the properties (Barth et al., 2010). Even after a similar plant
91
source, pollen composition may vary due to seasonal and regional variations (de Melo, Freitas,
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Barth, & Almeida-Muradian, 2009). 4
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Bee pollen contains carbohydrates (13-55 %), proteins (10-40 %), lipids (1-13 %), crude
94
fibre (0.3-20 %) and ash content (2-6%) (Campos et al., 2008). In addition, it is composed of all
95
essential amino and fatty acids, free amino acids, vitamins mainly B-complex, essential minerals,
96
carotenoids and flavonoids (Mărgăoan et al., 2014; de Melo et al., 2016; Ghosh & Jung, 2017;
97
Thakur & Nanda 2018a). Fructose followed by glucose and sucrose is the major sugar and nearly
98
1% of remaining sugars in pollen include arabinose, isomaltose, melibiose, melezitose, ribose,
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trehalose, and turanose (Chantarudee et al., 2012; Liolios et al., 2018). It is acclaimed for its
100
excellent nutrition and therapeutic properties, and currently, commercially consumed as a dietary
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supplement. Bee pollen has been acknowledged by law as a food additive in Argentina, Brazil,
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and Switzerland where its standard norms of physico-chemical and microbiological quality have
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been officially instituted. Likewise, several other countries have established the physico-
104
chemical parameters of pollen for its healthy intake (Fuenmayor et al., 2014; Canale et al., 2016).
105
Therefore, a vast research interest has been observed about bee pollen and numerous studies
106
have been conducted for characterizing the pollen of varying floral origins from different regions
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of numerous countries like Brazil, China, Greece, India, Portugal, Romania, Spain, South Africa,
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Saudi Arabia, etc. to identify the peculiarities (Yang et al., 2013; Liolios et al., 2016; Sagona et
109
al., 2017; de Melo et al., 2018a; de Melo et al., 2018b; Gardana, Del Bo, Quicazan, Corrrea, &
110
Simonetti, 2018; Liolios et al., 2018; Thakur & Nanda, 2018a; Isik, Ozdemir, & Doymaz, 2019;
111
Liolios et al., 2019a,b). However, as per the literature survey, a detailed review of bee pollen still
112
lacks its physico-chemical and functional properties. Globally, a generic quality criterion for
113
pollen was suggested by Campos et al. (2008) whereas Puerto, Prieto, and Castro (2015) focused
114
on the phytochemicals reported in pollen contributing to antioxidant potential. As per the
115
literature, the biological and medicinal activities of pollen were discussed by Denisow and 5
116
Denisow-Pietrzyk (2016); the extraction techniques of pollen derived bioactive compounds were
117
analyzed by Ares, Valverde, Bernal, Nozal, and Bernal (2017) and Li et al. (2018) studied the
118
nutritional and biological properties of pollen from a limited botanical and geographical sources.
119
Further, the metabolism of bee pollen derived natural metabolites and food safety of pollen were
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discussed in many studies which seems to be unsatisfactory without the detailed knowledge of
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bee pollen composition and functionality. This paper, therefore, aims to present a comprehensive
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and updated summary of researches from the previous 10 years on physico-chemical
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composition and functionality of bee pollen from diverse botanical and geographic roots of more
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than 20 countries which will fortify the existing knowledge about the bee pollen composition.
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2. Nutritional value
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Today the health-conscious consumers prefer to consume the value-added products which
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allow replacing the conventional food ingredients with high-nutritional value component to
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supplement the existing processed products. The human diet should provide the energy and other
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essential nutrients required for physical and mental development and health in amounts that meet
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standards (Kieliszek et al., 2018). Due to the excellent nutrient profile, bee pollen can
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supplement the human diet and provides a significant daily intake of nutrients. Average bee
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pollen composition, as reviewed by Campos et al. (2008) is compared with nutritional
133
requirements for an average adult in Table 1. The share of major nutritional components
134
particularly carbohydrates and fats are comparatively small; however, the crude fiber and protein
135
can contribute significantly up to 60% and 70% of required daily intake (RDI), respectively
136
based on the floral source and location. Further, the daily intake of 50g bee pollen provides all
137
essential vitamins (except pyridoxine and pantothenic acid) and minerals (except calcium)
138
sufficient to meet above 50% requirement of RDI. Bee pollen intake can be increased by adding 6
139
them in routine foods, for instance, mixing in milk, smoothies, yogurt, bread, cookies, fruit
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juices, etc. as seen in case of flaxseed addition in bakery products (Kaur, 2011; Čukelj et al.,
141
2017; Kaur et al., 2018). According to Nagai et al. (2007), the free amino acids, required by the
142
body are adequately provided even by 15g Spanish pollen. Some studies even reported that bee
143
pollen intake is enough for human survival (Nogueira, Iglesias, Feás, & Estevinho, 2012). The
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vitamins from bee pollen contribute to the nutrition greatly and almost all the essential minerals
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are reported in bee pollen in good amounts. However, RDI can vary according to the difference
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in bee pollen composition. The pollen derived nutrients are digested and assimilated in a better
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way which improves the immune system against pathogens, and physical and chemical agents.
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Chinese rape bee pollen is employed as the immunity enhancer of the organism against cancer
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diseases (Omar, Azhar, Fadzilah, & Kamal, 2016). Bee pollen, when administered daily in 40 g
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to heart patients, caused a decrease in their cholesterol level, blood viscosity and fibrinogen and
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fibrin (Campos, Frigerioc, Lopes, & Bogdanov, 2010). Bee pollen also decreases the lipid
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content in blood serum which is considered to link with the level of hormones like insulin,
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testosterone, and thyroxine (Komosinska-Vassev, Olczyk, Kafmierczak, Mencner, & Olczyk,
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2015). However, the bee pollen failed to substantiate health claims under EFSA Regulation (EC)
155
No. 1924/2006 EU (Mateescu. 2011; Onisei, Mateescu, & Răscol, 2018).
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3. Physico–chemical properties
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3.1. Physical properties
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3.1.1. Weight, shape, and size
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The average weight of bee pollen pellet is approximately 7.5-8 mg that varies according
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to the pollen accessibility during the visit. The pollen from a single floral source may be
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significantly dissimilar in shape and size thereby affecting the pollen-packing efficiency 7
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(Komosinska-Vassev, Olczyk, Kafmierczak, Mencner, & Olczyk, 2015). The anemophilous
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plants provide lighter and dried pollen resulting in larger and loosely arranged pellets whereas
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the entomophilous plants are responsible for smaller and more compacted form pollen (Friedman
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& Barrett, 2009).
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The fresh pollen may be cylindrical, round, triangular, or bell-shaped whereas the dried
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pollen pellets having diameter 0.01-0.05 mm are usually spherical or spindle-shaped (Barene,
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Daberte, & Siksna, 2015). Thakur and Nanda (2018b) evaluated the pollen pellets from Cocos
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nucifera, Coriandrum sativum, Brassica napus and multi-floral source of India and reported the
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variation in length, width, equivalent diameter, thousand pollen pellet weight, sphericity, surface
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area, bulk and true density, volume, porosity and angle of repose due to their moisture content.
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On the other hand, Bleha, Shevtsova, Kružík, Brindza, and Sinica (2019) reported the pollen
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loads (Brassica napus, Helianthus annuus, Papaver somniferum, Phacelia tanacetifolia, Robinia
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pseudoacacia, Trifolium repens) of mean 11.85 g weight, 3.10 mm height, and 3.55 mm width,
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from the Slovak Republic. Further, the surface texture of pollen grains provides a hint of their
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botanical composition due to distinct exine structure and properties (Fig. 2) which are
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representative of particular plant species (Wang & Dobritsa, 2018). For instance, the maize has
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thicker exine covered fully with tectum, exine in Brassica is thinner having a reticulated surface
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and Hibiscus contains exines densely covered with long-pointed spines (Basarkar, 2017; Wang
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& Dobritsa, 2018).
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3.1.2. Color
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The pollen quality can be roughly judged based on its color which is linked to plant
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pigments like carotenoids and anthocyanins, inherently found in different concentrations in
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pollen (Sattler et al., 2015). The natural brightness of anther pollen decreases due to the addition
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of moisture particularly nectar to form a pollen pellet. The bee pollen contains all shades of color 8
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from white to black (Fig. 2), however, the pollen collected from the same plant source may have
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different color and sometimes, the bee pollen from various botanical origins can be of similar
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color. Modro, Silva, Luz, and Message (2009) reported that such differences arise from the state
189
of flower thecae which may be either already open or split by honeybees.
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Color is affected by chemical composition also, as revealed by instrumental color
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analysis exhibiting the correlation between color values and Ca, Mg and Fe contents (Yang et al.,
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2013). Likewise, color values of Brazilian pollen were recommended as indices by de Melo et al.
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(2016) to determine the total phenolic content and antioxidant and antimicrobial potential by
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observing the correlation among these parameters. Further, the processing conditions also
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influence the color values, particularly L* and b* and grinding of pollen pellets after dehydration
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results in the supremacy of yellow color and higher positive values of b*. This may be due to
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oxidation reactions of some compounds like polyphenols during drying (Silva, Rosa, & Vilas-
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Boas, 2009).
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3.2. Chemical properties
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3.2.1. Moisture content and water activity
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The concentration of water is a major factor that affects the amount of remaining
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constituents in any product while the quality and storage life is closely associated with the water
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activity (aw) (Nogueira, Iglesias, Feás, & Estevinho, 2012). The higher aw stimulate the growth of
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microorganisms, particularly yeasts and molds, producing the mycotoxins and ochratoxins and
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enzyme activities in bee pollen which may be a fundamental cause of pollen toxicity, creating a
206
risk to consumer (Feás, Vazquez-Tato, Estevinho, Seijas, & Iglesias, 2012). However, the
207
legislations have not yet fixed the standards for its value. Usually, the various perspectives of
208
food quality and safety including moisture sorption, enzymatic activities, etc. are affected by
209
higher aw, thereby increasing the significance of hygienic conditions during handling, drying, and 9
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processing of bee pollen to minimize the likelihood of man-derived contaminations. Table 2
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showed the data about moisture content and aw of pollen of varying plant sources and countries.
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Fresh bee pollen may contain at least 7% and maximum up to 30% moisture content and
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is hence always at the risk of fungal contamination due to its highly hygroscopic nature thus
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questioning the safety of bee pollen (Carpes, Mourão, Alencar, & de Masson, 2009). Sun or
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shade drying should be avoided due to the enhancement of microbial growth and drying below
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3% moisture is also undesirable due to discoloration and generation of off-flavor derived from
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increased rate of chemical reactions like Maillard browning, fructose dehydration, loss of aroma
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compounds and lipids oxidation (Nogueira, Iglesias, Feás, & Estevinho, 2012). Therefore, the
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dried pollen must have moisture content varying from 5-9% and humidity level after drying
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should be kept in a range of 4‒8% which retains the pollen nutrients and ensures the safety (de
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Arruda, Pereira, de Freitas, Barth, and de Almeida-Muradian, 2013a). Freezing is another
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technique to preserve the pollen nutrients but pollen should be processed quickly after thawing,
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using lyophilization, desiccation, and microwave-assisted drying (Conte et al., 2017).
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3.2.2. Carbohydrates and sugars
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Carbohydrates are the largest constituent of bee pollen which accounts for nearly 2/3rd of
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the total pollen dry weight (Li et al., 2018). The higher amount of carbohydrates is due to the
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incorporation of honey or nectar during pellet formation thus enhancing the carbohydrates
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however, the plant species, growth and harvesting conditions are important factors affecting its
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amount. The carbohydrates show a huge variation from 18.50-82.80 % in pollen throughout the
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world (Table 2).
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Pollen consists of monosaccharides - fructose and glucose and disaccharides - sucrose,
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turanose, maltose, trehalose, and erlose, with the fructose/glucose ratio varying between 1.20-
233
1.5. The higher amount of reducing sugars is reported in bee collected pollen (Table 3) which 10
234
makes it distinct from plant pollen (Carpes, Mourão, Alencar, & de Masson, 2009). Liolios et al.
235
(2018) reported an average of 42.10% total sugars in thirty monofloral pollen samples from
236
Greece which varied from 34.70% to 63.50%. Among polysaccharides, the sporopollenin is
237
present in exine – the outer layer of a pollen grain, furnishing a rigid and sculptured framework
238
and is highly resistant to non-oxidative physical, biological and chemical degradation processes
239
including acetolysis thus contributing to encapsulate and protect the pollen contents including
240
bioactive compounds. The inner layer of pollen known as intine consists of cellulose and pectin
241
and Xu, Sun, Dong, and Zhang (2009) stated the structural resemblance between intine and plant
242
cell wall. However, these polysaccharides are not responsible for contributing any nutritional
243
value but important in the regulation of several biological functions.
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3.2.3. Proteins and amino acids
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Proteins are the largest component in pollen after carbohydrates and fulfill the honeybee
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nutritional requirements. It is highly varying in pollen collected from diverse plant sources
247
(Table 2). However, protein content even varies in uni-floral pollen of distinct countries:
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Brassica napus - 19.63% (India), 23 % (Brazil), 27.3 % (China); Cocos nucifera - 25.39%
249
(India), 10.3-20.3 (Brazil); and Zea mays – 14.86% (Greece), 17.9% (China), 23.3 % (Egypt)
250
(Yang et al., 2013; Liolios et al., 2016; de Melo et al., 2018a; Thakur & Nanda, 2018a). One the
251
other hand, the commercial bee pollen of Attiki Bee Culturing Co.-Alex Pittas S.A., Athens,
252
Greece contained 17.60% protein (Karabagias, Karabagias, Gatzias, & Riganakos, 2018). The
253
possible reason for this is the mixing of nectar in bee pollen. Moreover, bee pollen on drying
254
may contain 2.5-62% protein depending on the botanical origin and such a high amount signifies
255
the role of this macronutrient as a novel dietary supplement, particularly for vegetarians
256
(Campos, Frigerioc, Lopes, & Bogdanov, 2010).
11
257
Bee pollen dominantly contains bound-form amino acids and 1/10th of total proteins are
258
available as free amino acids whose composition is also affected by botanical origin and
259
processing and storage conditions (Domínguez-Valhondo, Gil, Hernández, & González-Gómez,
260
2011). The plant species affects the amino acid composition more in terms of quantity rather than
261
quality (Table 3). Glutamic acid and in some studies proline as well as aspartic acid are major
262
amino acids reported in pollen from plant species of different countries. The honeybees are
263
directly responsible for the proline level which seems to increase during storage due to its
264
synthesis in the presence of glutamate dehydrogenase from glutamic acid (Verslues & Sharma,
265
2010). Free amino acid content should be a minimum 2% which is essential for the
266
standardization of bee pollen in the European market. Besides this, the “proline index” must be
267
<80%, critical to indicate the pollen freshness (Canale et al., 2016). The bee pollen also contains
268
a higher level of essential amino acids (EAAs) which furnishes the high nutritional value for
269
honeybees and humans (Yang et al., 2013; da Silva et al., 2014). According to the previous
270
studies, among EAAs, leucine and lysine were reported in the greatest quantities from several
271
countries (Table 3). In the viewpoint of human nutrition, lysine – the limiting amino acid in
272
cereals is present in adequate amount and interestingly, tryptophan is reported in surprisingly
273
higher amount (0.70-14.80 g/100 g) in Chinese bee pollen which is otherwise the limiting amino
274
acid in pulses (Yang et al., 2013). Pollen also contains the threonine - the second rate-limiting
275
amino acid which is along with isoleucine and phenylalanine is known as glucogenic as well as
276
the ketogenic amino acid, respectively (Dong et al., 2018). Being the precursor of arserine,
277
carnosine, and histamine, the histidine is also important owing to the response of synthesized
278
histamine for allergic reactions and plays a great role in the dilation and blood vessels
279
contraction (Peachey, Scott, & Gatlin III, 2018). Arginine is considered as an essential amino 12
280
acid in the present paper which is critical for child nutrition only. Thus, all EAAs are reported in
281
bee pollen (except a few studies) ranging from 12-45.02% of total amino acid content which is
282
comparable to the supply of essential amino acids (33.9%) as per FAO reference protein
283
(Komosinska-Vassev, Olczyk, Kafmierczak, Mencner, & Olczyk, 2015; Thakur & Nanda,
284
2018a).
285
3.2.4. Lipids and fatty acids
286
After carbohydrates and proteins, lipids are the third-largest constituent of bee pollen
287
which are vital for the generation of royal jelly (Sattler et al., 2015). Pollen from some botanical
288
species contains total lipid content, varying from 1-13% of pollen dry weight (Campos et al.,
289
2008), however, Martins, Morgano, Vicente, Baggio, and Rodriguez-Amaya (2011), Odoux et al.
290
(2012), de Melo et al. (2018a) and Liolios et al. (2019b) revealed even higher lipid content up to
291
13.32, 24, 13.50 and 13.60%, respectively as shown in Table 2. They are usually comprised of
292
triglycerides, carotenoids, and sterols in bee pollen (Mărgăoan et al., 2014; Sattler et al., 2015).
293
However, a few investigations focused on the sterols profile in bee pollen (Mărgăoan et al.,
294
2014) and most research work in the literature focused on the estimation of total pollen lipid
295
content (Table 2). The relative proportion and level of certain fatty acids are very important in
296
determining the quality of lipids because honeybees require fatty acids for reproduction,
297
development, and nutrition. The bactericidal and antifungal properties of linoleic, linolenic,
298
myristic, and lauric acids primarily hinder the multiplication of Paenibacillus and Melissococcus
299
pluton – the spore-forming bacteria and other microorganisms which may colonize the brood
300
combs otherwise, thus contributing to colony hygiene (Dong, Yang, Wang, & Zhang, 2015). The
301
human also requires lipids due to fraction of essential fatty acids (EFAs) and antioxidant
302
substances for growth, development and prevention of diseases (Glick & Fischer, 2013). Many
303
biological functions require EFAs for regulated levels of plasma lipids, insulin activity, 13
304
cardiovascular, and immune function, etc. to ensure better health (Glick & Fischer, 2013; Kaur,
305
Chugh, & Gupta, 2014).
306
Conte et al. (2017) reported a higher amount of phospholipids, tocopherols, and
307
phytosterols, recommending an intensive lipolytic process as the pollen characterization
308
parameter. In bee pollen, a strong correlation was suggested between the fatty acids (FAs)
309
composition and botanical species, however, Brazilian pollen of Mimosa caesalpiniaefolia and
310
Cestrum showed a negative association (de Melo, Freitas, Barth, & Almeida-Muradian, 2009;
311
Mărgăoan et al., 2014; Sattler et al., 2015). These findings suggested the association of certain
312
pollen with more or fewer lipids concentrations. Moreover, huge variations are reported in lipid
313
content of mono-floral pollen from different countries: Brassica napus - 4.7% (Brazil), 6.6 %
314
(China), 7.76% (Greece), 12.38% (India); Cistus sp. -1.9 % (Italy), 3.80% (Greece), 7.2 %
315
(Spain); Cocos nucifera–10.43 % (India), 4.6-5.1% (Brazil) (Table 2) (Domínguez-Valhondo,
316
Gil, Hernández, & González-Gómez, 2011; Yang et al., 2013; Sagona et al., 2017; de Melo et al.,
317
2018b; Thakur & Nanda, 2018a; Liolios et al., 2019b).
318
Nearly 20 FAs were reported in bee pollen from C4 to C24 among which ω-3 fatty acids
319
are dominating (Table S1). Myristic, stearic and palmitic acids are the major saturated fatty acids
320
while α-linolenic, linoleic and oleic acids are the most prevalent unsaturated fatty acids reported
321
in bee pollen. According to the literature, bee pollen of several countries contains α -linolenic,
322
palmitic, and linoleic acids in higher amount along with significant levels of arachidonic,
323
behenic, capric, caproic, caprylic, 11-eicosenoic, elaidic, lauric, lignoceric, myristic, oleic, and
324
stearic acids (Table S1). Zea Mays (mono-floral) pollen from China contained α-linolenic (52%)
325
and palmitic (25%) acids as predominant fatty acids while the same origin pollen from Egypt
326
was rich in oleic (42%) and myristic (40%) acid. Likewise, the γ-linolenic acid (29.08 %) and 14
327
eicosatrienoic acid (13.83%) were reported prevalent in Indian Brassica napus pollen whereas
328
the α-linolenic acid (30.82%) and myristic acid (20.70%) were present in higher amount in bee
329
pollen of the same origin from China (Yang et al., 2013; Thakur & Nanda, 2018a). Keeping in
330
view the previous studies, it is observed that fatty acids are the same in different pollen but their
331
proportion varies according to the floral sources or even within the same species and
332
geographical regions. It is believed that honeybees prefer the pollens which contain a higher
333
amount of unsaturated fatty acids compared to saturated ones. Thakur and Nanda (2018a)
334
reported the values of unsaturated: saturated fatty acid (UFA to SFA ratio) of bee pollen ranging
335
from 2.2-6.7 which refers to the high quality of bee pollen lipids. A higher value of UFA/SFA
336
demonstrates the reduced levels of fats and cholesterol, thereby preventing cardiovascular
337
disease, but if the value is below 1, the UFA/SFA ratio then exhibits the degradation of
338
unsaturated fatty acids during the time due to the storage and dehydration process. The UFAs are
339
an important component of membrane phospholipids and therefore helps to maintain the
340
membrane fluidity which will thus improve the membrane functionality and also cell metabolism
341
(Mărgăoan et al., 2014). Among fatty acids, the saturated, monounsaturated and polyunsaturated
342
fatty acids represented the 4.29-71.47%, 1.29-53.24%, and 4.33-75.71%, respectively in pollen
343
whereas ω-3 fatty acids varied from 8.07-44.1% and ω-6 fatty acids ranged from 1.77-38.25 % as
344
reported in several studies summarized in Table S1. Any fresh food is said to be the “source of
345
ω-3 FAs” if ω-3 fats are found in concentration 300 mg/100g under the regulation EC 1924/06 of
346
Europe; therefore, bee pollen can be regarded as a significant ω-3 FAs source for improved
347
human nutrition (Li et al., 2018). Further, the ω-6: ω-3 FAs ratio performs a critical role in the
348
eicosanoids synthesis in the human body thereby regarded as beneficial to health. ω-6:ω-3 ratio
349
is an important criterion to evaluate the health properties of food and it must be 5:1 or less 15
350
(Simopoulos & DiNicolantonio 2016). Bee pollen contained this ratio varied from 0.059-3.090;
351
thereby it is an essential source of ω-3 FAs in the human diet (Margaoan et al., 2014; Thakur &
352
Nanda, 2018a).
353
Bee pollen is the potential source of EFAs: α-linolenic and linoleic acid, however, its
354
amount varies according to the botanical origins (Komosinska-Vassev, Olczyk, Kafmierczak,
355
Mencner, & Olczyk, 2015). The amount of linoleic acid differed greatly like 3.25-11.32 g/100g
356
in bee pollen from India, 7.62-33.21 g/100g from Romania and 2.66-24.38 g/100g from China,
357
while the α-linolenic acid ranged from 0.5-16.28 g/100g from Indian bee pollen, 20.28-46.93
358
g/100g in Romanian bee pollen, and 4.11- 58.52 g/100g in Chinese bee pollen (Yang et al., 2013;
359
Mărgăoan et al., 2014; Thakur & Nanda, 2018a). Both EFAs are important to carry the metabolic
360
processes and also being present as the component of cell membranes thus improves the brain
361
function (Perini et al., 2010). Docosahexenoic acid, simply DHA (C22:6n-3) usually present in
362
fish oil is also reported in bee pollen. Nervonic acid – an important constituent of the white
363
matter of animal brains is mainly obtained from lipids of fish and crab eggs but its presence in
364
bee pollen from different botanical origins of multiple countries is a novel finding (Table S1),
365
revealing the pollen significance in human’s nervous system and brain development.
366
Bee pollen also contains minute levels of phospholipids and plant sterols (mainly β-
367
sitosterol) (1.5 and 1.1%, respectively) wherein β-sitosterol and triterpene compounds such as
368
oleanolic and ursolic acid reduces the cholesterol absorption in intestines and generation of
369
tumor diseases, respectively (Komosinska-Vassev, Olczyk, Kafmierczak, Mencner, & Olczyk,
370
2015).
371
3.2.5. Dietary fiber
372
The dietary fiber, also known as roughage refers to the portion of food which remains
373
intact throughout the stomach and small intestine thus contributing nothing to the nutritional 16
374
value of food but is essential to human health. The dietary fibers are basically of two types:
375
soluble and insoluble. The soluble dietary fiber (SDF) reduces the blood cholesterol and glucose
376
levels whereas the insoluble dietary fiber (IDF), also called resistant starch, supports the passage
377
of food through the digestive system thus increasing the stool bulk and preventing the irregular
378
stools or constipation.
379
The dietary fiber comes from sporopollenin, cellulose, hemicellulose, and pectin found in
380
the outer-covering of bee pollen while the starch and other insoluble polysaccharides such as
381
callose, cellulose, lignin, etc. constitute the crude fiber. However, the highest and lowest values
382
of crude fiber alter considerably (Table 2) due to various analytical methods and plant sources.
383
Enzymes hydrolyze the complicated fibrous pollen structures and release sugars to harness as a
384
source of carbon for bacterial fermentation (Bobadilla, 2009). However, the change in fiber
385
concentration due to fermentation is not significant from the nutritional quality viewpoint.
386
Bee pollen is a useful fiber source for food, with cellulose and callose as the main
387
portion. Total dietary fiber (TDF) ranged from 17.60-31.26% while the IDF and SDF values
388
varied from 73-82% and 0.86-5.92% of TDF in pollen from China (Yang et al., 2013). Likewise,
389
the Colombian pollen contained IDF contents higher (8.0- 13.9 g/100g) than the SDF (1.3-2.3
390
g/100g) with TDF of 9.9-15 g/100g (Bobadilla, 2009). However, Fuenmayor et al. (2014)
391
reported a higher amount of SDF 2.7± 1.8 g/100 g compared to IDF (11.7±3.3 g/100 g) in
392
Colombian pollen with TDF of 14.5 g/100 g. On the other hand, Domínguez-Valhondo, Gil,
393
Hernández, and González-Gómez (2011) studied the Spanish bee pollen which showed no
394
remarked variations in their dietary fiber (14.50-14.65% dry weight) and suggested the
395
exploration of pollen fiber in processed foods to reduce the lack of dietary fiber.
396
3.2.6. Minerals
17
397
The mineral or ash content is essential for retaining the cell protection, activities,
398
homeostasis, and health. For instance, calcium (Ca), phosphorus (P), and magnesium (Mg), in
399
combination, assists in the development and maintenance of bone tissue and regulating the blood
400
as well as intercellular and cellular fluids osmotic pressure while cobalt (Co), copper (Cu), iron
401
(Fe), manganese (Mn), and zinc (Zn) are crucial for the body growth, development, reproduction,
402
and blood formation. Hence, the insufficiency of these bio-elements may cause diverse metabolic
403
disorders, acute growth defects and even result in mortal illnesses (Prashanth, Kattapagari,
404
Chitturi, Baddam, and Prasad, 2015; Quintaes & Diez-Garcia, 2015).
405
The day-to-day mineral requirements for humans were recorded: Ca: 0.8-0.9 g, Cu: 1-3
406
mg, Fe: 10-20 mg, K: 800 mg, Mg: 300-400 mg, Mn: 4-5 mg, nickel (Ni): 15-25 µg, P: 0.8-1.2 g,
407
selenium (Se): 60-120 µg, and Zn: 6-22 mg (Tayar & Cibik, 2011; Demirci, 2014) whereas the
408
following daily mineral specifications have been suggested by Brazilian laws: Ca: 1000 mg,
409
chromium (Cr): 35 µg, Cu: 900 µg, Fe: 14 mg, K: 4700 mg, Mg: 260 mg, Mn: 2.3 mg, P: 700
410
mg, Se: 0.034 mg and Zn: 7 mg for an adult of 19-30 years age (Sattler et al., 2016). The bee
411
pollen possesses 2.5–6.5% ash content (Table 2) wherein above 25 minerals are present in it but
412
the amount of each essential mineral varies as per different floral sources and countries (Table
413
4). Ca, Cu, Cr, Fe, K, Mg, Mn, Na, P, and Zn were commonly reported in bee pollen globally
414
and other minerals like boron (B), molybdenum (Mb) and selenium (Se) are rarely present in bee
415
pollen of few origins ranging from 8.2–14, 0.1–4.6 and <0.01–4.5 mg/kg, respectively (Yang et
416
al., 2013; Sattler et al., 2016; Altunatmaz, Tarhan, Aksu, Barutçu, & Or, 2017).
417
Ash content is largely affected by many factors, mainly soil, climate, geographical origin,
418
and botanical species in terms of plant capacity to accumulate the mineral salts in its pollen
419
(Carpes, 2008). Formicki et al. (2013) and Yang et al. (2013) have suggested that soil type is the 18
420
main cause for variation in element composition of pollen. Liolios et al. (2019a) had analyzed
421
the similar pollen taxa (Sinapis arvensis and Cistus creticus) from ten different regions of
422
Greece and found significant differences in mineral content, particularly K and Ca thus proving
423
evidence of the effect of soil on the mineral content of bee pollen. Another important reason for
424
the mineral variation is the addition of nectar to pollen which may alter the level of certain
425
minerals (Kostic et al., 2015b). However, the drying process did not show any effect on the
426
amount of Ca, Cu, K, Mg, Na, and Zn, as observed by de Melo et al. (2016).
427
The mono-floral Brassica napus pollen from India and China contained K as 4700 and
428
3825 mg/kg, respectively, whereas the Brassicaceae based monofloral pollen from Serbia
429
contained the K content of 3200 mg/kg (Yang et al., 2013; Kostic et al., 2015b; Thakur & Nanda,
430
2018a). These days, Na consumption is increased among the population because of the raised
431
intake of processed foods. But, bee pollen doesn’t contain accelerated Na content (Thakur &
432
Nanda, 2018a). According to the literature, 25 g of bee pollen supplies a maximum of 10% of the
433
suggested intake of Na (2 g/day) by the World Health Organization (WHO, 2012). Generally,
434
most studies reported Na content below 1000 mg/kg but this value reached to 1466, 6223 and
435
8350 mg/kg in Brazilian, Turkish and Saudi Arabian bee pollen, respectively (Morgano et al.
436
2012; Taha, 2015; Kalaycıoğlu, Kaygusuz, Döker, Kolaylı, & Erim, 2017). However, Na level
437
was less than 400 mg/kg from more than 75% Brazilian pollen samples (Morgano et al., 2012; de
438
Melo et al., 2016). Therefore, pollen contains a higher K: Na ratio owing to higher K and lower
439
Na levels which is essential to maintain the optimum electrolytic balance in the body (Carpes et
440
al., 2009).
441
According to the Institute of Medicine (US) (2011), the daily Ca intake of 1000 mg is
442
suggested for a person of age 19-50 years and in the literature, the maximum Ca content (5752 19
443
mg/kg) was reported by Taha (2015). Bee pollen from Brazil had Ca content varying from 643 to
444
4670 g/kg (Carpes, Mourão, De Alencar, & Masson, 2009; Morgano et al., 2012; de Melo et al.,
445
2016). Through the phosphate (PO4−3) salts, Ca plays an important part in blood coagulation,
446
neuromuscular functions, the liberation of hormones, a large number of enzyme-mediated
447
mechanisms and bone and tooth formation beyond being an enzyme component. Investigations
448
supported that an adult may get 2-45% of recommended Mg intake which is 260 mg/day from 25
449
g bee pollen. Recent pieces of evidence suggested that osteoporosis and related bone damages,
450
artery hardening or calcification is the result of elevated Ca and low Mg intakes (Lee, Kim, Kim,
451
Seo, & Song, 2014). Likewise, Fe when consumed in inadequate amounts, causes the behavioral
452
and developmental disorders, anemia, and poor immune system. Bee pollen is a good source of
453
iron and studies revealed that pollen in 25 g may supply 2-220% of the recommended Fe intake
454
i.e. 14 mg/day. Fe is greater in bee pollen than other regular foods like bamboo shoot, cabbage,
455
cassava, cauliflower, mung beans, soybeans, and animal originated foodstuffs (Yang et al., 2013;
456
de Melo et al., 2018a). Similarly, bee pollen (25 g) can satisfy requirements of Zn to a maximum
457
of 120% otherwise its daily suggested consumption for an adult is 7 mg. Bee pollen also contains
458
the elevated Cu content and the positive association between levels of Zn and Cu and antioxidant
459
capacity (determined by DPPH and ORAC methods) was noted, however, Zn and Cu are not
460
considered antioxidant compounds. The reason for this may be an antioxidant enzyme named
461
Cu-Zn superoxide dismutase (Cu-Zn SOD) which is commonly found as cofactors in crops
462
(Mondola, Damiano, Sasso, & Santillo, 2016). Therefore, the presence of Zn and Cu may be
463
considered as an index for the existence of Cu-Zn SOD enzymes in bee pollen also. The lack of
464
Mn may cause deficiency diseases particularly in females which can be reduced by incorporating
465
Mn-rich bee pollen thus supplementing the diet (Panziera, Dorneles, Durgante, & Silva, 2011). 20
466
Se is the constituent of proteins that have a significant part in metabolic activities of thyroid
467
hormone, synthesis of DNA, reproduction and prevent the infection or injury caused due to
468
oxidative stress (Fairweather-Tait et al., 2011). Se content ranged from <0.001–0.445 mg/100g
469
in 154 Brazilian bee pollen samples; however, it was not reported in Chinese bee pollen
470
(Morgano et al. 2012; Yang et al., 2013).
471
Further, Taha (2015) recommended the mineral constituents of pollen as distinct markers
472
to trace the floral source and regulate its quality. However, sometimes due to insufficient
473
cleaning methods, impurities may present in pollen thus enhancing the ash content. Therefore,
474
the each mineral must be examined for its level in bee pollen using advanced and reliable
475
techniques like inductively coupled plasma-optical emission spectrometry (ICP-OES),
476
microwave plasma or inductively coupled argon plasma - atomic emission spectroscopy (MP-
477
AES or ICP-AES) and total reflection X-ray fluorescence (TXRF) which is an important quality
478
index (Yang et al., 2013; Kostić et al., 2015b; Formicki et al., 2013; da Silva et al., 2014; Thakur
479
& Nanda, 2018a).
480
3.2.7. Vitamins
481
Vitamins have a major part to synthesize the vital cofactors, enzyme, and coenzymes
482
based metabolic reactions (Mellidou et al., 2019). They can be found in their original form in
483
nature or exist as precursors or pro-vitamins. Bee pollen usually contains a higher amount of
484
water-soluble vitamins and carotenoids, presented in Table 4. On part of International Honey
485
Commission (IHC), the specifications for vitamin composition of pollen were suggested to be:
486
0.6–1.3 mg/100g thiamine, 0.6–2 mg/100g riboflavin, 4–11 mg/100g niacin, and 0.2–0.7
487
mg/100g pyridoxine whereas the vitamin B complex was also discussed by Mărgăoan,
488
Mărghitaş, Dezmirean, Mihai, and Bobiş (2010) and they reported the following levels of
21
489
thiamine: 0.6–1.3 mg/100g, riboflavin: 0.6–2.0 mg/100g, niacin: 4.0–11.0 mg/100 g, pantothenic
490
acid: 0.5–2.0 mg/100g and pyridoxine: 0.2–0.7 mg/100 g.
491
Very few studies (Table 4) have been conducted about the vitamin composition of bee
492
pollen, focused on Brazil and Thailand only. A high concentration of B-complex vitamins was
493
reported by de Arruda et al. (2013a) and de Arruda, Pereira, Estevinho, & de Almeida-Muradian
494
(2013b) in bee pollen from Brazil. Riboflavin, with involvement in the metabolism of lipids,
495
carbohydrates, proteins, pyridoxine, folic acid, and cobalamin has a significant function in
496
cellular respiration (Pinto & Zempleni, 2016). Niacin after riboflavin is the dominating among
497
B-complex vitamins, thus indicating it a promising supplement for pellagra (Chantarudee et al.,
498
2012). Some authors reported the insignificant amount of lipid-soluble vitamins and vitamin C.
499
However, Sattler et al. (2015) revealed the higher amount of ascorbic acid (6.03-79.70 mg/100g)
500
in Brazilian bee pollen, till date and determined four tocopherols - α, β, γ, and delta-tocopherol
501
with their respective mean values of 328, 0.21, 0.46 and 0.63 mg/100g. Vitamin E has been
502
shown to correlate strongly with b* value, and thus yellow-colored pollen might probably be
503
linked with α-tocopherol (Sattler et al., 2015).
504
β-carotene, also known as provitamin A has 1/6th biological activity of vitamin A and is
505
one of the antioxidant vitamins. Vitamin A in terms of β-carotene was reported in corn bee
506
pollen from Thailand (1.530 mg/100 g) (Chantarudee et al., 2012) and Southeastern Brazil (5.63-
507
19.89 mg/100g) (Oliveira et al., 2009). The difference in vitamin levels may be employed as an
508
indicator of the determination of plant source of pollen; however, the botanical origin, season
509
and processing conditions affect the vitamin composition (Farag & El–Rayes, 2016). Further, the
510
vitamin compounds due to their complexity and low concentration are quite difficult to detect
511
and quantify. Instead of optimizing the efficient extraction and purification process, however, the 22
512
development and validation of the quantification technique may significantly reduce the analysis
513
time, generate less waste and improve the quantification of certain compounds (de Arruda et al.,
514
2013a).
515
3.2.8. Polyphenols
516
Polyphenolic compounds refer to the main secondary plants’ metabolites ranging from
517
anthocyanins, flavonoids, flavonols, flavonones, tannins, etc. to phenolic acids. The phenolic
518
compounds exhibit several biological properties like anti-tumor, anti-aging, anti-inflammatory,
519
anti-diabetic, anti-cancer, etc. due to their function of regulating the enzymatic activity and
520
signal transduction, scavenging the free radicals, chelating the metal ions, and activating the
521
transcription factors and gene expression (Działo et al., 2016).
522
Usually, bee pollen of Portugal, USA, Brazil, China, Egypt, New Zealand, and Greece
523
had total phenolic content (TPC) and total flavonoid content (TFC) values ranging from 0.50-213
524
mg GAE/g and 1.00-5.50 mg QE/g, respectively (de Melo & Almeida-Murandian, 2017;
525
Karabagias, Karabagias, Gatzias, & Riganakos, 2018). Likewise, 56 bee pollen samples from
526
four different regions of Brazil had TPC and TFC values of 6.50–29.20 mg GAE/g and 0.30–
527
17.50 mg QE/g, respectively (de Melo et al., 2018a). TPC and TFC of bee pollen from different
528
botanical sources of several nations are summarized in Table 5. Recently, Kostić et al. (2019)
529
reported TPC and TFC in sunflower (Helianthus annuus) bee pollen of Serbia varying from
530
2907-3816 mg/kg GAE and 843-865 mg/kg QE, respectively which were higher than detected
531
for the same bee pollen of Slovakia (Fatrcová-Šramková, Nôžková, Máriássyová, & Kačániová,
532
2016). The possible reason for this would be the variation in climatic conditions and
533
geographical origin which influence the levels of phenolic compounds in plants (Tolić et al.,
534
2017). When pollen is exposed to poor air or cold conditions, there would be an improvement in
23
535
the biosynthesis of flavonoids during pollen generation and growth (Rezanejad, 2012;
536
Mohammadrezakhani, Hajilou, & Rezanejad, 2018).
537
The phenolic composition of bee pollen of distinct countries differs in geographical and
538
botanical backgrounds and possesses the flavonoids such as apigenin, epicatechin, hesperetin,
539
isorhamnetin, catechin, kaempferol, luteolin, quercetin, naringenin, etc. and phenolic acids like
540
chlorogenic acid, ferulic acid, caffeic acid, gallic acid, vanillic acid, syringic acid, p-coumaric
541
acid, etc. (Table 5). The rape bee pollen from China contained following biologically active
542
compounds: isorhamnetin, kaempferol, and its 3-O-glucosides, naringenin, rutin and quercetin
543
and its 3-O-glucosides (Zhang, Yang, Jamali, & Peng, 2016) whereas the same biologically
544
active compounds (except naringenin and rutin) were reported in Spain originated Cistus sp.
545
pollen (Maruyama, Sakamoto, Araki, & Hara, 2010). On the other hand, the apigenin, catechin,
546
epicatechin, kaempferol, luteolin, naringenin, rutin, and quercetin were detected in bee pollen
547
from Egypt (Mohdaly, Mahmoud, Roby, Smetanska, & Ramadan, 2015). The bee pollen of
548
Echium plantagineum from Spain possessed the glucosides of anthocyanins, delphinidin,
549
petunidinm, and malvidin (Sousa, Andrade, & Valentão, 2016). Silva, Rosa, and Vilas-Boas
550
(2009) reported isorhamnetin-3-O-(6″-O-E-p-coumaroyl)-β-D-glucopyranoside, for the first
551
time, in pollen collected by Melipona rufiventris – the stingless bee. Bee pollen usually contains
552
the following phenolic acids and their ester derivatives: caffeic, p-coumaric, ferulic, p-
553
hydroxybenzoic, gallic, protocatechuic, syringic, and vanillic acid. de Florio Almeida et al.
554
(2017) and Negri et al. (2011) revealed the complex rosmarinic acid dihexoside and amide
555
derivatives of hydroxycinnamic and ferulic acids while Karabagias, Karabagias, Gatzias, and
556
Riganakos (2018) reported the presence of isopimpinellin (furancoumarins), urolithin B
557
(hydroxycoumarins) and flavononols 3-O- or 7-O-glucosides (quercetin 3-O-rhamnosyl24
558
galactoside, quercetin 3-O-xylosyl-glucuronide, isorhamnetin-3-O-glucoside 7-O rhamnoside,
559
and quercetin 3-O-rutinoside) in commercial Greek pollen.
560
Polyphenolic compounds in bee pollen protect from biotic (microbial growth) and abiotic
561
(high temperature, synthesis of reactive oxygen species and UV radiation) stress by their
562
capacity to neutralize the free radicals. Polyphenol metabolism includes the breaking of
563
flavonoids into monomeric units in the stomach. Sometimes, in the small intestine, few flavonoid
564
glycosides would be absorbed as whole by Na-dependent glucose transporter 1 (SGLT1)
565
(Williamson, 2017). The flavonoids are mainly metabolized in the small intestine due to the
566
existence of metabolizing enzymes like lactase phlorizin hydrolase, broad-specific-β-
567
glucosidase, and UDP-glucuronosyl transferase which produce the metabolites like sulfates,
568
glucuronides, and O-methylated aglycones including epicatechin, hesperetin, luteolin,
569
naringenin, and quercetin (Rzepecka-Stojko et al., 2015). These metabolites enter the liver
570
through membranes of the small intestine resulting in multiple positive health effects. The
571
remaining absorption of flavonoids carries in colon containing gut microflora based enzymes
572
which would decompose the flavonoids into phenolic acids (Li et al., 2018). Being simpler in
573
structures, the phenolic acids are easily metabolized or absorbed in the liver. However, the
574
metabolism of polyphenols is quite unclear and further research work must be conducted
575
focusing the polyphenol metabolism in humans.
576
3.2.9. pH and titratable acidity
577
pH and titratable acidity are critical factors during pollen storage because they can
578
influence the stability and shelf life. Both values also indicate the dynamic microbial activity in
579
food (Nogueira, Iglesias, Feás, & Estevinho, 2012). The increased levels of pH and titratable
580
acidity in food are caused due to fermentation, particularly by Gram-positive bacteria. The pH
581
value varied from 3.49-6.33 showing the natural slightly acidic nature of bee pollen. Portuguese, 25
582
Greek, and Indian bee pollen had almost similar pH values of 4.3-5.2, 4.70, and 4.74-5.48,
583
respectively (Feás et al., 2012; Karabagias, Karabagias, Gatzias, & Riganakos, 2018; Thakur &
584
Nanda, 2018a). However, the free acidity ranged from 128-294 meq/kg which exhibited the
585
acidic character of Brazilian bee pollen (Martins, Morgano, Vicente, Baggio, & Rodriguez-
586
Amaya, 2011) while Colombian bee pollen contained 155 – 402 meq/kg free acidity (Fuenmayor
587
et al., 2014) which provides information regarding conversion of sugars into organic acids.
588
However, the free acidity was not acclaimed by Campos et al. (2008) as a product quality index
589
Furthermore, no substantial pH (4.11) and titratable acidity (256.9 meq/kg) difference
590
was caused while drying (60 °C) the pollen compared to fresh bee-pollen (pH- 4.16; titratable
591
acidity-245.6 meq/kg) but difference was significant for both variables when drying was carried
592
out at 40°C (pH - 4.02; acidity - 305.8 meq/kg) and 50 °C (pH - 4.04; acidity - 283.2 meq/kg).
593
This recommends that the temperatures below 60 °C may support some microbial activity that
594
raises titratable acidity and decreases pH values owing to their metabolic action (Zuluaga-
595
Domínguez, Serrato-Bermudez, & Quicazán, 2018).
596
4. Functional properties
597
The functional properties refer to the attribute(s) of food components or ingredients
598
except for its nutritional value which affects its utilization (Thakur & Nanda, 2018b). These
599
properties affect the finished product in terms of appearance, taste, and texture and consequently,
600
acceptance of the product. Bee pollen is typically multi-component colloidal system, made up of
601
biopolymers and a variety of particles, such as oil droplets, gaseous bubbles, lipid crystals, etc.
602
The nature and strength of interactions of active surface components with themselves and
603
other pollen compounds (lipids, ash, and carbohydrates) affect the properties of pollen system
604
(Dickinson, 2013). Bee pollen is known to have outstanding emulsifying characteristics, higher 26
605
carbohydrate solubility, and oil retention capacity. However, variation in pollen composition
606
owing to diverse botanical and geographical origin may alter the functional properties. Recently,
607
the addition of bee pollen in different food products, as reported in few studies, was successful
608
efforts for processing the pollen (Krystyjan, Gumul, Ziobro, & Korus, 2015; Zuluaga et al.,
609
2016; Conte, Caro, Balestra, Piga, & Fadda, 2018; Thakur & Nanda, 2019). However, its role as
610
a functional component in the food industry relies on the pollen functional characteristics which
611
therefore must be discussed in detail.
612
4.1. Solubility
613
The dissolution ability of any substance in water, called as solubility followed the
614
following process: (1) wettability of product, (2) disintegration of product into primary particles,
615
(3) material discharge from particles into the aqueous phase and consistent destruction of surface
616
layer simultaneously until the complete particle breakdown and (4) thorough dissolution of all
617
materials (Mimouni, Deeth, Whittaker, Gidley, & Bhandari, 2010).
618
Bee pollen has solubility ranging from 84.91-87.56 % which is majorly influenced by
619
nature and composition of protein and carbohydrates based on proportion between soluble (e.g.
620
salivary secretions, simple sugars, lower molecular weight proteins (50–25 kDa), vitamins, etc.)
621
and insoluble (e.g. cellulose, lignin, sporopollenin, lipids, higher molecular weight proteins, etc.)
622
constituents and corresponding interlinkages (Kostic et al., 2015a; Thakur & Nanda, 2018b). The
623
pollen protein and carbohydrate solubility varied between 2.8 – 25.9% and 31.2 – 75%,
624
respectively (Kostic et al., 2015a). Protein solubility in pollen is similar to commercial
625
concentrated and isolated soy protein flours and also affects the other functional properties like
626
emulsification, foaming, and gelation (Kostic et al., 2015a). It is positively correlated to the
627
carbohydrates level however; the lipid and ash contents adversely affect the protein solubility. It
628
is also associated with the protein composition, conformation, their interaction with other 27
629
constituents and processing conditions. Kostic et al. (2015a) reported the three limits viz. higher
630
(80-50 kDa), moderate (50-25 kDa) and lower range (25-10 kDa) molecular weight proteins
631
which accounted for 13.40-32.20, 22.20-43.60 and 32.90-63.40% of soluble proteins (Kostic et
632
al., 2015a). The higher levels of 80-50 kDa molecular weight proteins were reported to
633
negatively affect the protein solubility. Compared to protein solubility, the carbohydrate
634
solubility was higher in bee pollen due to the presence of nectar (comprising mainly water-
635
soluble sugars), starch and pectin and it can be affected by the proportion of soluble and
636
insoluble carbohydrates and their association with other components. The correlation test showed
637
the positive association of protein and lipid content with carbohydrate solubility (Kostic et al.,
638
2015a).
639
Another important factor affecting solubility is wettability and dispersibility which were
640
examined by Thakur and Nanda (2018b) and varied between 285.67-1,909.46s and 34.10 –
641
51.06%, respectively. The enormous difference in pollen wettability and dispersibility is caused
642
due to pollen chemical constituents, surface area properties, variation in cultivar, and
643
arrangement, texture, and configuration of each pollen grains. The correlation studies by Thakur
644
and Nanda (2018b) exhibited a strong negative relationship between the surface area and
645
wettability of bee pollen.
646
4.2. Water and oil holding capacity (WHC)
647
It is essential for products where the retention of moistness is associated with quality.
648
Food ingredients that have high WHC may make the product dry and brittle, mainly during
649
storage. WHC of bee pollen ranged from 0.47-2.25 g/g and this difference in WHC is mainly due
650
to hydrophilic components such as polar groups of insoluble proteins and carbohydrates which
651
are reported in 3-D structures and correspondingly bind the water molecules through capillary 28
652
action (Kostic et al., 2015a; Thakur & Nanda, 2018b). Further, the lipid molecules which have
653
polar and charged regions may account for improved water holding. Therefore, variation in the
654
composition of protein, carbohydrate, and lipid indicates the significant differences in WHC of
655
pollen.
656
Oil holding capacity (OHC) is the degree of physical capture of oil by food constituents
657
on the grounds of composite capillary-attraction process and ranged from 1.00–3.53 g/g in bee
658
pollen (Kostic et al., 2015a; Thakur & Nanda, 2018b). Thakur and Nanda (2018b) revealed the
659
strong correlation between OHC and cohesiveness of bee pollen. OHC is affected by several
660
inherent variables like amino acid composition, hydrophobicity and protein conformation.
661
Further, the sporopollenin is structurally similar to fatty acid-lignin-like material entangles the
662
oil in the matrix thus contributing to OHC. The higher value of OHC in any product would
663
enhance its applications. Thakur and Nanda (2018b) recommended the coconut pollen to
664
improve mouthfeel and retain the flavor which showed its probability to utilize in different
665
formulations as a functional component.
666
WHC to OHC ratio, (known as water-oil holding index - WOHI) reveals the equilibrium
667
between hydrophilic and lipophilic constituents of pollen and is lower than 1 which indicates its
668
superior lipophilic properties. Moreover, no correlation of WHC or OHC was obtained with
669
other functional properties and carbohydrates, lipids or protein contents which demonstrate the
670
complexity of interactions among them (Kostic et al., 2015a; Thakur & Nanda, 2018b).
671
4.3. Emulsifying properties
672
Emulsion usually provides the desired mouthfeel and is essential in the structural
673
development of foods such as frozen desserts, beverages, coffee whiteners, mayonnaise, etc.
674
(Serdaroğlu, Öztürk, & Kara, 2015). Emulsifying properties of bee pollen including emulsion
675
activity and stability ranged from 44.83-46.76 % and 21.62-26.32 %, respectively (Thakur & 29
676
Nanda, 2018b). The emulsifying properties are influenced by amount, conformation,
677
hydrophobicity, and solubility of proteins; size and distribution of liquid droplets; phase volume
678
ratio; pH, temperature and salt level of solvents and continuous phase viscosity (Avramenko,
679
Low, & Nickerson, 2013). The correlation studies by Kostic et al. (2015a) reported the
680
significant positive association between emulsion stability and protein solubility while emulsion
681
activity was negatively linked to protein solubility. The protein with molecular weight 50-25 kDa
682
account for the emulsion stability while higher molecular weight proteins are negatively linked
683
thus indicating that oil/water interface can adsorb smaller protein molecules better to produce
684
stronger interfacial layers compared to larger molecules (Kostic et al., 2015a). Further, emulsion
685
stability and activity shared a negative correlation due to stabler emulsions formation having
686
greater adsorbed substances at the interface.
687
Usually, natural food emulsifiers are proteins but polar lipids may have good potential for
688
better emulsifying properties. The interfacial material of oil/water emulsion is comprised of
689
proteins, phospholipids, monoglycerides, esters of lipid acids, or mixture thereof. All these
690
compounds are present in pollen but in varying proportions due to plant sources (Liang, Zhang,
691
Shu, Liu, & Shu, 2013). Further, pollen contains bioelements like K, Ca and other complex
692
carbohydrates that blend with interfacial compounds to create either stabilization or
693
destabilization properties. Hence, the main reason for lower coefficient values of associations of
694
pollen emulsion activity/stability with protein solubility is the surface-active elements and their
695
interactions (Kostic et al., 2015a).
696
4.4. Foaming properties
697
Foam refers to the systems which are formed by entrapping the gas molecules in large
698
amount inside the thin film of liquid or solid. Several food products like bread, cakes, ice-cream,
699
and whipped toppings are dependent on the foam to maintain the structure and texture. The 30
700
retention of foam in the definite state is a tough task than emulsions due to the different
701
microstructure of foam bubble and its surroundings than an emulsion droplet (Green, Littlejohn,
702
Hooley, & Cox, 2013).
703
The bee pollen from Serbia did not possess any foam producing capacity while the Indian
704
bee pollen had foam capacity and stability ranged from 6.21-8.69 % and 17.50-20.00 % (Kostic
705
et al., 2015a; Thakur & Nanda, 2018b). Foaming capacity is strongly associated with proteins
706
that can reduce the water-air interface surface tension and produce a constant cohesive film
707
within the foam surrounding the air bubbles (Kaushal, Kumar, & Sharma, 2012). Thakur and
708
Nanda (2018b) recommended the use of Indian bee pollen in foam derived formulations such as
709
marshmallows, cakes, ice-creams, mousses, whipped cream, etc., whereas Kostic et al. (2015a)
710
suggested the pollen utilization as a foam depressant.
711
5. Food applications of bee pollen
712
Owing to its well-recognized nutritional and therapeutic properties, bee pollen is usually
713
consumed as a natural dietary supplement either in fresh or dried form. Recently, the researchers
714
have focused to utilize the bee pollen in food systems, not only as a nutritious ingredient but also
715
as a functional component to enhance the product quality characteristics. Yerlikaya (2014)
716
incorporated the bee pollen into fermented milk beverages and reported that antimicrobial
717
activity was exhibited by pollen when added in range 10-20 mg/mL. The supplementation of
718
fermented beverages with pollen also enhanced the probiotic viability and beverage viscosity
719
without affecting the sensorial attributes. Similarly, acidophilus milk and probiotic yoghurt were
720
also enriched with bee pollen (0.6% w/w) wherein the lactic acid production was increased,
721
regardless of fat level (Glušac, Stijepić, Milanović and Đurđević-Milošević, 2015). The use of
722
bee pollen in bakery products is trending where Krystyjan, Gumul, Ziobro and Korus (2015) had 31
723
fortified the biscuits and Conte, Del Caro, Balestra, Piga and Fadda (2018) supplemented the
724
gluten-free bread using bee pollen. Wheat flour when substituted with 10% bee pollen, the
725
prepared biscuits contained significantly increased levels of protein, sugar, ash, fiber
726
polyphenols, and antioxidant potential; however, 5% of pollen was needed to provide taste
727
similar to the control samples of biscuits (Krystyjan, Gumul, Ziobro and Korus, 2015). On the
728
other hand, Conte, Del Caro, Balestra, Piga and Fadda (2018) showed an improvement of
729
techno-functional properties, decreased rate of staling, and an increase in overall organoleptic
730
acceptability of bread without any destruction to dough development and leavening attributes
731
when enriched with bee pollen from 3-5%. These studies can provide a base for further
732
exploration of bee pollen as a promising ingredient in other bakery products.
733
Some recent studies recommended the bee pollen as a natural antioxidant substitute to
734
inhibit the fat oxidation in black pudding and refrigerated pork sausages which are attributed to
735
the increased antioxidant potential and higher levels of phenolic compounds (de Florio Almeida
736
et al., 2017; Anjos et al., 2019). Zuluaga et al. (2016) revealed an increase in bioactive
737
compounds, mainly carotenoids and antioxidant potential of pineapple juice under pressure (400
738
MPa for 15 min) whereas Karabagias, Karabagias, Gatzias, and Riganakos (2018) reported an
739
increase in total phenolic content and antioxidant capacity of bee pollen yogurt in addition to
740
improvement of end product cohesion and organoleptic characteristics. Similarly, Thakur and
741
Nanda (2019) developed the polyphenol-rich vacuum-dried milk powder using rapeseed bee
742
pollen which may have potential in the formulation of processed products as a functional
743
component. Further applications of bee pollen in food products are thus based on thorough
744
assurance about its nutritional value, bioactive compounds, techno-functionalities, organoleptic
745
attributes, and safety. There is also a need to compare the effect of adding the monofloral and 32
746
multifloral bee pollen to food products for better understanding the impact of botanical source on
747
product quality.
748
6. Safety aspects of bee pollen
749
Bee pollen intake is highly recommended as a natural dietary supplement on account of
750
its outstanding nourishing and healthy nutrients; however, few risks are also associated with its
751
intake due to the presence of potential contaminants like bacterial and fungal toxins, heavy
752
metals, pesticides, and allergic response. The poor and unhygienic production and storage
753
conditions of bee pollen may favor the microbial spoilage due to yeasts, molds, total viable
754
count, lactic acid bacteria and Enterobacteriaceae, which grows optimally at moderate
755
temperatures. This increases the health risk linked to intake of fresh pollen whereas the bee
756
pollen after drying are reported as microbiologically safe (Mauriello, De Prisco, Di Prisco, La
757
Storia, & Caprio, 2017). On exposing to the environment (anthropogenic pollution, water, and
758
soil), the bee pollen may accumulate toxic heavy metals. Several investigations reported the
759
presence of heavy metals like arsenic (As), cadmium (Cd), mercury (Hg), lead (Pb) and
760
strontium (Sr) (Roman, 2009; Kostić et al., 2015b; Dinkov & Stratev, 2016).
761
de Oliveira, do Nascimento Queiroz, da Luz, Porto, and Rath (2016) and Böhme,
762
Bischoff, Zebitz, Rosenkranz and Wallner (2018) reported the presence of 26 and 73 different
763
pesticides in bee pollen from Brazil and Germany, respectively. The exposure of pesticide-
764
contaminated bee pollen to humans may result in several chronic diseases like the neurological
765
deficit, respiratory diseases, cancer, etc. (Mesnage & Seralini, 2018). The mycotoxin
766
contamination is a greater concern where ochratoxin A is among the hazardous toxic substances
767
generated by Aspergillus (Bogdanov, 2017). Echium vulgare, Symphytum officinale, and Senecio
768
jacobaea bee pollen reported the pyrrolizidine alkaloids associated with hepatotoxic 33
769
characteristics (Kempf et al., 2010). Moreover, allergic reactions including anaphylaxis are
770
usually the immediate IgE-mediated hypersensitivity reactions which are identified after pollen
771
intake because individual pollen grains are collected from insect-pollinated plants as well as
772
wind-pollinated weeds or trees which may cause the allergic reactions due to accidental intake of
773
airborne pollens (Makris et al., 2010; Jagdis & Sussman, 2012; Choi, Jang, Oh, Kim, & Hyun,
774
2015). Recently, McNamara and Pien (2019) reported the relation of exercise-induced
775
anaphylaxis with pollen consumption in atopic individuals due to the reduction of threshold for
776
mast cell degranulation during exercise on account of enhanced gastrointestinal permeability or
777
osmotic effects and recommended that such individuals after pollen intake should skip exercise
778
for 4 -6 hours. Taking everything into account, it may be said that primary risks behind allergy of
779
bee pollen are blending of bee pollen with airborne-pollen allergens, fungal cross-reactive
780
allergenic substances, contamination with pesticides and exercise quickly after its intake.
781
Various international organizations such as WHO, FAO, and WTO - World Trade
782
Organization are responsible for establishing food quality and safety standards; however, there
783
are no harmonized global standards for bee pollen safety to date. A few countries like Argentina,
784
Bulgaria, Brazil, and Poland have established their guidelines for improving the quality
785
surveillance of pollen to increase safety. There is an urgent need to revise the bee pollen
786
guidelines by evaluating the botanical source, maximum residue limits (MRL) for heavy metals
787
and pesticides, microbial load and processing techniques before introducing the bee pollen in the
788
market. Further, labeling of bee pollen and any food containing bee pollen should include the
789
allergenic risk statements to avoid the risks for allergic individuals. Legal requirements also need
790
to be established and adapted for processing systems from the farm scale to pilot scale industries,
34
791
producers, and bee pollen processing stages. Moreover, effective training of beekeepers is very
792
much necessary by competent authorities so that the safety of bee pollen can be ensured.
793
7. Future trends
794
The research work on characterizing the bee pollen, based on physico-chemical and
795
functional properties, has been increased rapidly from the last 5 years. This may be due to the
796
huge demand for natural and healthy dietary supplements like bee pollen. Moreover, the use of
797
geographical index has further enhanced the horizon of bee pollen global market particularly for
798
properly analyzed distinct bee pollen from botanical source and geographical origin. The plenty
799
of pollen studies are focused in Brazil, Colombia and Romania attributed to their botanical
800
diversity. However, bee pollen is still a new term in many developing countries where even the
801
beekeepers are unaware of its potential as healthy food or functional ingredient or dietary
802
supplement. Therefore, the food industries, governments, and private organizations should come
803
forward to encourage the beekeepers to harvest the bee pollen which must be properly examined
804
for their properties before using in food processing. Further, the comprehensive composition of
805
bee pollen should be examined with a focus on the botanical and geographic origins using the
806
novel and advanced techniques with higher sensitivity, resolution, and accuracy. However, the
807
determination of functional properties of bee pollen is essential for its valorization. Only a few
808
studies have been reported in the literature highlighting the functional characteristics, however,
809
these properties are also affected by the botanical diversity and location. Therefore, scientists and
810
researchers must pay attention to study the mono-floral bee pollen which has a unique
811
composition. Also, there is a strong need to carry more research work to identify the mono-floral
812
pollen up to species level which is necessary for establishing the international quality parameters
813
of bee pollen. 35
814
8. Conclusion
815
Bee pollen as per nutritional and physico-chemical composition is an excellent source of
816
vital amino acids, ω-3 fatty acids, B-complex vitamins, minerals, and polyphenols; however, the
817
huge variation in composition due to the different botanical and geographical origin is still a
818
challenge to promote the bee pollen market. Proteins and its composition followed by lipid
819
characterization are mostly studied by the scientists and researchers with a mere focus on the
820
functional properties. Summarizing the data, bee pollen exhibited significant differences in
821
nutritional and physico-chemical composition as well as functional properties. Emphasis should
822
be given to study the mono-floral pollen of varying geographical and plant sources for
823
establishing their uniqueness as well as safety in the diet. Further intensive research should be
824
conducted to enrich the diversity of bee pollen for promoting its application in food processing
825
industries.
826
Acknowledgements
827
The authors thankfully acknowledge Mr. Rishi Ravindra Naik and Ms. Kirty Pant from
828
Department of Food Engineering and Technology, Sant Longowal Institute of Engineering and
829
Technology, Longowal (Punjab) India for assisting in modifying the corrections.
830
Conflicts of interest
831
The authors declare that there are no conflicts of interest.
832
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1433
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1434 1435
Ulusoy, E., & Kolayli, S. (2014). Phenolic composition and antioxidant properties of Anzer bee pollen. Journal of Food Biochemistry, 38(1), 73–82. https://doi.org/10.1111/jfbc.12027.
1436
Vasconcelos, M. R. D. S., Duarte, A. W. F., Gomes, E. P., Silva, S. C. D., & López, A. M. Q.
1437
(2017). Physicochemical composition and antioxidant potential of bee pollen from
1438
different botanical sources in Alagoas, Brazil. Ciência e Agrotecnologia, 41(4), 447-458.
1439
http://dx.doi.org/10.1590/1413-70542017414009317.
1440
Verslues, P. E., & Sharma, S. (2010). Proline metabolism and its implications for plant-
1441
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1442
e0140. https://doi.org/10.1199/tab.0140.
1443
Wang, R., & Dobritsa, A. A. (2018). Exine and aperture patterns on the pollen surface: Their
1444
formation and roles in plant reproduction. In J. A. Roberts (Ed.). Annual Plant Reviews.
1445
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Weiner, C. N., Hilpert, A., Werner, M., Linsenmair, K. E., & Blüthgen, N. (2010). Pollen amino
1447
acids
1448
https://doi.org/10.1051/apido/2009083.
1449 1450
1451 1452
and
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specialisation
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bees.
Apidologie,
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476–487.
Williamson, G. (2017). The role of polyphenols in modern nutrition. Nutrition bulletin, 42(3), 226–235. https://doi.org/10.1111/nbu.12278. World Health Organization (WHO). 2012. Guideline: Sodium intake for adults and children. Geneva: World Health Organization (WHO).
1453
Xu, X., Sun, L., Dong, J., & Zhang, H. (2009). Breaking the cells of rape bee pollen and
1454
consecutive extraction of functional oil with supercritical carbon dioxide. Innovative
1455
Food
1456
https://doi.org/10.1016/j.ifset.2008.08.004.
Science
&
Emerging
Technologies,
10(1),
42-46.
1457
Yang, K., Wu, D., Ye, X., Liu, D., Chen, J., & Sun, P. (2013). Characterization of chemical
1458
composition of bee pollen in China. Journal of Agricultural and Food Chemistry, 61(3),
1459
708-718. https://doi.org/10.1021/jf304056b.
1460
Yerlikaya, O. (2014). Effect of bee pollen supplement on antimicrobial, chemical, rheological,
1461
sensorial properties and probiotic viability of fermented milk beverages. Mljekarstvo,
1462
64, 268-279. https://doi.org/10.15567/mljekarstvo.2014.0406
1463
Zhang, Y., Yang, F., Jamali, M. A., & Peng, Z. (2016). Antioxidant enzyme activities and lipid
1464
oxidation in Rape (Brassica campestris L.) bee pollen added to salami during processing.
1465
Molecules, 21(11), 1439. https://doi.org/10.3390/molecules21111439.
66
1466
Zhou, J., Qi, Y., Ritho, J., Zhang, Y., Zheng, X., Wu, L., ... & Sun, L. (2015). Flavonoid
1467
glycosides as floral origin markers to discriminate of unifloral bee pollen by LC–
1468
MS/MS. Food Control, 57, 54-61. https://doi.org/10.1016/j.foodcont.2015.03.035.
1469
Zuluaga, C., Martínez, A., Fernández, J., López-Baldó, J., Quiles, A., & Rodrigo, D. (2016).
1470
Effect of high pressure processing on carotenoid and phenolic compounds, antioxidant
1471
capacity,
1472
beverage. Innovative
1473
https://doi.org/10.1016/j.ifset.2016.07.023.
and
microbial Food
counts
of
Science
bee-pollen &
paste
Emerging
and
bee-pollen-based
Technologies, 37,
10-17.
1474
Zuluaga-Domínguez, C., Serrato-Bermudez, J., & Quicazán, M. (2018). Influence of drying-
1475
related operations on microbiological, structural and physicochemical aspects for
1476
processing of bee-pollen. Engineering in Agriculture, Environment and Food, 11(2), 57-
1477
64. https://doi.org/10.1016/j.eaef.2018.01.003.
1478 1479 1480 1481 1482 1483 1484 1485 1486 1487 1488 67
1489
Table 1
1490
Average bee pollen composition and nutritional requirements as Required Daily Intake (RDI).
Nutrients
1491 1492 1493 1494 1495
Amount (%)
Average RDI
% RDI for 50 g of bee pollen
Carbohydrates (Fructose, 13-55 320* 3.33-15.34 glucose, sucrose, fibre) Crude fibre 0.3 – 20 30* 1.00-60.03 Protein 10 – 40 50* 18.01-73.37 Fat 1 – 13 80* 0.33-13.34 † # Potassium 400 – 2000 2000 16.68-90.04 Phosphorus 80 – 600† 1000# 6.67-53.36 † # Calcium 20 – 300 1100 1.67-23.34 350# 6.67-76.71 Magnesium 20 – 300† Zinc 3 – 25† 8.5# 33.35-263.46 Manganese 2 – 11† 3.5# 50.02-283.47 Iron 1.1 – 17† 12.5# 6.67-123.39 Copper 0.2 – 1.6† 1.2# 13.34-120.06 0.9# 100.05-2001 β-Carotene 1 – 20† Tocopherol 4 – 32† 13# 26.68-220.11 Niacin 4 – 11† 15# 23.34-66.70 † # Pyridoxine 0.2 – 0.7 1.4 13.34-43.35 1.1# 50.03-106.72 Thiamine 0.6 – 1.3† Riboflavin 0.6 – 2† 1.3# 40.02-140.07 Pantothenic acid 0.5 – 2† 6# 6.67-30.02 Folic acid 0.3 – 1† 0.4# 66.7-223.45 Biotin 0.05 – 0.07† 0.045# 100.05-140.07 100# 6.67-50.025 Ascorbic acid 7 – 56† Bee pollen composition is according to Campos et al. (2008) and RDI are according to the Reports of the Scientific Committee for Food (2010) and Denisow and Denisow-Pietrzyk (2016). † : Amount is given in mg/100g *: RDI is given in g/day #: RDI is given in mg/day
68
1496
Table 2
1497 1498
Summary of studies on physico-chemical properties of bee pollen from different botanical origins throughout the world and International standards for bee pollen quality. Country
Botanical source
Worldwide Literature Reports Italy Hedera helix L, Cistus incanus, Cornus sanguinea L., Cruciferae Brassica, Castanea sativa Miller, Lamiaceae L form, Fraxinus ornus L, Helianthus annuus, Papaver rhoeas L., Crataegus monogyna Jacq., Prunus, Rubus ulmifolius Schott, Gleditsia triacanthos L., Hedysarum coronarium, Trifolium alexandrinum, and Coriandrum sativum (n=32, dried pollen) Turkey (n=1, fresh and dried pollen)
Chemical composition LP CF (%) TM (%) (%)
MC (%)
CHO (%)
PT (%)
–
–
13.60 40.70
–
–
8.8028
61.96 78.70
12.43 30.36
5.50 7.22
–
69
References pH
aw
–
–
–
Castiglioni et al. (2019)
2.142.18
–
–
Isik, Ozdemir, & Doymaz (2019)
Greece
Erica manipuliflora, – Morus sp., Robinia pseudoacacia, Eucalyptus sp., Vicia sp., Phacelia tanacetifolia, Trifolium sp., Zea mays, Platanus sp., Pinus sp., Eryngium campestre, Erica arborea, Ranunculus sp., Laurus nobilis, Chenopodium sp., Helianthus annuus, Acer sp., Actinidia chinensis, Veronica persica, Convolvulus arvensis, Lamium sp., Salix sp., Polygonum aviculare, Centaurea calcitrapa, Cistus sp., Olea europaea, Papaver rhoeas, Portulaca oleracea, Hedera helix, Verbascum sp., Centaurea sp., Asphodelous sp., Aesculus hippocastanum, Amorpha fruticosa, Inula viscosa,
–
–
1.15 13.6 0
70
–
–
–
–
Liolios et al. (2019b)
Slovenia
Brazil
centaurea solstitialis, Pyrus communis, Pastinaca sativa, Chondrilla juncea, Cirsium sp., Cichorium intybus, Brassica napus, Brassica nigra, Taraxacum officinale, Sisymbrium irio, and Echinops ritro (n=46, fresh pollen) 14.80Brassicaceae, Castanea sativa, 32.10 Hedera helix, Fagopyrum esculentum, and multi-floral (n=28, fresh pollen) Mimosa caesalpiniifolia, Eucalyptus, Rubiaceae, Astrocaryum aculeatissimum, C. nucifera, M. verrucosa, Myrcia, Alternanthera, Asteraceae,
–
–
–
–
10.1021.37
–
–
–
Bertoncelj et al. (2018)
54.90 – 82.80
7.90– 32.20
3.20 – 13.5 0
–
1.90– 3.60
–
–
de Melo et al. (2018a)
71
Columbia, Italy and Spain
Greece
Anadenanthera, and Brassica asmonofloraland other multi-floral samples (n=56, dried pollen) Alternanthera, Anadenanthera; Cocos nucifera; Mimosa caesalpiniaefolia; Myrcia; Mimosa scabrella, Mimosa scabrella and Mimosa scabrella (n=8, dried pollen) (n=25, fresh pollen)
–
Multi-floral (n=3, commerical pollen)
14.9015.50
Commerical bee pollen (Papaver rhoes, Chamomila recutita, Sinapis arvensis, Cistus sp., Trifolium sp., Dorycnium sp., Cichorium sp., Convolvulus sp., Circium sp., Malva sylvestris, Fumana
–
–
–
10.60 33.90
3.20 8.30
–
2.603.80
–
–
de Melo et al. (2018b)
18.50 4.509.90 45.00 37.70 14-24 44.10 61 17.60
2-6
–
–
4.90-5.90
–
2.50 -6
–
1.802.10
–
–
7
8.40
2.28
4.70
–
Duarte, Vasconcelos, Oda-Souza, Oliveira, & López (2018) Gardana, Del Bo, Quicazan, Corrrea, & Simonetti (2018) Karabagias, Karabagias, Gatzias, & Riganakos (2018)
72
Brazil
Romania
India
Brazil
Republic
sp., Eucalyptus camaldulensis, Anemone sp., Ononis sp., Asphodelus sp., Quercus ilex) (n=1, commercial pollen from Attiki Bee Culturing Co.-Alex Pittas S.A., Athens, Greece) Cocos nucifera (n=1, 24.40* dried pollen) Brassica sp, 16.92Carduus sp., 31.08 Helianthus annuus, Prunus L. sp., Crataegus monogyna and bifloral and multifloral (n=10, fresh pollen) Cocos nucifera, 12.72Coriandrum 19.59 sativum, Brassica napus and Multifloral (n=35, fresh pollen) Commercial bee 3.06pollen (n=62, dried 8.12 pollen) Actinidia arguta and
4.4-
–
13.15
2.70
–
2.54
4.00
–
23.31 48.63
13.16 24.14
1.33 5.47
–
1.342.81
–
–
46.16 42.33
19.63 25.39
7.14 12.3 8
3.054.31
2.273.45
–
15.49 34.73
–
1.914.61
–
–
de Arruda et al. (2017)
–
23.2-
3.25 10.9 6 7.0-
3.1-4.2
5.2-5.3
–
–
Ghosh and Jung
73
Negri, Barreto, Sper, Carvalho, & Campos (2018) Spulber et al. (2018)
4.74-5.48 0.39-0.47 Thakur and Nanda (2018a)
of Korea Italy
Brazil
Quercus (n=2, dried pollen) Rubus, Cistus, Castanea, and Hedera (n=5, fresh pollen) (n=2, dried pollen)
Eucalyptus, Asteraceae, Mimosa caesalpiniaefolia,Pip er, Elephantopus, Cyperaceae and Anacardiaceae (n=4, dried pollen) (n=21, fresh pollen) Italy
Serbia
Brazil
13.8
26.5
4.5
(2017)
8.529.5
44.861.3
21.328.7
0.91 -2.2
–
1.9-3.0
–
–
Sagona et al. (2017)
37.1253.39*
25.66 44.27
24.00 37.63
9.3013.65
2.744.03
3.343.70*
0.850.91*
Rebelo, Ferreira, & Carvalho-Zilse (2016)
–
–
8.311.4
6.47 10.8 1 6.68.2
–
–
–
–
de Melo et al. (2016)
36.0± 2† 10.7512.03
–
21±2
–
3.6±1. 4† –
4.9±0. 3† 2.552.85
3.49±0.0 4† –
0.86±0.0 2† –
Bárbara et al. (2015)
–
1.183.32
–
–
Kostic et al. (2015a)
-
1.7-2.3
–
–
Sattler et al. (2015)
Castanea, Rubus and Cistus (n=3, fresh pollen) Brassicaceae, Salix, 4.35Fabaceae and multi- 14.35 floral samples (n=3, fresh pollen) Andira, Rubiaceae, 16.1Asteraceae, 18 Mimosaceae, (fresh) Fabaceae, and Aquifoliaceae, 2.8Anacardiaceae, 3.6 Myrtaceae, (dried)
†
54.84 57.98 64.42 81.84
25.87 28.42 14.81 27.25
1.92 2.83 1.31 6.78
–
15.322.9
1.93.9
74
Gabriele et al. (2015)
Saudi Arabia
Colombia India, China, Romania, Spain, Bulgaria, Hungary and Poland
Brazil
Caesalpineaceae, Brassicaceae, and others (n=21, dried pollen) Cucurbita pepo Thunb, Phoenix dactylifera, Helianthus annuus., Brassica napus and Medicago sativa (n=5, dried pollen) Multi-floral (n=196, dried pollen)
Commercial bee pollen (n=9, commercial pollen)
Bee pollen samples collected during summer, spring, autumn and winter (n=48, dried pollen) Arecaceae, Cecropia, Cestrum, Cyperaceae, Eucalyptus, Ilex, Myrcia, Piper, Vernonia, and Trema (n=7, dried pollen)
9.1610.5
14.71 19.45
1.82 5.38
0.151.70
1.883.88
–
–
–
16.132.1
2.89.7
7.818.1
1.5-3.2
3.8 -5.4
–
2.09.1
–
15.826.1
4.98.0
4#
–
18.66 24.39
3.163.99
–
22.15 25.11
1.811.8
–
Taha (2015)
Fuenmayor et al. (2014)
8-14.5
1.5-4.3
4.3-5.4
–
2.26 4.95
1.814.05
–
–
–
Negrão et al. (2014)
4.57 6.13
–
2.773.24
–
–
de Arruda, Pereira, de Freitas, Barth, & de AlmeidaMuradian (2013a)
75
China
Egypt
Thailand
Portugal
Brassica napus, Citrullus lanatus, Camellia japonica, Dendranthema indicum, Fagopyrum esculentum, Helianthus annuus,Nelumbo nucifera Gaertn, Papaver rhoeas, Rosa rugosa, Schisandra chinensis, Vicia faba, and Zea mays (n=12, commercial pollen from Zhenzhou Kerun Apiculture Co., Ltd., Zhenzhou, Henan Province, People's Republic of China) Zea mays, Trifolium alexandrinum, and Phoenix dactylifera (n=3, fresh pollen) Z. mays (n=1, dried pollen) Multi-floral (n=10, dried pollen) Cistus and Multi-floral including
other
1.827.52
59.43 77.82
14.26 28.95
0.66 6.56
17.6031.26
1.675.01
–
–
Yang et al. (2013)
11.9128.15
–
12.35 38.06
0.41 1.09
–
1.727.75
–
–
Khider, Elbanna, Mahmoud, & Owayss (2013)
7.03
64.42
19.12
7.00
0.86
2.43
–
–
4.336.67
–
2.313.99
61.270.6
2.60 3.32 4.36.3
–
–
24.23 34.18 19.127.1
–
2-4
4.3–5.2
0.210.54
76
Chantarudee et al. (2012) 4.33-6.33 0.32-0.55 Estevinho et al. (2012) Feás et al. (2012)
Romania
Portugal and Spain
France
Boraginaceae, Rosaceae, Fagaceae, Asteraceae, Fabaceae, Ericaceae, Mimosaceae and Myrtaceae (n=22, dried pollen) (n=16, fresh pollen)
Cistaceae, Fabaceae, Ericaceae, Fagaceae, and Boraginaceae (n=8, commercial pollen) Zea mays, Papaver, Sinapis, Sorghum, Helianthus, Daucus/Ammi, Cichorium, Brassica napus, Hypericum, Polygonum, Plantago, Veronica, Reseda, Platanus, Elaeagnus, Berberis, Viburnum, Aesculus, Laurus, Tamaris, Vicia, Onobrychis, Taraxacum,
16.27 2.13 -8.93 26.50
–
1.753.25
–
69.68 84.25
12.50 25.15
2.35 3.06
-
0.503.16
4.235.17
–
16.70 29.90
7.50 24.4 0
–
–
–
17.5929.55
–
6.028.40
–
77
Mărgăoan, Al. Mărghitaş, Dezmirean, Bobiş, & Mihai (2012) 0.26-0.43 Nogueira, Iglesias, Feás, & Estevinho (2012) –
–
Odoux et al. (2012)
Spain
Brazil
Fraxinus, Liliaceae, Ficaria and Quercus (n=52, fresh pollen) Cistus ladanifer, multifloral and commercial bee pollen (n=5, fresh and dried pollen) Commercial bee pollen samples (n=154, dried pollen)
Colombia
Dry and wet Multifloral samples (n=2, dried pollen) Brazil Asteraceae and other multi-floral pollen (n=36, dried pollen) Brazil Mimosa caesalpiniaefolia, Myrtaceae and other multi-floral (n=6, dried pollen) International Standards Argentina – Brazil
–
France
–
–
–
17.64 16.08
2.86 3.71
14.5014.65
–
–
3.009.39
–
12.28 27.07
–
1.334.13
–
5.5719.90
–
16.323.8
6.908.60
–
4.6364.830
3.454.85
–
–
–
–
1.502.99
–
18.55 22.60 19.98 28.28
4.01 13.3 2 5.36 6.69 4.59 5.07 4.53 5.69
–
2.893.30
–
–
de Melo, Freitas, Barth, & AlmeidaMuradian (2009)
<8 (dried) <4 (dried) <30 (fresh) <6 (dried)
–
15-28
–
–
<4
4-6
–
–
>8
>1.8
–
<4
–
–
Alimentos azucarados (2010) Instrução normativa N.º 3 (2001)
–
10-41
1-10
–
2-6
78
0.100.66
DomínguezValhondo, Gil, Hernández, & González-Gómez (2011) – Martins, Morgano, Vicente, Baggio, & Rodriguez-Amaya (2011) 0.27-0.72 Bobadilla (2009)
0.37-0.38 Carpes et al.(2009)
–
de Arruda, Pereira, de Freitas, Barth, & de Almeida-
1499 1500 1501 1502 1503
Mexico
–
4.5-8
–
12-18
Switzerla nd
–
<6 (dried)
–
10-40
2.56.5 1-10
–
1.5-2.2
>4
–
–
2-6
–
–
MC: Moisture content, CHO: Carbohydrates, PT: Proteins, LP: Lipids, CF: Crude Fibre, TM: Total minerals, aw: water activity *: Fresh bee pollen #
: Fixed moisture content
†
: Average value±standard deviation
1504 1505 1506 1507 1508 1509 1510 1511 1512 1513 1514 1515 79
Muradian (2013a) Fuenmayor et al. (2014) Lebensmittelverordn ung 817.02 (2005)
1516
Table 3
1517
Summary of sugars and amino acid composition (g/100g) of bee pollen from different botanical origins throughout the world. Sugars (g/100g)
Country
Slovenia
Botanical source Brassicaceae, Castanea sativa, Hedera helix, Fagopyrum esculentum, and multi-floral
References Glucose
Fructose
Sucrose
Maltose
11.94-28.49
13.17-26.48
0.05-0.28
0.16- 6.03
Bertoncelj et al. (2018)
Columbia, Italy and Spain
Multi-floral
14‒16
17.1
5‒6
–
Gardana, Del Bo, Quicazan, Corrrea, & Simonetti (2018)
Greece
Actinidia chinensis, Castanea sativa, Chenopodium album, Cichorium intybus, Cistus creticus, Convolvulus arvensis, Ecballium elaterium, Erica manipuliflora, Inula viscosa, Hedera helix, Lamium amplexicaule, Marticaria chamomilla, Oryza sativa, Papaver rhoeas, Parthenocissus inserta, Phacelia tanacetifolia, Pinus halepensis, Polygonum aviculare, Portulaca oleracea, Ranunculus arvensis, Robinia pseudoacacia, Rubus ulmifolius, Salvia verbenaca, Silybum marianum, Sisymbrium irio, Sonchus asper, Tamarix parviflora, Taraxacum officinalis, Tilia intermedia, and Tribulus
13.59-27.69
15.53-33.48
0.10-8.24
0.26-3.66
Liolios et al. (2018)
80
terrestris
2.77-20.90
8.08-25.71
–
–
de Arruda et al. (2017)
13.3-18.2
18.7-26.9
–
–
de Melo et al. (2016)
Brazil
Andira, Rubiaceae, Asteraceae, Mimosaceae, Fabaceae, Aquifoliaceae, Anacardiaceae, Myrtaceae, Caesalpineaceae, Brassicaceae, and others
6.3-7
4.9-5.5
–
–
Sattler et al. (2015)
Colombia
Multi-floral
11.6-20.3
4.5-9.0
–
Fuenmayor et al. (2014)
Thailand
Z. mays
6.42
0.60
0.53
Chantarudee et al. (2012)
Brazil
Colombia
Commercial bee pollen Eucalyptus, Asteraceae, caesalpiniaefolia, Piper, Cyperaceae and Anacardiaceae
Mimosa Elephantopus,
18.1-21.3
7.16
Romania
-
4.37-16.14
8.44-15.39
–
–
Mărgăoan, Al. Mărghitaş, Dezmirean, Bobiş, & Mihai (2012)
Spain
Cistus ladanifer and commercial multifloral bee pollen
22.47-26.86
19.88-23.78
3.04-8.55
–
DomínguezValhondo, Gil,
81
Hernández, & GonzálezGómez (2011)
Brazil
Commercial bee pollen
6.99-21.85
12.59-23.62
–
–
Martins, Morgano, Vicente, Baggio, and RodriguezAmaya (2011)
Colombia
Dry and wet Multi-floral
11.94-20.27
15.65-20.34
4.42- 9.02
–
Bobadilla (2009)
Amino Acids Essential amino acids Country
Botanical source
References Arg
Saudi Arabia
Colombia, Spain and Italy
His
Summer squash, date palm, rape 0.28- 0.32sunflower, and alfalfa 0.42 0.63
Multi-floral
0.96- 0.494.64 0.68
Ile
Leu
Lys
0.460.72
0.970.13
0.64- 0.040.89 0.07
0180.64
0.471.34
82
Met
0.39- 0.190.87 0.21
Phe
Thr
Trp
Val
0.120.31
0.400.52
0.050.12
0.830.99
Taha et al. (2019)
0.290.70
Gardana, Del Bo, Quicazan, Corrrea, & Simonetti (2018)
0.440.87
0.100.31
0.110.15
India
Cocos nucifera, Coriandrum 0.97- 0.35sativum, Brassica napus and Multi1.19 1.23 floral
Republic of Korea
Actinidia arguta and Quercus
Brazil
Senna sp, Chamaecrista sp Mimosa tenuiflora
China
Brassica napus, Citrullus lanatus, Camellia japonica,Dendranthema indicum, Fagopyrum esculentum, 0.72- 0.42and Helianthus annuus, 2.58 0.93 Nelumbo nucifera Gaertn, Papaver rhoeas, Rosa rugosa, Schisandra chinensis, Vicia faba, and Z. mays
and
0.381.01
1.762.47
1.35- 0.122.01 0.47
0.920.65
0.531.04
0.260.46
0.711.03
Thakur and Nanda (2018a)
0.21.2
0.40.9
–
0.91.4
Ghosh and Jung (2017)
1.11.5
0.40.6
0.91.3
1.5-2
0.71.2
0.03
0.07
0.010.02
0.06
0.03- 0.010.05 0.02
0.030.04
0.020.03
–
0.030.04
da Silva et al. (2014)
0.561.33
0.792.06
0.70- 0.121.55 0.62
0.461.30
0.430.99
0.7014.80
0.641.57
Yang et al. (2013)
Ser
Tyr
Asn
Gln
0.710.89
0.130.29
–
–
Taha et al. (2019)
0.090.23
Gardana, Del Bo, Quicazan, Corrrea, & Simonetti
-–
Non-essential amino acids Ala Saudi Arabia
Colombia, Spain and Italy
Asp
Summer squash, date palm, rape 1.13- 1.42sunflower, and alfalfa 1.35 1.65
Multi-floral
0.43- 0.211.19 0.46
Cys
Glu
Gly
0.120.24
1.321.84
1.47- 0.031.76 0.06
0.070.09
0.130.29
83
Pro
0.08- 16.20.25 19.8
0.230.47
0.360.89
0.290.49
(2018) Cocos nucifera, Coriandrum 1.59- 2.32sativum, Brassica napus and Multi2.33 2.81 floral
India
Republic of Korea
Actinidia arguta and Quercus
Brazil
Senna sp, Chamaecrista sp Mimosa tenuiflora
China
Brassica napus, Citrullus lanatus, Camellia japonica,Dendranthema indicum, Fagopyrum esculentum, 0.87- 1.13Helianthus annuus, Nelumbo 1.45 2.58 nucifera Gaertn, Papaver rhoeas, Rosa rugosa, Schisandra chinensis, Vicia faba, and Z. mays
1518 1519 1520
and
1.11.4
1.62.7
0.09
–
0.190.25
2.353.03
0.22- 2.081.84 2.52
0.520.91
0.360.44
–
–
Thakur and Nanda (2018a)
0.10.3
2.12.2
0.91.2
0.7
0.91.1
0.6
–
–
Ghosh and Jung (2017)
–
–
0.04
0.951.18
0.370. 43
0.030.04
0.080.10
0.020. 02
da Silva et al. (2014)
0.150.30
1.112.87
0.55- 0.951.25 5.95
0.511.25
0.280.85
–
–
Yang et al. (2013)
Arg: Arginine, His: Histidine, Ile: Isoleucine, Leu: Leucine, Lys: Lysine, Met: Methionine, Phe: Phenylalanine, Thr: Threonine, Trp: Tryptophan, Val: Valine, Ala: Alanine, Asp: Aspartic acid, Cys: Cysteine, Glu: Glutamic acid, Pro: Proline, Ser: Serine, Tyr: Tyrosine, Asn: Asparagine, Gln: Glutamine
84
1521
Table 4
1522 1523
Summary of mineral (mg/kg) and vitamins (mg/100g) composition of bee pollen from different botanical origins throughout the world.
Countr y
Minerals (mg/kg) Botanical source K
Ca
P
Mg
–
31827376
14013724
32576886
7891744
38- 76
Mimosa caesalpiniifolia, Eucalyptus, Rubiaceae, Astrocaryum aculeatissimum, C. nucifera, M. verrucosa, Myrcia, Alternanthera, Asteraceae, Anadenanthera, and Brassica as monofloral and other heterofloral pollen
34009800
9004100
–
6002400
30101
Alternanthera, Anadenanthera; Cocos nucifera; Mimosa caesalpiniaefolia; Myrcia; Mimosa scabrella, Mimosa scabrella and Mimosa scabrella
57009100
8003900
–
9002300
50.0899.0
Romani Brassica sp, Carduus sp., Helianthus annuus, Prunus L. a sp., Crataegus monogyna and
19804284
294.12437
–
286.120.211505 59.57
Brazil
Brazil
Brazil
85
Zn
Fe
–
Mn
Cu
Na
–
–
–
46-1180
25-215
7.419.7
20374
78.91017.5
43.5314
10-17.1
38279.3
21.73150.9
–
–
–
Cr
Referenc es
–
Costa et al. (2019)
–
de Melo et al. (2018a)
–
de Melo et al. (2018b)
–
Spulber et a. (2018)
bifloral and multifloral
India
Turkey
Cocos nucifera, Coriandrum sativum, Brassica napus and Multi-floral
36004100
Commercial bee pollen
992.1 22894. 14
Republi c of Actinidia arguta and Quercus Korea
Turkey
Chestnut, buckwheat, oak and multi-floral pollen
Nigeria
-
Brazil
Caesalpineaceae, Brassicaceae, Eucalyptus, Carica, Machaerium and Rubiaceae
1600-2 000
32004600
491.851472.1 0
795.8 95246. 99
10267 11670
19475041
24204932
909.02380
–
133.6
991.5948.3
910.0826.6
–
643722
76665174
44305240
8401050
271.1 21278. 34
17582737
25.2753.82
82.40243
36.3070.81
7.8212.81
14.8339.07
28.60725.36
8.1554.63
3.7314.99
96102
624.225.941083 49.74 44.0 – 72.0
–
86
0.13.0
29 -43
322-345
44.79161.4
2.6-4.3
58-312
53- 204
28-47
12.3640.46
7.22213.42
0.1-0.4
28 -62
0.4-0.5
6.813.1
150284
0.651.79
Thakur and Nanda (2018a)
–
0.341.59
Altunatm az et al. (2017)
106567
–
Ghosh and Jung (2017)
54976223
2.817.94
Kalaycıo ğlu et al. (2017)
–
Odimba et al. (2016)
2-42
Sattler et al. (2016)
105.8111.2
–
Brazil
Eucalyptus, Asteraceae/Linguliflora, Mimosa caesalpiniaefolia,Piper, Elephantopus, Cyperaceae and Anacardiaceae
26005200
12001700
Serbia
Brassicaceae, Salix, Fabaceae and other multi-floral samples
24624236
Saudi Arabia
Cucurbita pepo Thunb, Phoenix dactylifera L., Helianthus annuus L., Brassica napus L. and Medicago sativa L.
6232. 798258. 50
Brazil
5918. Senna sp, Chamaecrista sp and 5Mimosa tenuiflora 13366 .6
Colomb Multi-floral ia India, China, Romani Commercial bee pollen a, Spain, Bulgari a,
3.06 7.62
36079542
–
8.113.3
30.450.2
–
de Melo et al. (2016)
44.10114.93
13.5292.23
5.26110.737
4.9554.88
0.1700.465
Kostic et al. (2015b)
31.9244.18
338.12562.06
16.6038.61
4.246.69
63458350. 27
–
Taha (2015)
–
975.4 – 2166. 1
36.4 71.2
16.433.5
35.175.0
0.8 – 1.9
–
–
da Silva et al. (2014)
–
3431542
19.870.6
23.2 126.6
–
8.9206
–
Fuenmay or et al. (2014)
–
4841194
26.153.2
28.8197.7
–
84379
–
Fuenmay or et al. (2014)
–
500900
63.6105.8
–
8562032
–
503964
31.7175.92
2086.3 65752.1 9
234.4 0468.0 5
2353. 114680. 53
1864.13424.9
1.092.41
4682376
87
–
–
Hungar y and Poland
China
Brazil
Brassica napus, Citrullus lanatus, Camellia japonica,Dendranthema indicum, Fagopyrum esculentum, Helianthus annuus,Nelumbo nucifera Gaertn, Papaver rhoeas, Rosa rugosa, Schisandra chinensis, Vicia faba, and Zea mays Commercial pollen
dehydrated
bee
23536358
8283053
21369587
3212777
14319910
8284670
21778165
3483621
28.2565.30
5.176.1
75.2207.8
11.1551.6
8.69357.4
8.3125.11
274.1846.4
12-211
3.225.4
< 0.0041466
–
Yang et al. (2013)
–
Morgano et al. (2012)
–
Cistus ladanifer and commercial multifloral bee pollen
4961. 795357. 82
Romani Helianthus annuus and Salix sp. a
3246. 50-
Spain
520.33792.60
3096. 703197. 29
352.2 2437.7 2
16.3020.21
20.1529.66
18.7038.33 ±
5.057.20
60.7464.77
1409.7 9-
–
2630. 67-
31.6140.06
27.42122.87
–
–
–
88
–
Domíngu ezValhond o, Gil, Hernánd ez, & González -Gómez (2011) Stanciu et al.
Brazil
Asteraceae and other multifloral pollen
5421. 85
2630.6 7
4773. 265383. 73
848.361179.0 5
1008. 28 6873. 407102. 29
679.0 1818.0 2
(2011)
45.0755.22
59.4886.66
42.6073.51
10.4112.05
191.0 2215.3 5
–
Carpes et al. (2009)
Vitamins (mg/100g) Fat-soluble Countr y
Botanical source
Vit. A (βcarote ne)
Water-soluble
Vit. K
Vit. B1
–
0.51.3
Vit. D
Vit. E
–
2.725.37
–
–
–
–
–
0.64– 1.01
1.77– 2.56
7.27– 14.43
Brazil
Eucalyptus, Asteraceae/Linguliflora, Mimosa caesalpiniaefolia,Piper, Elephantopus, Cyperaceae and Anacardiaceae
–
Brazil
Andira, Rubiaceae, Asteraceae, Mimosaceae, Fabaceae, Aquifoliaceae, Anacardiaceae, Myrtaceae, Caesalpineaceae, Brassicaceae, and others
0.0817.92
–
0.469.57
Brazil
Arecaceae, Cecropia, Cestrum, Cyperaceae, Eucalyptus, Ilex,
–
–
–
89
Vit. B2
0.4-0.6
Vit. B3
1.3-3.8
Referenc es
Vit. B5
Vit. B6
–
0.13.8
–
de Melo et al. (2016)
–
6.0379.70
Sattler et al. (2015)
0.33– 0.77
7-56
de Arruda,
–
Vit. C
Myrcia, Piper, Vernonia and Trema
Brazil
Arecaceae, Cecropia, Cestrum, Cyperaceae, Eucalyptus, Ilex, Myrcia, Piper, Vernonia and Trema
Pereira, de Freitas, Barth, & de AlmeidaMuradia n (2013a)
–
–
–
–
90
0.591.09
1.732.41
6.4315.34
0.500.79
–
de Arruda, Perei de Arruda, Pereira, Estevinh o, & de AlmeidaMuradia n (2013b)r a, Estevinh o, & de AlmeidaMuradia n (2013b)
Thailan Z. mays d
Brazil
Brazil
Brazil
1524 1525
Commercial bee pollen
1.530
0.319.92
Mimosa caesalpiniaefolia, Myrtaceae and other multi-floral
0.517.79
Arecaceae, Philodendron sp, Anadenanthera and Eucalyptus
5.6319.89
–
–
6.21
1.63-
–
–
0.20
–
0.50
–
7.03
–
0.39
–
–
Chantaru dee et al. (2012)
11.434.0
de Melo and AlmeidaMuradia n 2010)
–
11.434.0
de Melo, Freitas, Barth, & AlmeidaMuradia n (2009)
–
27.39 -56.03
Oliveira et al. (2009)
ND
–
4.30
–
1.63-
–
–
–
–
–
3.86
–
1.354.25
–
–
–
–
–
K: Potassium; Ca: Calcium; P: Phosphorus; Mg: Magnesium; Zn: Zinc; Fe: Iron; Mn: Manganese; Cu: Copper; Na: Sodium; and Cr: Chromium
1526 1527 1528 1529
91
1530
Table 5
1531 1532
Summary of total pheolic content (TPC), total flavonoid content (TFC) and phytochemical composition of bee pollen from different botanical origins throughout the world. Phenolic compound(s)
Country
Portugal
Botanical source
Cistus ladanifer, Echium sp. and Apiaceae
Total phenolic content (TPC)
35.05 mg GAE/g
References
Total flavonoid content (TFC)
Name
6.81 mg QE/g
Coumaroyl quinic acid, Myricetin-O-rutinoside, LuteolinO-dihexoside, Quercetin-O-dihexoside, Myricetin-Ohexoside, Myricetin-O-(malonyl)rutinoside, Isorhamnetin-O-dihexoside, Quercetin-O-hexosylpentoside, Quercetin-O-rutinoside isomer 1, Myricetin-O(malonyl)hexoside, Quercetin-O-rutinoside isomer 2, Luteolin-di-O-hexosyl-rhamosíde, Quercetin-O(malonyl)rutinoside, Isorhamnetin-O-rutinoside, Hydroxybenzoyl myricetin, Quercetin-O(malonyl)hexoside, Quercetin-O-rhamnoside, Isorhamnetin-O-(malonyl)hexoside isomer 1, Luteolin-O(malonyl)hexoside, Myricetin, Isorhamnetin-O(malonyl)hexoside isomer 2, Myricetin-Odihydroferuloyl protocatechuic acid, Myricetin-O-acetyl hydroxybenzoyl protocatechuic acid-isomer 1, MyricetinO-acetyl hydroxybenzoyl protocatechuic acid isomer 2, Quercetin-O-acetyl hydroxybenzoyl protocatechuic acid isomer 1, Myricetin-O-acetyl hydroxybenzoyl hydrobenzoic acid isomer 2, Quercetin-O-acetyl hydroxybenzoyl hydrobenzoic acid isomer 1, QuercetinO-acetyl hydroxybenzoyl hydrobenzoic acid isomer 2, Odihydroxybenzoyl acetyl malonyl coumaric acid flavonoid derivative 92
Anjos et al. (2019)
Serbia
Helianthus L.
Italy
Hedera helix L., Helianthus annuus L., Asteraceae T form, Cistus L., Cistus incanus/creticus, Brassica type, Gleditsia triacanthos L, Hedysarum coronarium L., Trifolium pratense gr., Castanea sativa Miller, Labiatae L. form, Magnolia, Fraxinus ornus L., Papaver rhoeas L., Crataegus monogyna Jacq., Prunus L., Rubus ulmifolius Schott., Daucus and Coriandrum gr.
Egypt
annuus
Trifolium alexanderinum L
2.91-3.82 mg GAE/g
4.2 - 29.6 mg GAE/g
0.8-2.3 mg GAE/g
0.84-0.87 mg QE/g
Protocatechuic acid, 5-O-Caffeoylquinic acid, Caffeic acid, p-Coumaric acid, Ferulic acid, Quercetin, Quercetin 3-O-galactoside, Quercetin 3-O-rhamnoside, Rutin, Kostić et al. Isorhamnetin, Isorhamnetin 3-O-glucoside, Narcissin, (2019) Kaempferol, Galangin, Luteolin, Apigenin, Acacetin, Genkwanin, Eriodictyol, Naringenin, Taxifolin, Phloretin, Aesculin
–
Cyanidin 3-O-xyloside/arabinoside, Delphinidin 3-O-(60 ’-p-coumaroyl-glucoside), Petunidin 3-O-arabinoside, Pelargonidin 3-O-glucoside, Delphinidin 3-O-glucoside, Delphinidin 3-O-glucosyl-glucoside, Delphinidin 3-Orutinoside, Cyanidin 3-O-sophoroside, Naringin 6'malonate, Naringin 4'-O-glucoside, Naringenin 7-Oglucoside, Apigenin 7-O-(6’-malonyl-apiosyl-glucoside), Tetramethylscutellarein, Luteolin 7-O-glucuronide, Rocchetti et Apigenin 6-C-glucoside, Kaempferol 3-O-glucuronide, al. (2019) Quercetin 3-O-rutinoside, Kamepferol 3,7-O-diglucoside, Quercetin 3-O-galactoside 7-O-rhamnoside, Quercetin 3O-rhamnosyl-galactoside, Kaempferol 3-O-sophoroside, 3,7-Dimethylquercetin, Dihydroquercetin, Formononetin, Genistin, Gallic acid ethyl ester, Syringic acid, Caffeic acid 4-O-glucoside, Caffeoyl glucose, Feruloyl glucose, Caffeic acid, Hydroxytyrosol 4-O-glucoside, Carnosic acid.
0.1-0.85 mg QE/g
93
AbdElsalam , Foda, Abdel-Aziz & El-Hady
(2018)
Brazil
Mimosa caesalpiniifolia, Eucalyptus, Rubiaceae, Astrocaryum aculeatissimum, C. nucifera, M. verrucosa, Myrcia, Alternanthera, Asteraceae, Anadenanthera, and Brassica asmonofloral and other multi-floral samples Alternanthera, Anadenanthera, Cocos nucifera, Mimosa caesalpiniaefolia, Myrcia, and Mimosa scabrella
–
6.5–29.2 mg GAE/g
5.6-29.7 mg GAE/g
6.9-21.0 mg GAE/g
0.3–17.5 mg QE/g
Gallic acid, Protocatechic acid, Chlorogenic acid, syringic acid, p-coumaric acid, Vanillic acid, Caffeic acid, ferulic acid, β-Resorcylic acid, rutin, naringenin, kaempferol, quercetin, catechin, naringin and epicatechin
de Melo et al. (2018a)
0.3-19 mg QE/g
Gallic acid, protocatechic acid, catechin, chlorogenic acid, vanillic acid, caffeic acid, epicatechin, b-resorcylic acid, syringic acid, p-coumaric acid, ferulic acid, synapic acid, naringin, rutin, cinnamic acid, naringenin, quercetin, kaempferol
de Melo et al. (2018b)
–
Duarte, Vasconcelo s, OdaSouza, Oliveira, & López (2018)
0.3-17 mg QE/g
94
Italy, Spain and Colombi a
Greece
Cistus ladanifer, Echium, Rubus ulmifolius, Parthenocissus quinquefolia Ampelopsis brevipedunculata, Brassica napus, Taraxacum officinale, and Trifolium pratense. Commerical bee pollen (Papaver rhoes, Chamomila recutita, Sinapis arvensis, Cistus sp., Trifolium sp., Dorycnium sp., Cichorium sp., Convolvulus sp., Circium sp., Malva sylvestris, Fumana sp., Eucalyptus camaldulensis, Anemone sp., Ononis sp., Asphodelus sp., and Quercus ilex)
–
5.050 mg GAE/ml
–
Tri-caffeoyl- and caffeoyl-di-p-coumaroyl spermidine derivatives
Gardana, Del Bo, Quicazan, Corrrea, & Simonetti (2018)
–
Isopimpinellin, quercetin 3-O-xylosyl-glucuronide, hydroxycaffeic acid, urolithin B, p-coumaroyl tyrosine, quercetin 3-O-rhamnosyl-galactoside, quercetin 3-Oxylosyl-glucuronide, isorhamnetin-3-O-glucoside 7-Orhamnoside, quercetin 3-O-rutinoside
Karabagias, Karabagias, Gatzias, & Riganakos (2018)
95
Brazil
Cocos nucifera
–
–
Greece
Cistus creticus
15.20-60.20 mg GAE/g
6.00- 57.60 mg QE/g
33.46-135.93 mg GAE/g
15.28-31.80 mg QE/g
Malaysia
–
6-O-caffeoyl glucoside, trihydroxycinnamic acid, quercetin-3-O-rhamnosylglucoside, isorhamnetin-di-3,7O-glucoside, Isorhamnetin-3-O-(2”,3”-Odirhamnosyl)glucoside, isorhamnetin-3-O-(2”-ONegri, rhamnosyl) glucoside, N’,N”,N’”-tris-caffeoyl Barreto, spermidine, quercetin-3-O-rhamnoside - (quercetrin), Sper, isorhamnetin-3-O-(2”-O-rhamnosyl acetyl) glucoside, Carvalho, & N’,N”-dicaffeoyl,N’”-coumaroyl spermidine, N’,N”Campos dicaffeoyl,N’”-feruloyl spermidine, N’-caffeoyl-N”(2018) feruloyl,N’”-coumaroyl spermidine, N’-caffeoyl-N”,N’”dicoumaroylspermidine, N’,N”,N’”-tris-p-coumaroyl spermidine, isorhamnetin-3-O-(6”-O-p-coumaroyl)glucoside, and N’,N”,N’”-tris-p-feruloyl spermidine Atsalakis, Chinou, Quercetin-7-rhamnoside, quercetin-3-neohesperidoside, Makropoulo u, kaempferol-3-neohesperidoside, myricetin-3neohesperidoside, kaempferol-3-glucoside and quercetin- Karabourni 3-glucoside oti, & Graikou (2017)
–
96
Fadzilah, , Jaapar, Jajuli, & Wan Omar (2017)
12.57 mg GAE/g
22.89 mg RE/g
Rutin, p-hydroxybenzoic acid , benzoic acid, resveratrol, quercetin, cinnamic acid, vanillin, kaempferol, protocatechuic acid, p-coumaric acid, gallic acid and catechin
Sun, Guo, Zhang, & Zhuang (2017)
–
Vasconcelo s et al. (2017)
China
Rapeseed
Brazil
Mimosa misera, Mimosa caesalpinifolia, Erythrina velutina, Ziziphus joazeiro, Prosopis juliflora, Maytenus rígida, Mimosa tenuiflora, Coutarea hexandra, Piptadenia macrocarpa, Coutarea hexandra, Hyptis suaveolens, and Coutarea hexandra
5.85-46.25 mg GAE/g
1.82-107.00 mg QE/g
–
3.5-23.3 mg GAE/g
–
Quercetin 3-O-sophoroside, quercetin dihexoside and Čeksteryté isorhamnetin 3-glucoside et al. (2016)
–
FatrcováŠramková et al. (2016)
Lithuania
Slovakia
Helianthus L.
annuus
0.69 – 0.80 mg GAE/g
Quercetin, kaempferol, luteolin, apigenin 97
China
Brassica campestris
–
Colombi a
–
24.79 -33.69 mg GAE/g
Brazil
–
40 mg GAE/g
Lithuania
Castanea, Rubus and Cistus –
13.53-24.75 mg GAE/g 24.4 - 38.9 mg
China
Rapeseed
–
Egypt
Zea mays
–
Echium plantagineum
–
Portugal
Watermelon, rape, camellia, corn poppy, corn, motherwort, buckwheat, sesame,
–
Italy
China
604 mg RE/g
Quercetin 3-O-glucoside, kaempferol 3-O-glucoside, naringenin, rutin, quercitrin, kaempferol, and isorhamnetin
Zhang et al. (2016)
Zuluaga et al. (2016) Bárbara et 1 mg CAE/g – al. (2015) 5.91-15.86 mg/g Gallic acid, 4-hydroxybenzoic acid, caffeic acid, and p– Domenici et CE coumaric acid al. (2015) 7.3–10.0 mg RE/g – Kaškonienė Lv et al. – Rutin, quercetin, kaempferol, and isohamnetin (2015) Gallic acid, Vanillic acid, Synringic acid, p-Coumaric acid, Ferulic acid, Caffeic acid 4.21 ± 0.22 11.4 ± 0.04 Quercitin 6.4 ± 0.30 2.24 ± 0.02 Rutin 3.46 ± 0.14 6.4 ± 0.11 Catechin 4.8 ± 0.18 2.1 ± 0.13 Epicatechin 2.1 ± Mohdaly et – 0.08 nd α-Catechin 0.58 ± 0.05 nd Kaempferol 1.65 ± al., (2015) 0.24 0.59 ± 0.19 Apigenin 2.4 ± 0.25 3.57 ± 0.21 3,4Dimethoxycinnamic acid 45.8 ± 0.16 nd Naringenin 3.34 ± 0.12 2.56 ± 0.28 Luteolin Kaempferol-3-O-(4″-rhamnosyl)-neohesperidoside, kaempferol-3-O-sophoroside, kaempferol-3-Oneohesperidoside, kaempferol-3-O-neohesperidoside-7O-rhamnoside, kaempferol-3-O-glucoside, kaempferol-3- Sousa et al. – O-rutinoside + kaempferol-3-O-(3″/4″-acetyl)(2015) neohesperidoside, delphinidin-3-O-glucoside, delphinidin-3-O-rutinoside, petunidin-3-O-glucoside, petunidin-3-O-rutinoside, and malvidin-3-O-rutinoside –
–
–
Quercetin-3-O-b-D-glucosyl-(2/l)-b-glucoside, kaempferol-3, 40-di-O-b-D-glucoside and kaempferol-3O-b-D-glucosyl-(2/l)-b-D-glucoside 98
Zhou et al.(2015)
broad bean and rose India
Brassica juncea
Portugal and Spain
Cistaceae, Fabaceae, Cistaceae, Ericaceae, Boraginaceae
Latvia , Lithuania , China, Spain and Turkey
Brazil
18.29 mg GAE/g
–
18.55-32.15 mgGAE/g
3.92-10.14 mg QE/g
-
24.1 - 45.5 mg RE/g
6.1 - 11.6 mg RE/g
–
44.07-124.10 mg GAE/g
–
20.22-48.76 mg GAE/g
6.58-28.43 mg QE/g
– 41.5 to 213.2 mg GAE/g
Brassicaceae, Asteraceae elephantopus, Asteraceae gochnatia, Myrtaceae eucalyptus, Asteraceae baccharis
and
Rutin, chrysin, kaempferol and quercetin
–
Ketkar et al., 2014 Pascoal, Rodrigues, Teixeira, Feás, & Estevinho (2014)
2-hydroxycinnamic acid, rutin, quercetin, naringenin, and Kaškonienė gallic, caffeic, and ferulic acids et al. (2014) Catechin, epicatechin, quercetin, rutin, and gallic, protocatechuic, p-hydroxybenzoic, chlorogenic, vanillic, caffeic, syringic, p-coumaric, ferulic, benzoic, ocoumaric, abscisic and trans-cinnamic acid
Ulusoy and Kolayli (2014)
Rutin, myricetin
Carpes et al. (2013)
–
o-, p-coumaric acid, ferulic acid, myricetin, cinnamic acid, quercetin, naringenin, hesperitin and kaempferol
Fanali et al. (2013)
–
Isoquercetin, myricetin, tricetin, quercetin, luteolin, selagin, kaempferol, and isorhamnetin
Freire et al. (2012)
and
Greece
–
Brazil
Cecropia, Eucalyptus, Elaeis, Mimosa pudica, Eupatorium, and
99
Portugal
USA
Scoparia Rosaceae, Cistaceae, Boraginaceae, Asteraceae, Fagaceae, Ericaeae, Myrtaceae and Fabaceae
Mesquite, yucca, palm, terpentine bush, mimosa, and chenopod
10.50–16.80 mg GAE/g
15.91- 34.85 mg GAE/g
–
–
Morais, Moreira, Feás, & Estevinho, 2011
2.66-5.48 mg QE/g
Naringenin, 4′,5-dihydroxy-7-methoxyflavanone, 7,8,2′,4′-tetrahydroxy isoflavone, benzene acetic acid, αoxo, methyl ester, anthraquinone derivative, 5-methoxy7-methyl-1,2-naphthoquinone, 7-hydroxy-1-indanone, 1p-tolyl-anthraquinone, 2-methyl-5-hydroxybenzofuran, 5methoxy-7-methyl-1,2-naphthoquinone, 1,2,3,4tetrahydro-2-(2-hydroxy-3-phenoxypropyl)-6,7dimethoxyisoquinoline, 1-)2-methoxy phenyl)-9,10anthracenedione, 2,6-Dihydroxy-6-methylbenzaldehyde, 2-formyloxy-1-phenylethanone, α-oxo, methyl ester, and 1,1-diphenyl-9-methyldeca-3,5-dien-1,9-diol-8-one
LeBlanc, Davis, Boue, de Lucca, & Deeby (2009)
1533 1534
100
1535
Figure Legends
1536
Fig. 1. The collection process of bee pollen by honeybees.
1537 1538 1539 1540
[1] Honeybee, [2] Flower with pollen, [3] Honeybee covered with microscopic pollen, [4] Honeybee carrying pollen pellet in her hind legs, [5] Honeybee ready to carry pollen pellet, [6] Hind-legs with pollen pellet, [7] Pollen trap at hive entrance, [8] Trap-tray for bee pollen collection and [9] Collected bee pollen
1541 1542
Fig. 2. Bee pollen of (a) several colors and (b) morphology and surface texture (examined using Scanning Electron Microscope, SEM) from diverse botanical origin.
1543 1544 1545 1546 1547 1548 1549 1550 1551 1552 1553 1554 1555 1556 1557 1558 1559
[1] Asphodelus tenuifolius: Dull orange color, [2] Brassica napus: Bright yellow color, [3] Castanea: Light yellow color, [4] Cistus: Dull yellow color, [5] Cocos nucifera: Creamish yellow color, [6] Coriandrum sativum: Pale brown color , [7] Pennisetum glaucum: Bright brown color, [8] Rubus: Yellow green color, [9] and [10] Multi-floral: Samples having different colors of pollen grain, [11] Zea mays: Monad, spherical and presence of germination pore, [12] Quercus sp: Monad, prolate and tricolpate (30x27µm), [13] Actinidia arguta: Monad, prolate, tricolporate, and oval (24.5x17.5 µm), [14] Elaeis guineensis: Monad, circular and tectate exine , [15] Camellia sinensis: Monad, triangular and radially symmetric, [16] Mimosa diplotricha: Rhomboidal tetrad, oval and reticulated exine , [17] Arecaceae sp: Monad, isopolar, prolate, tricolpate, presence of furrow and smooth surface, [18] Cocos nucifera: Monad, monocolpate, elliptical shape with smooth surface and furrow, [19] Coriandrum sativum: Long, stick-shaped, monad and had smooth surface along with furrows containing pores, [20] Brassica napus: Monad, prolate, and tricolpate along with distinct net-like pattern over exine, [21] Maytenus sp: Monad, tetrahedral, oblate and reticulated surface, [22] Aloe greatheadii: Monad, bilaterally symmetrical and elliptical shape with a deep furrow (44-50 µm), [23] Asteraceae eupatorium: Monad, spherical and spinules surface, and [24] and [25] Multi-floral: Samples containing individual pollen grain with different shapes and surface properties
1560 1561 1562
Adapted from: Chantarudee et al. (2012); Forcone, Calderón and Kutschker (2013); Human et al. (2013); Rebiai and Lanez (2013); Gabriele et al. (2015); de Florio Almeida et al. (2017); Ghosh and Jung (2017) and Peukpiboon, Benbow and Suwannapong (2017)
101
Fig. 1
(a)
(b) Fig. 2
Highlights •
Physicochemical and functional properties of bee pollen from varying sources are summarized.
•
Bee pollen has average 54.22% carbohydrates, 21.30% proteins, 5.31% lipids and 2.91% ash content.
•
Functional properties are reviewed as key elements for valorization of bee pollen.
•
Investigating the mono-floral bee pollen from diverse botanical and geographical origin is proposed.
•
The need of harmonized global standards for bee pollen safety is also addressed.
PII:
S0924-2244(19)31021-0
DOI:
https://doi.org/10.1016/j.tifs.2020.02.001
Reference:
TIFS 2736
To appear in:
Trends in Food Science & Technology
Received Date: 16 November 2019 Revised Date:
5 January 2020
Accepted Date: 3 February 2020
Please cite this article as: Thakur, M., Nanda, V., Composition and functionality of bee pollen: A review, Trends in Food Science & Technology (2020), doi: https://doi.org/10.1016/j.tifs.2020.02.001. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2020 Published by Elsevier Ltd.
Authors’ Contribution Statement Mamta Thakur has framed the article structure; searched, complied and interpreted the literature and written the manuscript. Professor Vikas Nanda has technically reviewed and edited the manuscript. Both authors contributed critically to the final revised form of the manuscript.
1
Composition and functionality of bee pollen: A review
2
Running head: Bee pollen: Composition & functionality
3
Mamta Thakur* and Vikas Nanda
4
Department of Food Engineering and Technology
5
Sant Longowal Institute of Engineering and Technology (Deemed-to-be-University), Longowal -
6
148106 (Punjab) India
7 8 9 10 11 12 13 14 15 16 *
17
Corresponding Author:
18
Mamta Thakur
19
Department of Food Engineering and Technology
20
Sant Longowal Institute of Engineering and Technology (Deemed-to-be-University)
21
Longowal - 148106 (Punjab) India
22
E-mail: [email protected]
23
ORCID: 0000-0002-6052-6819 1
24
Abstract
25
Background
26
The food industry today is returning to natural foods after emphasizing the processed products
27
due to the higher consumer demand for foods which are well recognized by healthy nutrients.
28
Bee pollen is known as a natural superfood due to its indispensable nutritional and medicinal
29
properties. However, the physico-chemical and nutritional properties of bee pollen are
30
ambiguous which vary greatly due to the difference of botanical and geographical origin.
31
Scope and approach
32
The current study, therefore, presents an updated overview by critically reviewing the literature
33
for chemical constituents (sugars, amino acids, fatty acids, minerals, vitamins, and phenolic
34
compounds) of bee pollen since 2009 from more than 20 nations of the world. The functional
35
properties of different plant-derived bee pollen and their food applications are also discussed for
36
the first time.
37
Key findings and conclusions
38
As per the systematic review of above 100 studies, the bee pollen contains average 54.22%
39
(18.50-84.25%) carbohydrates, 21.30% (4.50-40.70%) proteins, 5.31% (0.41-13.50%) lipids,
40
8.75% (0.15-31.26%) fibre, 2.91% (0.50-7.75%) ash, 13.41 g/100g (2.77-28.49 g/100g) glucose,
41
15.36 g/100g (4.9-33.48 g/100g) fructose, 4.25 g/100g (0.05-9.02 g/100g) sucrose, 4951.61
42
mg/kg (3.06-13366.60 mg/kg) potassium, 4157.86 mg/kg (234.40-9587.00 mg/kg) phosphorus,
43
1751.22 mg/kg (1.09-5752.19 mg/kg) calcium, 1246.99 mg/kg (44.00-4680.53 mg/kg)
44
magnesium, 46.97 mg/kg (0.10-105.80 mg/kg) zinc, 197.41 mg/kg (2.60-1180.00 mg/kg) iron,
45
and 30.59 mg GAE/g (0.69-213.20 mg GAE/g) total phenolic content. Bee pollen, based on its
46
functional properties can be recommended as a natural food ingredient in several processed food 2
47
products. Further, the present paper strongly focuses to investigate the mono-floral bee pollen
48
from different geographical regions and related safety issues to establish the global pollen quality
49
and safety standards in coming years.
50
Keywords: Bee pollen; essential amino and ω-3 fatty acids; B-complex vitamins; polyphenols;
51
functional properties; food applications
52
1. Introduction
53
Recently, the bee pollen has demonstrated great attention in food processing as it is a
54
paragon of wholesome nutrients (Sattler et al., 2015; Thakur & Nanda, 2018a). It contains
55
mainly lipids, proteins, and micronutrients essential for honeybees whereas it exhibits the
56
nutraceutical potential for humans, thereby preventing several diseases (de Melo & Almeida-
57
Muradian, 2010; Komosinska-Vassev, Olczyk, Kafmierczak, Mencner, & Olczyk, 2015). For the
58
heightened application of bee pollen, its comprehensive characterization based on physico-
59
chemical, nutritional, and functional characteristics as per floral and geographical source is need
60
of the hour.
61
Basically, the pollen is the microscopic structure like grains, found in the anther of
62
stamen in the angiosperms (Steven, 2014). Worker honeybees during visits attract the hundreds
63
to thousands of pollen grains using weak electrostatic field generated between flower (negatively
64
charged) and bee body (positively charged) (Clarke, Morley, & Robert, 2017). The pollen grains
65
are agglutinated using the several combs and hairs of bee’s hind legs which are moistened with
66
salivary secretions and nectar to form a pellet of size 1.4-4 mm i.e. characteristically distinct
67
from wind pollen (Saavedra, Rojas, & Delgado, 2013). Thus bees carry the pollen as pellets
68
using the pollen basket and stored inside the alveoli for further consumption to fulfill the
69
requirements for protein and to synthesize the jelly in their food glands (Di Pasquale et al., 3
70
2013). The bee colony can collect 50-250 g of pollen per day or 15-40 kg per year (Komosinska-
71
Vassev, Olczyk, Kafmierczak, Mencner, & Olczyk, 2015).
72
Bee pollen, also known as apicultural or bee-collected or corbicular pollen can be
73
harvested with the help of trap, fixed at the entrance of beehives. While returning home, the
74
pollen is lost from the hind legs and collected in the collection tray of the trap (Fig. 1). The
75
nutrient-dense pollen thus collected is high in moisture content and its properties initiate to
76
degrade after the collection. Therefore, the bee pollen must be consumed either fresh or quickly
77
dried carefully to retain the nutrients (Denisow & Denisow-Pietrzyk, 2016; Kieliszek et al.,
78
2018). The plant sources of bee pollen, as determined by palynological analysis strongly affect
79
its nutritional, physico-chemical, and functional properties (da Silva et al., 2014; Nogueira,
80
Iglesias, Feás, & Estevinho, 2012; Yang et al., 2013; Thakur & Nanda, 2018a). The pollen
81
pellets from unique botanical taxon or the ones having single predominant pollen at > 90%
82
frequency or containing no accessory pollen at > 60% frequency are considered as mono-floral
83
(Barth et al., 2010). However, in case of inadequate flora surrounding the hive, the honeybee will
84
visit the flower of other botanical sources and thus the microscopic pollen grains are mixed,
85
resulting in the pellet known as multi-floral pollen when there is no predominance and may
86
present accessory pollen varying from 15-45% (Barth et al., 2010). The flower from plant
87
species affects the color of pollen grain ranging from white or creamish white and yellow to
88
orange, red, green, gray and dark brown. The physico-chemical, functional and sensory
89
properties are usually fixed for mono-floral pollen of a particular botanical origin whereas the
90
multi-floral pollen loads vary in the properties (Barth et al., 2010). Even after a similar plant
91
source, pollen composition may vary due to seasonal and regional variations (de Melo, Freitas,
92
Barth, & Almeida-Muradian, 2009). 4
93
Bee pollen contains carbohydrates (13-55 %), proteins (10-40 %), lipids (1-13 %), crude
94
fibre (0.3-20 %) and ash content (2-6%) (Campos et al., 2008). In addition, it is composed of all
95
essential amino and fatty acids, free amino acids, vitamins mainly B-complex, essential minerals,
96
carotenoids and flavonoids (Mărgăoan et al., 2014; de Melo et al., 2016; Ghosh & Jung, 2017;
97
Thakur & Nanda 2018a). Fructose followed by glucose and sucrose is the major sugar and nearly
98
1% of remaining sugars in pollen include arabinose, isomaltose, melibiose, melezitose, ribose,
99
trehalose, and turanose (Chantarudee et al., 2012; Liolios et al., 2018). It is acclaimed for its
100
excellent nutrition and therapeutic properties, and currently, commercially consumed as a dietary
101
supplement. Bee pollen has been acknowledged by law as a food additive in Argentina, Brazil,
102
and Switzerland where its standard norms of physico-chemical and microbiological quality have
103
been officially instituted. Likewise, several other countries have established the physico-
104
chemical parameters of pollen for its healthy intake (Fuenmayor et al., 2014; Canale et al., 2016).
105
Therefore, a vast research interest has been observed about bee pollen and numerous studies
106
have been conducted for characterizing the pollen of varying floral origins from different regions
107
of numerous countries like Brazil, China, Greece, India, Portugal, Romania, Spain, South Africa,
108
Saudi Arabia, etc. to identify the peculiarities (Yang et al., 2013; Liolios et al., 2016; Sagona et
109
al., 2017; de Melo et al., 2018a; de Melo et al., 2018b; Gardana, Del Bo, Quicazan, Corrrea, &
110
Simonetti, 2018; Liolios et al., 2018; Thakur & Nanda, 2018a; Isik, Ozdemir, & Doymaz, 2019;
111
Liolios et al., 2019a,b). However, as per the literature survey, a detailed review of bee pollen still
112
lacks its physico-chemical and functional properties. Globally, a generic quality criterion for
113
pollen was suggested by Campos et al. (2008) whereas Puerto, Prieto, and Castro (2015) focused
114
on the phytochemicals reported in pollen contributing to antioxidant potential. As per the
115
literature, the biological and medicinal activities of pollen were discussed by Denisow and 5
116
Denisow-Pietrzyk (2016); the extraction techniques of pollen derived bioactive compounds were
117
analyzed by Ares, Valverde, Bernal, Nozal, and Bernal (2017) and Li et al. (2018) studied the
118
nutritional and biological properties of pollen from a limited botanical and geographical sources.
119
Further, the metabolism of bee pollen derived natural metabolites and food safety of pollen were
120
discussed in many studies which seems to be unsatisfactory without the detailed knowledge of
121
bee pollen composition and functionality. This paper, therefore, aims to present a comprehensive
122
and updated summary of researches from the previous 10 years on physico-chemical
123
composition and functionality of bee pollen from diverse botanical and geographic roots of more
124
than 20 countries which will fortify the existing knowledge about the bee pollen composition.
125
2. Nutritional value
126
Today the health-conscious consumers prefer to consume the value-added products which
127
allow replacing the conventional food ingredients with high-nutritional value component to
128
supplement the existing processed products. The human diet should provide the energy and other
129
essential nutrients required for physical and mental development and health in amounts that meet
130
standards (Kieliszek et al., 2018). Due to the excellent nutrient profile, bee pollen can
131
supplement the human diet and provides a significant daily intake of nutrients. Average bee
132
pollen composition, as reviewed by Campos et al. (2008) is compared with nutritional
133
requirements for an average adult in Table 1. The share of major nutritional components
134
particularly carbohydrates and fats are comparatively small; however, the crude fiber and protein
135
can contribute significantly up to 60% and 70% of required daily intake (RDI), respectively
136
based on the floral source and location. Further, the daily intake of 50g bee pollen provides all
137
essential vitamins (except pyridoxine and pantothenic acid) and minerals (except calcium)
138
sufficient to meet above 50% requirement of RDI. Bee pollen intake can be increased by adding 6
139
them in routine foods, for instance, mixing in milk, smoothies, yogurt, bread, cookies, fruit
140
juices, etc. as seen in case of flaxseed addition in bakery products (Kaur, 2011; Čukelj et al.,
141
2017; Kaur et al., 2018). According to Nagai et al. (2007), the free amino acids, required by the
142
body are adequately provided even by 15g Spanish pollen. Some studies even reported that bee
143
pollen intake is enough for human survival (Nogueira, Iglesias, Feás, & Estevinho, 2012). The
144
vitamins from bee pollen contribute to the nutrition greatly and almost all the essential minerals
145
are reported in bee pollen in good amounts. However, RDI can vary according to the difference
146
in bee pollen composition. The pollen derived nutrients are digested and assimilated in a better
147
way which improves the immune system against pathogens, and physical and chemical agents.
148
Chinese rape bee pollen is employed as the immunity enhancer of the organism against cancer
149
diseases (Omar, Azhar, Fadzilah, & Kamal, 2016). Bee pollen, when administered daily in 40 g
150
to heart patients, caused a decrease in their cholesterol level, blood viscosity and fibrinogen and
151
fibrin (Campos, Frigerioc, Lopes, & Bogdanov, 2010). Bee pollen also decreases the lipid
152
content in blood serum which is considered to link with the level of hormones like insulin,
153
testosterone, and thyroxine (Komosinska-Vassev, Olczyk, Kafmierczak, Mencner, & Olczyk,
154
2015). However, the bee pollen failed to substantiate health claims under EFSA Regulation (EC)
155
No. 1924/2006 EU (Mateescu. 2011; Onisei, Mateescu, & Răscol, 2018).
156
3. Physico–chemical properties
157
3.1. Physical properties
158
3.1.1. Weight, shape, and size
159
The average weight of bee pollen pellet is approximately 7.5-8 mg that varies according
160
to the pollen accessibility during the visit. The pollen from a single floral source may be
161
significantly dissimilar in shape and size thereby affecting the pollen-packing efficiency 7
162
(Komosinska-Vassev, Olczyk, Kafmierczak, Mencner, & Olczyk, 2015). The anemophilous
163
plants provide lighter and dried pollen resulting in larger and loosely arranged pellets whereas
164
the entomophilous plants are responsible for smaller and more compacted form pollen (Friedman
165
& Barrett, 2009).
166
The fresh pollen may be cylindrical, round, triangular, or bell-shaped whereas the dried
167
pollen pellets having diameter 0.01-0.05 mm are usually spherical or spindle-shaped (Barene,
168
Daberte, & Siksna, 2015). Thakur and Nanda (2018b) evaluated the pollen pellets from Cocos
169
nucifera, Coriandrum sativum, Brassica napus and multi-floral source of India and reported the
170
variation in length, width, equivalent diameter, thousand pollen pellet weight, sphericity, surface
171
area, bulk and true density, volume, porosity and angle of repose due to their moisture content.
172
On the other hand, Bleha, Shevtsova, Kružík, Brindza, and Sinica (2019) reported the pollen
173
loads (Brassica napus, Helianthus annuus, Papaver somniferum, Phacelia tanacetifolia, Robinia
174
pseudoacacia, Trifolium repens) of mean 11.85 g weight, 3.10 mm height, and 3.55 mm width,
175
from the Slovak Republic. Further, the surface texture of pollen grains provides a hint of their
176
botanical composition due to distinct exine structure and properties (Fig. 2) which are
177
representative of particular plant species (Wang & Dobritsa, 2018). For instance, the maize has
178
thicker exine covered fully with tectum, exine in Brassica is thinner having a reticulated surface
179
and Hibiscus contains exines densely covered with long-pointed spines (Basarkar, 2017; Wang
180
& Dobritsa, 2018).
181
3.1.2. Color
182
The pollen quality can be roughly judged based on its color which is linked to plant
183
pigments like carotenoids and anthocyanins, inherently found in different concentrations in
184
pollen (Sattler et al., 2015). The natural brightness of anther pollen decreases due to the addition
185
of moisture particularly nectar to form a pollen pellet. The bee pollen contains all shades of color 8
186
from white to black (Fig. 2), however, the pollen collected from the same plant source may have
187
different color and sometimes, the bee pollen from various botanical origins can be of similar
188
color. Modro, Silva, Luz, and Message (2009) reported that such differences arise from the state
189
of flower thecae which may be either already open or split by honeybees.
190
Color is affected by chemical composition also, as revealed by instrumental color
191
analysis exhibiting the correlation between color values and Ca, Mg and Fe contents (Yang et al.,
192
2013). Likewise, color values of Brazilian pollen were recommended as indices by de Melo et al.
193
(2016) to determine the total phenolic content and antioxidant and antimicrobial potential by
194
observing the correlation among these parameters. Further, the processing conditions also
195
influence the color values, particularly L* and b* and grinding of pollen pellets after dehydration
196
results in the supremacy of yellow color and higher positive values of b*. This may be due to
197
oxidation reactions of some compounds like polyphenols during drying (Silva, Rosa, & Vilas-
198
Boas, 2009).
199
3.2. Chemical properties
200
3.2.1. Moisture content and water activity
201
The concentration of water is a major factor that affects the amount of remaining
202
constituents in any product while the quality and storage life is closely associated with the water
203
activity (aw) (Nogueira, Iglesias, Feás, & Estevinho, 2012). The higher aw stimulate the growth of
204
microorganisms, particularly yeasts and molds, producing the mycotoxins and ochratoxins and
205
enzyme activities in bee pollen which may be a fundamental cause of pollen toxicity, creating a
206
risk to consumer (Feás, Vazquez-Tato, Estevinho, Seijas, & Iglesias, 2012). However, the
207
legislations have not yet fixed the standards for its value. Usually, the various perspectives of
208
food quality and safety including moisture sorption, enzymatic activities, etc. are affected by
209
higher aw, thereby increasing the significance of hygienic conditions during handling, drying, and 9
210
processing of bee pollen to minimize the likelihood of man-derived contaminations. Table 2
211
showed the data about moisture content and aw of pollen of varying plant sources and countries.
212
Fresh bee pollen may contain at least 7% and maximum up to 30% moisture content and
213
is hence always at the risk of fungal contamination due to its highly hygroscopic nature thus
214
questioning the safety of bee pollen (Carpes, Mourão, Alencar, & de Masson, 2009). Sun or
215
shade drying should be avoided due to the enhancement of microbial growth and drying below
216
3% moisture is also undesirable due to discoloration and generation of off-flavor derived from
217
increased rate of chemical reactions like Maillard browning, fructose dehydration, loss of aroma
218
compounds and lipids oxidation (Nogueira, Iglesias, Feás, & Estevinho, 2012). Therefore, the
219
dried pollen must have moisture content varying from 5-9% and humidity level after drying
220
should be kept in a range of 4‒8% which retains the pollen nutrients and ensures the safety (de
221
Arruda, Pereira, de Freitas, Barth, and de Almeida-Muradian, 2013a). Freezing is another
222
technique to preserve the pollen nutrients but pollen should be processed quickly after thawing,
223
using lyophilization, desiccation, and microwave-assisted drying (Conte et al., 2017).
224
3.2.2. Carbohydrates and sugars
225
Carbohydrates are the largest constituent of bee pollen which accounts for nearly 2/3rd of
226
the total pollen dry weight (Li et al., 2018). The higher amount of carbohydrates is due to the
227
incorporation of honey or nectar during pellet formation thus enhancing the carbohydrates
228
however, the plant species, growth and harvesting conditions are important factors affecting its
229
amount. The carbohydrates show a huge variation from 18.50-82.80 % in pollen throughout the
230
world (Table 2).
231
Pollen consists of monosaccharides - fructose and glucose and disaccharides - sucrose,
232
turanose, maltose, trehalose, and erlose, with the fructose/glucose ratio varying between 1.20-
233
1.5. The higher amount of reducing sugars is reported in bee collected pollen (Table 3) which 10
234
makes it distinct from plant pollen (Carpes, Mourão, Alencar, & de Masson, 2009). Liolios et al.
235
(2018) reported an average of 42.10% total sugars in thirty monofloral pollen samples from
236
Greece which varied from 34.70% to 63.50%. Among polysaccharides, the sporopollenin is
237
present in exine – the outer layer of a pollen grain, furnishing a rigid and sculptured framework
238
and is highly resistant to non-oxidative physical, biological and chemical degradation processes
239
including acetolysis thus contributing to encapsulate and protect the pollen contents including
240
bioactive compounds. The inner layer of pollen known as intine consists of cellulose and pectin
241
and Xu, Sun, Dong, and Zhang (2009) stated the structural resemblance between intine and plant
242
cell wall. However, these polysaccharides are not responsible for contributing any nutritional
243
value but important in the regulation of several biological functions.
244
3.2.3. Proteins and amino acids
245
Proteins are the largest component in pollen after carbohydrates and fulfill the honeybee
246
nutritional requirements. It is highly varying in pollen collected from diverse plant sources
247
(Table 2). However, protein content even varies in uni-floral pollen of distinct countries:
248
Brassica napus - 19.63% (India), 23 % (Brazil), 27.3 % (China); Cocos nucifera - 25.39%
249
(India), 10.3-20.3 (Brazil); and Zea mays – 14.86% (Greece), 17.9% (China), 23.3 % (Egypt)
250
(Yang et al., 2013; Liolios et al., 2016; de Melo et al., 2018a; Thakur & Nanda, 2018a). One the
251
other hand, the commercial bee pollen of Attiki Bee Culturing Co.-Alex Pittas S.A., Athens,
252
Greece contained 17.60% protein (Karabagias, Karabagias, Gatzias, & Riganakos, 2018). The
253
possible reason for this is the mixing of nectar in bee pollen. Moreover, bee pollen on drying
254
may contain 2.5-62% protein depending on the botanical origin and such a high amount signifies
255
the role of this macronutrient as a novel dietary supplement, particularly for vegetarians
256
(Campos, Frigerioc, Lopes, & Bogdanov, 2010).
11
257
Bee pollen dominantly contains bound-form amino acids and 1/10th of total proteins are
258
available as free amino acids whose composition is also affected by botanical origin and
259
processing and storage conditions (Domínguez-Valhondo, Gil, Hernández, & González-Gómez,
260
2011). The plant species affects the amino acid composition more in terms of quantity rather than
261
quality (Table 3). Glutamic acid and in some studies proline as well as aspartic acid are major
262
amino acids reported in pollen from plant species of different countries. The honeybees are
263
directly responsible for the proline level which seems to increase during storage due to its
264
synthesis in the presence of glutamate dehydrogenase from glutamic acid (Verslues & Sharma,
265
2010). Free amino acid content should be a minimum 2% which is essential for the
266
standardization of bee pollen in the European market. Besides this, the “proline index” must be
267
<80%, critical to indicate the pollen freshness (Canale et al., 2016). The bee pollen also contains
268
a higher level of essential amino acids (EAAs) which furnishes the high nutritional value for
269
honeybees and humans (Yang et al., 2013; da Silva et al., 2014). According to the previous
270
studies, among EAAs, leucine and lysine were reported in the greatest quantities from several
271
countries (Table 3). In the viewpoint of human nutrition, lysine – the limiting amino acid in
272
cereals is present in adequate amount and interestingly, tryptophan is reported in surprisingly
273
higher amount (0.70-14.80 g/100 g) in Chinese bee pollen which is otherwise the limiting amino
274
acid in pulses (Yang et al., 2013). Pollen also contains the threonine - the second rate-limiting
275
amino acid which is along with isoleucine and phenylalanine is known as glucogenic as well as
276
the ketogenic amino acid, respectively (Dong et al., 2018). Being the precursor of arserine,
277
carnosine, and histamine, the histidine is also important owing to the response of synthesized
278
histamine for allergic reactions and plays a great role in the dilation and blood vessels
279
contraction (Peachey, Scott, & Gatlin III, 2018). Arginine is considered as an essential amino 12
280
acid in the present paper which is critical for child nutrition only. Thus, all EAAs are reported in
281
bee pollen (except a few studies) ranging from 12-45.02% of total amino acid content which is
282
comparable to the supply of essential amino acids (33.9%) as per FAO reference protein
283
(Komosinska-Vassev, Olczyk, Kafmierczak, Mencner, & Olczyk, 2015; Thakur & Nanda,
284
2018a).
285
3.2.4. Lipids and fatty acids
286
After carbohydrates and proteins, lipids are the third-largest constituent of bee pollen
287
which are vital for the generation of royal jelly (Sattler et al., 2015). Pollen from some botanical
288
species contains total lipid content, varying from 1-13% of pollen dry weight (Campos et al.,
289
2008), however, Martins, Morgano, Vicente, Baggio, and Rodriguez-Amaya (2011), Odoux et al.
290
(2012), de Melo et al. (2018a) and Liolios et al. (2019b) revealed even higher lipid content up to
291
13.32, 24, 13.50 and 13.60%, respectively as shown in Table 2. They are usually comprised of
292
triglycerides, carotenoids, and sterols in bee pollen (Mărgăoan et al., 2014; Sattler et al., 2015).
293
However, a few investigations focused on the sterols profile in bee pollen (Mărgăoan et al.,
294
2014) and most research work in the literature focused on the estimation of total pollen lipid
295
content (Table 2). The relative proportion and level of certain fatty acids are very important in
296
determining the quality of lipids because honeybees require fatty acids for reproduction,
297
development, and nutrition. The bactericidal and antifungal properties of linoleic, linolenic,
298
myristic, and lauric acids primarily hinder the multiplication of Paenibacillus and Melissococcus
299
pluton – the spore-forming bacteria and other microorganisms which may colonize the brood
300
combs otherwise, thus contributing to colony hygiene (Dong, Yang, Wang, & Zhang, 2015). The
301
human also requires lipids due to fraction of essential fatty acids (EFAs) and antioxidant
302
substances for growth, development and prevention of diseases (Glick & Fischer, 2013). Many
303
biological functions require EFAs for regulated levels of plasma lipids, insulin activity, 13
304
cardiovascular, and immune function, etc. to ensure better health (Glick & Fischer, 2013; Kaur,
305
Chugh, & Gupta, 2014).
306
Conte et al. (2017) reported a higher amount of phospholipids, tocopherols, and
307
phytosterols, recommending an intensive lipolytic process as the pollen characterization
308
parameter. In bee pollen, a strong correlation was suggested between the fatty acids (FAs)
309
composition and botanical species, however, Brazilian pollen of Mimosa caesalpiniaefolia and
310
Cestrum showed a negative association (de Melo, Freitas, Barth, & Almeida-Muradian, 2009;
311
Mărgăoan et al., 2014; Sattler et al., 2015). These findings suggested the association of certain
312
pollen with more or fewer lipids concentrations. Moreover, huge variations are reported in lipid
313
content of mono-floral pollen from different countries: Brassica napus - 4.7% (Brazil), 6.6 %
314
(China), 7.76% (Greece), 12.38% (India); Cistus sp. -1.9 % (Italy), 3.80% (Greece), 7.2 %
315
(Spain); Cocos nucifera–10.43 % (India), 4.6-5.1% (Brazil) (Table 2) (Domínguez-Valhondo,
316
Gil, Hernández, & González-Gómez, 2011; Yang et al., 2013; Sagona et al., 2017; de Melo et al.,
317
2018b; Thakur & Nanda, 2018a; Liolios et al., 2019b).
318
Nearly 20 FAs were reported in bee pollen from C4 to C24 among which ω-3 fatty acids
319
are dominating (Table S1). Myristic, stearic and palmitic acids are the major saturated fatty acids
320
while α-linolenic, linoleic and oleic acids are the most prevalent unsaturated fatty acids reported
321
in bee pollen. According to the literature, bee pollen of several countries contains α -linolenic,
322
palmitic, and linoleic acids in higher amount along with significant levels of arachidonic,
323
behenic, capric, caproic, caprylic, 11-eicosenoic, elaidic, lauric, lignoceric, myristic, oleic, and
324
stearic acids (Table S1). Zea Mays (mono-floral) pollen from China contained α-linolenic (52%)
325
and palmitic (25%) acids as predominant fatty acids while the same origin pollen from Egypt
326
was rich in oleic (42%) and myristic (40%) acid. Likewise, the γ-linolenic acid (29.08 %) and 14
327
eicosatrienoic acid (13.83%) were reported prevalent in Indian Brassica napus pollen whereas
328
the α-linolenic acid (30.82%) and myristic acid (20.70%) were present in higher amount in bee
329
pollen of the same origin from China (Yang et al., 2013; Thakur & Nanda, 2018a). Keeping in
330
view the previous studies, it is observed that fatty acids are the same in different pollen but their
331
proportion varies according to the floral sources or even within the same species and
332
geographical regions. It is believed that honeybees prefer the pollens which contain a higher
333
amount of unsaturated fatty acids compared to saturated ones. Thakur and Nanda (2018a)
334
reported the values of unsaturated: saturated fatty acid (UFA to SFA ratio) of bee pollen ranging
335
from 2.2-6.7 which refers to the high quality of bee pollen lipids. A higher value of UFA/SFA
336
demonstrates the reduced levels of fats and cholesterol, thereby preventing cardiovascular
337
disease, but if the value is below 1, the UFA/SFA ratio then exhibits the degradation of
338
unsaturated fatty acids during the time due to the storage and dehydration process. The UFAs are
339
an important component of membrane phospholipids and therefore helps to maintain the
340
membrane fluidity which will thus improve the membrane functionality and also cell metabolism
341
(Mărgăoan et al., 2014). Among fatty acids, the saturated, monounsaturated and polyunsaturated
342
fatty acids represented the 4.29-71.47%, 1.29-53.24%, and 4.33-75.71%, respectively in pollen
343
whereas ω-3 fatty acids varied from 8.07-44.1% and ω-6 fatty acids ranged from 1.77-38.25 % as
344
reported in several studies summarized in Table S1. Any fresh food is said to be the “source of
345
ω-3 FAs” if ω-3 fats are found in concentration 300 mg/100g under the regulation EC 1924/06 of
346
Europe; therefore, bee pollen can be regarded as a significant ω-3 FAs source for improved
347
human nutrition (Li et al., 2018). Further, the ω-6: ω-3 FAs ratio performs a critical role in the
348
eicosanoids synthesis in the human body thereby regarded as beneficial to health. ω-6:ω-3 ratio
349
is an important criterion to evaluate the health properties of food and it must be 5:1 or less 15
350
(Simopoulos & DiNicolantonio 2016). Bee pollen contained this ratio varied from 0.059-3.090;
351
thereby it is an essential source of ω-3 FAs in the human diet (Margaoan et al., 2014; Thakur &
352
Nanda, 2018a).
353
Bee pollen is the potential source of EFAs: α-linolenic and linoleic acid, however, its
354
amount varies according to the botanical origins (Komosinska-Vassev, Olczyk, Kafmierczak,
355
Mencner, & Olczyk, 2015). The amount of linoleic acid differed greatly like 3.25-11.32 g/100g
356
in bee pollen from India, 7.62-33.21 g/100g from Romania and 2.66-24.38 g/100g from China,
357
while the α-linolenic acid ranged from 0.5-16.28 g/100g from Indian bee pollen, 20.28-46.93
358
g/100g in Romanian bee pollen, and 4.11- 58.52 g/100g in Chinese bee pollen (Yang et al., 2013;
359
Mărgăoan et al., 2014; Thakur & Nanda, 2018a). Both EFAs are important to carry the metabolic
360
processes and also being present as the component of cell membranes thus improves the brain
361
function (Perini et al., 2010). Docosahexenoic acid, simply DHA (C22:6n-3) usually present in
362
fish oil is also reported in bee pollen. Nervonic acid – an important constituent of the white
363
matter of animal brains is mainly obtained from lipids of fish and crab eggs but its presence in
364
bee pollen from different botanical origins of multiple countries is a novel finding (Table S1),
365
revealing the pollen significance in human’s nervous system and brain development.
366
Bee pollen also contains minute levels of phospholipids and plant sterols (mainly β-
367
sitosterol) (1.5 and 1.1%, respectively) wherein β-sitosterol and triterpene compounds such as
368
oleanolic and ursolic acid reduces the cholesterol absorption in intestines and generation of
369
tumor diseases, respectively (Komosinska-Vassev, Olczyk, Kafmierczak, Mencner, & Olczyk,
370
2015).
371
3.2.5. Dietary fiber
372
The dietary fiber, also known as roughage refers to the portion of food which remains
373
intact throughout the stomach and small intestine thus contributing nothing to the nutritional 16
374
value of food but is essential to human health. The dietary fibers are basically of two types:
375
soluble and insoluble. The soluble dietary fiber (SDF) reduces the blood cholesterol and glucose
376
levels whereas the insoluble dietary fiber (IDF), also called resistant starch, supports the passage
377
of food through the digestive system thus increasing the stool bulk and preventing the irregular
378
stools or constipation.
379
The dietary fiber comes from sporopollenin, cellulose, hemicellulose, and pectin found in
380
the outer-covering of bee pollen while the starch and other insoluble polysaccharides such as
381
callose, cellulose, lignin, etc. constitute the crude fiber. However, the highest and lowest values
382
of crude fiber alter considerably (Table 2) due to various analytical methods and plant sources.
383
Enzymes hydrolyze the complicated fibrous pollen structures and release sugars to harness as a
384
source of carbon for bacterial fermentation (Bobadilla, 2009). However, the change in fiber
385
concentration due to fermentation is not significant from the nutritional quality viewpoint.
386
Bee pollen is a useful fiber source for food, with cellulose and callose as the main
387
portion. Total dietary fiber (TDF) ranged from 17.60-31.26% while the IDF and SDF values
388
varied from 73-82% and 0.86-5.92% of TDF in pollen from China (Yang et al., 2013). Likewise,
389
the Colombian pollen contained IDF contents higher (8.0- 13.9 g/100g) than the SDF (1.3-2.3
390
g/100g) with TDF of 9.9-15 g/100g (Bobadilla, 2009). However, Fuenmayor et al. (2014)
391
reported a higher amount of SDF 2.7± 1.8 g/100 g compared to IDF (11.7±3.3 g/100 g) in
392
Colombian pollen with TDF of 14.5 g/100 g. On the other hand, Domínguez-Valhondo, Gil,
393
Hernández, and González-Gómez (2011) studied the Spanish bee pollen which showed no
394
remarked variations in their dietary fiber (14.50-14.65% dry weight) and suggested the
395
exploration of pollen fiber in processed foods to reduce the lack of dietary fiber.
396
3.2.6. Minerals
17
397
The mineral or ash content is essential for retaining the cell protection, activities,
398
homeostasis, and health. For instance, calcium (Ca), phosphorus (P), and magnesium (Mg), in
399
combination, assists in the development and maintenance of bone tissue and regulating the blood
400
as well as intercellular and cellular fluids osmotic pressure while cobalt (Co), copper (Cu), iron
401
(Fe), manganese (Mn), and zinc (Zn) are crucial for the body growth, development, reproduction,
402
and blood formation. Hence, the insufficiency of these bio-elements may cause diverse metabolic
403
disorders, acute growth defects and even result in mortal illnesses (Prashanth, Kattapagari,
404
Chitturi, Baddam, and Prasad, 2015; Quintaes & Diez-Garcia, 2015).
405
The day-to-day mineral requirements for humans were recorded: Ca: 0.8-0.9 g, Cu: 1-3
406
mg, Fe: 10-20 mg, K: 800 mg, Mg: 300-400 mg, Mn: 4-5 mg, nickel (Ni): 15-25 µg, P: 0.8-1.2 g,
407
selenium (Se): 60-120 µg, and Zn: 6-22 mg (Tayar & Cibik, 2011; Demirci, 2014) whereas the
408
following daily mineral specifications have been suggested by Brazilian laws: Ca: 1000 mg,
409
chromium (Cr): 35 µg, Cu: 900 µg, Fe: 14 mg, K: 4700 mg, Mg: 260 mg, Mn: 2.3 mg, P: 700
410
mg, Se: 0.034 mg and Zn: 7 mg for an adult of 19-30 years age (Sattler et al., 2016). The bee
411
pollen possesses 2.5–6.5% ash content (Table 2) wherein above 25 minerals are present in it but
412
the amount of each essential mineral varies as per different floral sources and countries (Table
413
4). Ca, Cu, Cr, Fe, K, Mg, Mn, Na, P, and Zn were commonly reported in bee pollen globally
414
and other minerals like boron (B), molybdenum (Mb) and selenium (Se) are rarely present in bee
415
pollen of few origins ranging from 8.2–14, 0.1–4.6 and <0.01–4.5 mg/kg, respectively (Yang et
416
al., 2013; Sattler et al., 2016; Altunatmaz, Tarhan, Aksu, Barutçu, & Or, 2017).
417
Ash content is largely affected by many factors, mainly soil, climate, geographical origin,
418
and botanical species in terms of plant capacity to accumulate the mineral salts in its pollen
419
(Carpes, 2008). Formicki et al. (2013) and Yang et al. (2013) have suggested that soil type is the 18
420
main cause for variation in element composition of pollen. Liolios et al. (2019a) had analyzed
421
the similar pollen taxa (Sinapis arvensis and Cistus creticus) from ten different regions of
422
Greece and found significant differences in mineral content, particularly K and Ca thus proving
423
evidence of the effect of soil on the mineral content of bee pollen. Another important reason for
424
the mineral variation is the addition of nectar to pollen which may alter the level of certain
425
minerals (Kostic et al., 2015b). However, the drying process did not show any effect on the
426
amount of Ca, Cu, K, Mg, Na, and Zn, as observed by de Melo et al. (2016).
427
The mono-floral Brassica napus pollen from India and China contained K as 4700 and
428
3825 mg/kg, respectively, whereas the Brassicaceae based monofloral pollen from Serbia
429
contained the K content of 3200 mg/kg (Yang et al., 2013; Kostic et al., 2015b; Thakur & Nanda,
430
2018a). These days, Na consumption is increased among the population because of the raised
431
intake of processed foods. But, bee pollen doesn’t contain accelerated Na content (Thakur &
432
Nanda, 2018a). According to the literature, 25 g of bee pollen supplies a maximum of 10% of the
433
suggested intake of Na (2 g/day) by the World Health Organization (WHO, 2012). Generally,
434
most studies reported Na content below 1000 mg/kg but this value reached to 1466, 6223 and
435
8350 mg/kg in Brazilian, Turkish and Saudi Arabian bee pollen, respectively (Morgano et al.
436
2012; Taha, 2015; Kalaycıoğlu, Kaygusuz, Döker, Kolaylı, & Erim, 2017). However, Na level
437
was less than 400 mg/kg from more than 75% Brazilian pollen samples (Morgano et al., 2012; de
438
Melo et al., 2016). Therefore, pollen contains a higher K: Na ratio owing to higher K and lower
439
Na levels which is essential to maintain the optimum electrolytic balance in the body (Carpes et
440
al., 2009).
441
According to the Institute of Medicine (US) (2011), the daily Ca intake of 1000 mg is
442
suggested for a person of age 19-50 years and in the literature, the maximum Ca content (5752 19
443
mg/kg) was reported by Taha (2015). Bee pollen from Brazil had Ca content varying from 643 to
444
4670 g/kg (Carpes, Mourão, De Alencar, & Masson, 2009; Morgano et al., 2012; de Melo et al.,
445
2016). Through the phosphate (PO4−3) salts, Ca plays an important part in blood coagulation,
446
neuromuscular functions, the liberation of hormones, a large number of enzyme-mediated
447
mechanisms and bone and tooth formation beyond being an enzyme component. Investigations
448
supported that an adult may get 2-45% of recommended Mg intake which is 260 mg/day from 25
449
g bee pollen. Recent pieces of evidence suggested that osteoporosis and related bone damages,
450
artery hardening or calcification is the result of elevated Ca and low Mg intakes (Lee, Kim, Kim,
451
Seo, & Song, 2014). Likewise, Fe when consumed in inadequate amounts, causes the behavioral
452
and developmental disorders, anemia, and poor immune system. Bee pollen is a good source of
453
iron and studies revealed that pollen in 25 g may supply 2-220% of the recommended Fe intake
454
i.e. 14 mg/day. Fe is greater in bee pollen than other regular foods like bamboo shoot, cabbage,
455
cassava, cauliflower, mung beans, soybeans, and animal originated foodstuffs (Yang et al., 2013;
456
de Melo et al., 2018a). Similarly, bee pollen (25 g) can satisfy requirements of Zn to a maximum
457
of 120% otherwise its daily suggested consumption for an adult is 7 mg. Bee pollen also contains
458
the elevated Cu content and the positive association between levels of Zn and Cu and antioxidant
459
capacity (determined by DPPH and ORAC methods) was noted, however, Zn and Cu are not
460
considered antioxidant compounds. The reason for this may be an antioxidant enzyme named
461
Cu-Zn superoxide dismutase (Cu-Zn SOD) which is commonly found as cofactors in crops
462
(Mondola, Damiano, Sasso, & Santillo, 2016). Therefore, the presence of Zn and Cu may be
463
considered as an index for the existence of Cu-Zn SOD enzymes in bee pollen also. The lack of
464
Mn may cause deficiency diseases particularly in females which can be reduced by incorporating
465
Mn-rich bee pollen thus supplementing the diet (Panziera, Dorneles, Durgante, & Silva, 2011). 20
466
Se is the constituent of proteins that have a significant part in metabolic activities of thyroid
467
hormone, synthesis of DNA, reproduction and prevent the infection or injury caused due to
468
oxidative stress (Fairweather-Tait et al., 2011). Se content ranged from <0.001–0.445 mg/100g
469
in 154 Brazilian bee pollen samples; however, it was not reported in Chinese bee pollen
470
(Morgano et al. 2012; Yang et al., 2013).
471
Further, Taha (2015) recommended the mineral constituents of pollen as distinct markers
472
to trace the floral source and regulate its quality. However, sometimes due to insufficient
473
cleaning methods, impurities may present in pollen thus enhancing the ash content. Therefore,
474
the each mineral must be examined for its level in bee pollen using advanced and reliable
475
techniques like inductively coupled plasma-optical emission spectrometry (ICP-OES),
476
microwave plasma or inductively coupled argon plasma - atomic emission spectroscopy (MP-
477
AES or ICP-AES) and total reflection X-ray fluorescence (TXRF) which is an important quality
478
index (Yang et al., 2013; Kostić et al., 2015b; Formicki et al., 2013; da Silva et al., 2014; Thakur
479
& Nanda, 2018a).
480
3.2.7. Vitamins
481
Vitamins have a major part to synthesize the vital cofactors, enzyme, and coenzymes
482
based metabolic reactions (Mellidou et al., 2019). They can be found in their original form in
483
nature or exist as precursors or pro-vitamins. Bee pollen usually contains a higher amount of
484
water-soluble vitamins and carotenoids, presented in Table 4. On part of International Honey
485
Commission (IHC), the specifications for vitamin composition of pollen were suggested to be:
486
0.6–1.3 mg/100g thiamine, 0.6–2 mg/100g riboflavin, 4–11 mg/100g niacin, and 0.2–0.7
487
mg/100g pyridoxine whereas the vitamin B complex was also discussed by Mărgăoan,
488
Mărghitaş, Dezmirean, Mihai, and Bobiş (2010) and they reported the following levels of
21
489
thiamine: 0.6–1.3 mg/100g, riboflavin: 0.6–2.0 mg/100g, niacin: 4.0–11.0 mg/100 g, pantothenic
490
acid: 0.5–2.0 mg/100g and pyridoxine: 0.2–0.7 mg/100 g.
491
Very few studies (Table 4) have been conducted about the vitamin composition of bee
492
pollen, focused on Brazil and Thailand only. A high concentration of B-complex vitamins was
493
reported by de Arruda et al. (2013a) and de Arruda, Pereira, Estevinho, & de Almeida-Muradian
494
(2013b) in bee pollen from Brazil. Riboflavin, with involvement in the metabolism of lipids,
495
carbohydrates, proteins, pyridoxine, folic acid, and cobalamin has a significant function in
496
cellular respiration (Pinto & Zempleni, 2016). Niacin after riboflavin is the dominating among
497
B-complex vitamins, thus indicating it a promising supplement for pellagra (Chantarudee et al.,
498
2012). Some authors reported the insignificant amount of lipid-soluble vitamins and vitamin C.
499
However, Sattler et al. (2015) revealed the higher amount of ascorbic acid (6.03-79.70 mg/100g)
500
in Brazilian bee pollen, till date and determined four tocopherols - α, β, γ, and delta-tocopherol
501
with their respective mean values of 328, 0.21, 0.46 and 0.63 mg/100g. Vitamin E has been
502
shown to correlate strongly with b* value, and thus yellow-colored pollen might probably be
503
linked with α-tocopherol (Sattler et al., 2015).
504
β-carotene, also known as provitamin A has 1/6th biological activity of vitamin A and is
505
one of the antioxidant vitamins. Vitamin A in terms of β-carotene was reported in corn bee
506
pollen from Thailand (1.530 mg/100 g) (Chantarudee et al., 2012) and Southeastern Brazil (5.63-
507
19.89 mg/100g) (Oliveira et al., 2009). The difference in vitamin levels may be employed as an
508
indicator of the determination of plant source of pollen; however, the botanical origin, season
509
and processing conditions affect the vitamin composition (Farag & El–Rayes, 2016). Further, the
510
vitamin compounds due to their complexity and low concentration are quite difficult to detect
511
and quantify. Instead of optimizing the efficient extraction and purification process, however, the 22
512
development and validation of the quantification technique may significantly reduce the analysis
513
time, generate less waste and improve the quantification of certain compounds (de Arruda et al.,
514
2013a).
515
3.2.8. Polyphenols
516
Polyphenolic compounds refer to the main secondary plants’ metabolites ranging from
517
anthocyanins, flavonoids, flavonols, flavonones, tannins, etc. to phenolic acids. The phenolic
518
compounds exhibit several biological properties like anti-tumor, anti-aging, anti-inflammatory,
519
anti-diabetic, anti-cancer, etc. due to their function of regulating the enzymatic activity and
520
signal transduction, scavenging the free radicals, chelating the metal ions, and activating the
521
transcription factors and gene expression (Działo et al., 2016).
522
Usually, bee pollen of Portugal, USA, Brazil, China, Egypt, New Zealand, and Greece
523
had total phenolic content (TPC) and total flavonoid content (TFC) values ranging from 0.50-213
524
mg GAE/g and 1.00-5.50 mg QE/g, respectively (de Melo & Almeida-Murandian, 2017;
525
Karabagias, Karabagias, Gatzias, & Riganakos, 2018). Likewise, 56 bee pollen samples from
526
four different regions of Brazil had TPC and TFC values of 6.50–29.20 mg GAE/g and 0.30–
527
17.50 mg QE/g, respectively (de Melo et al., 2018a). TPC and TFC of bee pollen from different
528
botanical sources of several nations are summarized in Table 5. Recently, Kostić et al. (2019)
529
reported TPC and TFC in sunflower (Helianthus annuus) bee pollen of Serbia varying from
530
2907-3816 mg/kg GAE and 843-865 mg/kg QE, respectively which were higher than detected
531
for the same bee pollen of Slovakia (Fatrcová-Šramková, Nôžková, Máriássyová, & Kačániová,
532
2016). The possible reason for this would be the variation in climatic conditions and
533
geographical origin which influence the levels of phenolic compounds in plants (Tolić et al.,
534
2017). When pollen is exposed to poor air or cold conditions, there would be an improvement in
23
535
the biosynthesis of flavonoids during pollen generation and growth (Rezanejad, 2012;
536
Mohammadrezakhani, Hajilou, & Rezanejad, 2018).
537
The phenolic composition of bee pollen of distinct countries differs in geographical and
538
botanical backgrounds and possesses the flavonoids such as apigenin, epicatechin, hesperetin,
539
isorhamnetin, catechin, kaempferol, luteolin, quercetin, naringenin, etc. and phenolic acids like
540
chlorogenic acid, ferulic acid, caffeic acid, gallic acid, vanillic acid, syringic acid, p-coumaric
541
acid, etc. (Table 5). The rape bee pollen from China contained following biologically active
542
compounds: isorhamnetin, kaempferol, and its 3-O-glucosides, naringenin, rutin and quercetin
543
and its 3-O-glucosides (Zhang, Yang, Jamali, & Peng, 2016) whereas the same biologically
544
active compounds (except naringenin and rutin) were reported in Spain originated Cistus sp.
545
pollen (Maruyama, Sakamoto, Araki, & Hara, 2010). On the other hand, the apigenin, catechin,
546
epicatechin, kaempferol, luteolin, naringenin, rutin, and quercetin were detected in bee pollen
547
from Egypt (Mohdaly, Mahmoud, Roby, Smetanska, & Ramadan, 2015). The bee pollen of
548
Echium plantagineum from Spain possessed the glucosides of anthocyanins, delphinidin,
549
petunidinm, and malvidin (Sousa, Andrade, & Valentão, 2016). Silva, Rosa, and Vilas-Boas
550
(2009) reported isorhamnetin-3-O-(6″-O-E-p-coumaroyl)-β-D-glucopyranoside, for the first
551
time, in pollen collected by Melipona rufiventris – the stingless bee. Bee pollen usually contains
552
the following phenolic acids and their ester derivatives: caffeic, p-coumaric, ferulic, p-
553
hydroxybenzoic, gallic, protocatechuic, syringic, and vanillic acid. de Florio Almeida et al.
554
(2017) and Negri et al. (2011) revealed the complex rosmarinic acid dihexoside and amide
555
derivatives of hydroxycinnamic and ferulic acids while Karabagias, Karabagias, Gatzias, and
556
Riganakos (2018) reported the presence of isopimpinellin (furancoumarins), urolithin B
557
(hydroxycoumarins) and flavononols 3-O- or 7-O-glucosides (quercetin 3-O-rhamnosyl24
558
galactoside, quercetin 3-O-xylosyl-glucuronide, isorhamnetin-3-O-glucoside 7-O rhamnoside,
559
and quercetin 3-O-rutinoside) in commercial Greek pollen.
560
Polyphenolic compounds in bee pollen protect from biotic (microbial growth) and abiotic
561
(high temperature, synthesis of reactive oxygen species and UV radiation) stress by their
562
capacity to neutralize the free radicals. Polyphenol metabolism includes the breaking of
563
flavonoids into monomeric units in the stomach. Sometimes, in the small intestine, few flavonoid
564
glycosides would be absorbed as whole by Na-dependent glucose transporter 1 (SGLT1)
565
(Williamson, 2017). The flavonoids are mainly metabolized in the small intestine due to the
566
existence of metabolizing enzymes like lactase phlorizin hydrolase, broad-specific-β-
567
glucosidase, and UDP-glucuronosyl transferase which produce the metabolites like sulfates,
568
glucuronides, and O-methylated aglycones including epicatechin, hesperetin, luteolin,
569
naringenin, and quercetin (Rzepecka-Stojko et al., 2015). These metabolites enter the liver
570
through membranes of the small intestine resulting in multiple positive health effects. The
571
remaining absorption of flavonoids carries in colon containing gut microflora based enzymes
572
which would decompose the flavonoids into phenolic acids (Li et al., 2018). Being simpler in
573
structures, the phenolic acids are easily metabolized or absorbed in the liver. However, the
574
metabolism of polyphenols is quite unclear and further research work must be conducted
575
focusing the polyphenol metabolism in humans.
576
3.2.9. pH and titratable acidity
577
pH and titratable acidity are critical factors during pollen storage because they can
578
influence the stability and shelf life. Both values also indicate the dynamic microbial activity in
579
food (Nogueira, Iglesias, Feás, & Estevinho, 2012). The increased levels of pH and titratable
580
acidity in food are caused due to fermentation, particularly by Gram-positive bacteria. The pH
581
value varied from 3.49-6.33 showing the natural slightly acidic nature of bee pollen. Portuguese, 25
582
Greek, and Indian bee pollen had almost similar pH values of 4.3-5.2, 4.70, and 4.74-5.48,
583
respectively (Feás et al., 2012; Karabagias, Karabagias, Gatzias, & Riganakos, 2018; Thakur &
584
Nanda, 2018a). However, the free acidity ranged from 128-294 meq/kg which exhibited the
585
acidic character of Brazilian bee pollen (Martins, Morgano, Vicente, Baggio, & Rodriguez-
586
Amaya, 2011) while Colombian bee pollen contained 155 – 402 meq/kg free acidity (Fuenmayor
587
et al., 2014) which provides information regarding conversion of sugars into organic acids.
588
However, the free acidity was not acclaimed by Campos et al. (2008) as a product quality index
589
Furthermore, no substantial pH (4.11) and titratable acidity (256.9 meq/kg) difference
590
was caused while drying (60 °C) the pollen compared to fresh bee-pollen (pH- 4.16; titratable
591
acidity-245.6 meq/kg) but difference was significant for both variables when drying was carried
592
out at 40°C (pH - 4.02; acidity - 305.8 meq/kg) and 50 °C (pH - 4.04; acidity - 283.2 meq/kg).
593
This recommends that the temperatures below 60 °C may support some microbial activity that
594
raises titratable acidity and decreases pH values owing to their metabolic action (Zuluaga-
595
Domínguez, Serrato-Bermudez, & Quicazán, 2018).
596
4. Functional properties
597
The functional properties refer to the attribute(s) of food components or ingredients
598
except for its nutritional value which affects its utilization (Thakur & Nanda, 2018b). These
599
properties affect the finished product in terms of appearance, taste, and texture and consequently,
600
acceptance of the product. Bee pollen is typically multi-component colloidal system, made up of
601
biopolymers and a variety of particles, such as oil droplets, gaseous bubbles, lipid crystals, etc.
602
The nature and strength of interactions of active surface components with themselves and
603
other pollen compounds (lipids, ash, and carbohydrates) affect the properties of pollen system
604
(Dickinson, 2013). Bee pollen is known to have outstanding emulsifying characteristics, higher 26
605
carbohydrate solubility, and oil retention capacity. However, variation in pollen composition
606
owing to diverse botanical and geographical origin may alter the functional properties. Recently,
607
the addition of bee pollen in different food products, as reported in few studies, was successful
608
efforts for processing the pollen (Krystyjan, Gumul, Ziobro, & Korus, 2015; Zuluaga et al.,
609
2016; Conte, Caro, Balestra, Piga, & Fadda, 2018; Thakur & Nanda, 2019). However, its role as
610
a functional component in the food industry relies on the pollen functional characteristics which
611
therefore must be discussed in detail.
612
4.1. Solubility
613
The dissolution ability of any substance in water, called as solubility followed the
614
following process: (1) wettability of product, (2) disintegration of product into primary particles,
615
(3) material discharge from particles into the aqueous phase and consistent destruction of surface
616
layer simultaneously until the complete particle breakdown and (4) thorough dissolution of all
617
materials (Mimouni, Deeth, Whittaker, Gidley, & Bhandari, 2010).
618
Bee pollen has solubility ranging from 84.91-87.56 % which is majorly influenced by
619
nature and composition of protein and carbohydrates based on proportion between soluble (e.g.
620
salivary secretions, simple sugars, lower molecular weight proteins (50–25 kDa), vitamins, etc.)
621
and insoluble (e.g. cellulose, lignin, sporopollenin, lipids, higher molecular weight proteins, etc.)
622
constituents and corresponding interlinkages (Kostic et al., 2015a; Thakur & Nanda, 2018b). The
623
pollen protein and carbohydrate solubility varied between 2.8 – 25.9% and 31.2 – 75%,
624
respectively (Kostic et al., 2015a). Protein solubility in pollen is similar to commercial
625
concentrated and isolated soy protein flours and also affects the other functional properties like
626
emulsification, foaming, and gelation (Kostic et al., 2015a). It is positively correlated to the
627
carbohydrates level however; the lipid and ash contents adversely affect the protein solubility. It
628
is also associated with the protein composition, conformation, their interaction with other 27
629
constituents and processing conditions. Kostic et al. (2015a) reported the three limits viz. higher
630
(80-50 kDa), moderate (50-25 kDa) and lower range (25-10 kDa) molecular weight proteins
631
which accounted for 13.40-32.20, 22.20-43.60 and 32.90-63.40% of soluble proteins (Kostic et
632
al., 2015a). The higher levels of 80-50 kDa molecular weight proteins were reported to
633
negatively affect the protein solubility. Compared to protein solubility, the carbohydrate
634
solubility was higher in bee pollen due to the presence of nectar (comprising mainly water-
635
soluble sugars), starch and pectin and it can be affected by the proportion of soluble and
636
insoluble carbohydrates and their association with other components. The correlation test showed
637
the positive association of protein and lipid content with carbohydrate solubility (Kostic et al.,
638
2015a).
639
Another important factor affecting solubility is wettability and dispersibility which were
640
examined by Thakur and Nanda (2018b) and varied between 285.67-1,909.46s and 34.10 –
641
51.06%, respectively. The enormous difference in pollen wettability and dispersibility is caused
642
due to pollen chemical constituents, surface area properties, variation in cultivar, and
643
arrangement, texture, and configuration of each pollen grains. The correlation studies by Thakur
644
and Nanda (2018b) exhibited a strong negative relationship between the surface area and
645
wettability of bee pollen.
646
4.2. Water and oil holding capacity (WHC)
647
It is essential for products where the retention of moistness is associated with quality.
648
Food ingredients that have high WHC may make the product dry and brittle, mainly during
649
storage. WHC of bee pollen ranged from 0.47-2.25 g/g and this difference in WHC is mainly due
650
to hydrophilic components such as polar groups of insoluble proteins and carbohydrates which
651
are reported in 3-D structures and correspondingly bind the water molecules through capillary 28
652
action (Kostic et al., 2015a; Thakur & Nanda, 2018b). Further, the lipid molecules which have
653
polar and charged regions may account for improved water holding. Therefore, variation in the
654
composition of protein, carbohydrate, and lipid indicates the significant differences in WHC of
655
pollen.
656
Oil holding capacity (OHC) is the degree of physical capture of oil by food constituents
657
on the grounds of composite capillary-attraction process and ranged from 1.00–3.53 g/g in bee
658
pollen (Kostic et al., 2015a; Thakur & Nanda, 2018b). Thakur and Nanda (2018b) revealed the
659
strong correlation between OHC and cohesiveness of bee pollen. OHC is affected by several
660
inherent variables like amino acid composition, hydrophobicity and protein conformation.
661
Further, the sporopollenin is structurally similar to fatty acid-lignin-like material entangles the
662
oil in the matrix thus contributing to OHC. The higher value of OHC in any product would
663
enhance its applications. Thakur and Nanda (2018b) recommended the coconut pollen to
664
improve mouthfeel and retain the flavor which showed its probability to utilize in different
665
formulations as a functional component.
666
WHC to OHC ratio, (known as water-oil holding index - WOHI) reveals the equilibrium
667
between hydrophilic and lipophilic constituents of pollen and is lower than 1 which indicates its
668
superior lipophilic properties. Moreover, no correlation of WHC or OHC was obtained with
669
other functional properties and carbohydrates, lipids or protein contents which demonstrate the
670
complexity of interactions among them (Kostic et al., 2015a; Thakur & Nanda, 2018b).
671
4.3. Emulsifying properties
672
Emulsion usually provides the desired mouthfeel and is essential in the structural
673
development of foods such as frozen desserts, beverages, coffee whiteners, mayonnaise, etc.
674
(Serdaroğlu, Öztürk, & Kara, 2015). Emulsifying properties of bee pollen including emulsion
675
activity and stability ranged from 44.83-46.76 % and 21.62-26.32 %, respectively (Thakur & 29
676
Nanda, 2018b). The emulsifying properties are influenced by amount, conformation,
677
hydrophobicity, and solubility of proteins; size and distribution of liquid droplets; phase volume
678
ratio; pH, temperature and salt level of solvents and continuous phase viscosity (Avramenko,
679
Low, & Nickerson, 2013). The correlation studies by Kostic et al. (2015a) reported the
680
significant positive association between emulsion stability and protein solubility while emulsion
681
activity was negatively linked to protein solubility. The protein with molecular weight 50-25 kDa
682
account for the emulsion stability while higher molecular weight proteins are negatively linked
683
thus indicating that oil/water interface can adsorb smaller protein molecules better to produce
684
stronger interfacial layers compared to larger molecules (Kostic et al., 2015a). Further, emulsion
685
stability and activity shared a negative correlation due to stabler emulsions formation having
686
greater adsorbed substances at the interface.
687
Usually, natural food emulsifiers are proteins but polar lipids may have good potential for
688
better emulsifying properties. The interfacial material of oil/water emulsion is comprised of
689
proteins, phospholipids, monoglycerides, esters of lipid acids, or mixture thereof. All these
690
compounds are present in pollen but in varying proportions due to plant sources (Liang, Zhang,
691
Shu, Liu, & Shu, 2013). Further, pollen contains bioelements like K, Ca and other complex
692
carbohydrates that blend with interfacial compounds to create either stabilization or
693
destabilization properties. Hence, the main reason for lower coefficient values of associations of
694
pollen emulsion activity/stability with protein solubility is the surface-active elements and their
695
interactions (Kostic et al., 2015a).
696
4.4. Foaming properties
697
Foam refers to the systems which are formed by entrapping the gas molecules in large
698
amount inside the thin film of liquid or solid. Several food products like bread, cakes, ice-cream,
699
and whipped toppings are dependent on the foam to maintain the structure and texture. The 30
700
retention of foam in the definite state is a tough task than emulsions due to the different
701
microstructure of foam bubble and its surroundings than an emulsion droplet (Green, Littlejohn,
702
Hooley, & Cox, 2013).
703
The bee pollen from Serbia did not possess any foam producing capacity while the Indian
704
bee pollen had foam capacity and stability ranged from 6.21-8.69 % and 17.50-20.00 % (Kostic
705
et al., 2015a; Thakur & Nanda, 2018b). Foaming capacity is strongly associated with proteins
706
that can reduce the water-air interface surface tension and produce a constant cohesive film
707
within the foam surrounding the air bubbles (Kaushal, Kumar, & Sharma, 2012). Thakur and
708
Nanda (2018b) recommended the use of Indian bee pollen in foam derived formulations such as
709
marshmallows, cakes, ice-creams, mousses, whipped cream, etc., whereas Kostic et al. (2015a)
710
suggested the pollen utilization as a foam depressant.
711
5. Food applications of bee pollen
712
Owing to its well-recognized nutritional and therapeutic properties, bee pollen is usually
713
consumed as a natural dietary supplement either in fresh or dried form. Recently, the researchers
714
have focused to utilize the bee pollen in food systems, not only as a nutritious ingredient but also
715
as a functional component to enhance the product quality characteristics. Yerlikaya (2014)
716
incorporated the bee pollen into fermented milk beverages and reported that antimicrobial
717
activity was exhibited by pollen when added in range 10-20 mg/mL. The supplementation of
718
fermented beverages with pollen also enhanced the probiotic viability and beverage viscosity
719
without affecting the sensorial attributes. Similarly, acidophilus milk and probiotic yoghurt were
720
also enriched with bee pollen (0.6% w/w) wherein the lactic acid production was increased,
721
regardless of fat level (Glušac, Stijepić, Milanović and Đurđević-Milošević, 2015). The use of
722
bee pollen in bakery products is trending where Krystyjan, Gumul, Ziobro and Korus (2015) had 31
723
fortified the biscuits and Conte, Del Caro, Balestra, Piga and Fadda (2018) supplemented the
724
gluten-free bread using bee pollen. Wheat flour when substituted with 10% bee pollen, the
725
prepared biscuits contained significantly increased levels of protein, sugar, ash, fiber
726
polyphenols, and antioxidant potential; however, 5% of pollen was needed to provide taste
727
similar to the control samples of biscuits (Krystyjan, Gumul, Ziobro and Korus, 2015). On the
728
other hand, Conte, Del Caro, Balestra, Piga and Fadda (2018) showed an improvement of
729
techno-functional properties, decreased rate of staling, and an increase in overall organoleptic
730
acceptability of bread without any destruction to dough development and leavening attributes
731
when enriched with bee pollen from 3-5%. These studies can provide a base for further
732
exploration of bee pollen as a promising ingredient in other bakery products.
733
Some recent studies recommended the bee pollen as a natural antioxidant substitute to
734
inhibit the fat oxidation in black pudding and refrigerated pork sausages which are attributed to
735
the increased antioxidant potential and higher levels of phenolic compounds (de Florio Almeida
736
et al., 2017; Anjos et al., 2019). Zuluaga et al. (2016) revealed an increase in bioactive
737
compounds, mainly carotenoids and antioxidant potential of pineapple juice under pressure (400
738
MPa for 15 min) whereas Karabagias, Karabagias, Gatzias, and Riganakos (2018) reported an
739
increase in total phenolic content and antioxidant capacity of bee pollen yogurt in addition to
740
improvement of end product cohesion and organoleptic characteristics. Similarly, Thakur and
741
Nanda (2019) developed the polyphenol-rich vacuum-dried milk powder using rapeseed bee
742
pollen which may have potential in the formulation of processed products as a functional
743
component. Further applications of bee pollen in food products are thus based on thorough
744
assurance about its nutritional value, bioactive compounds, techno-functionalities, organoleptic
745
attributes, and safety. There is also a need to compare the effect of adding the monofloral and 32
746
multifloral bee pollen to food products for better understanding the impact of botanical source on
747
product quality.
748
6. Safety aspects of bee pollen
749
Bee pollen intake is highly recommended as a natural dietary supplement on account of
750
its outstanding nourishing and healthy nutrients; however, few risks are also associated with its
751
intake due to the presence of potential contaminants like bacterial and fungal toxins, heavy
752
metals, pesticides, and allergic response. The poor and unhygienic production and storage
753
conditions of bee pollen may favor the microbial spoilage due to yeasts, molds, total viable
754
count, lactic acid bacteria and Enterobacteriaceae, which grows optimally at moderate
755
temperatures. This increases the health risk linked to intake of fresh pollen whereas the bee
756
pollen after drying are reported as microbiologically safe (Mauriello, De Prisco, Di Prisco, La
757
Storia, & Caprio, 2017). On exposing to the environment (anthropogenic pollution, water, and
758
soil), the bee pollen may accumulate toxic heavy metals. Several investigations reported the
759
presence of heavy metals like arsenic (As), cadmium (Cd), mercury (Hg), lead (Pb) and
760
strontium (Sr) (Roman, 2009; Kostić et al., 2015b; Dinkov & Stratev, 2016).
761
de Oliveira, do Nascimento Queiroz, da Luz, Porto, and Rath (2016) and Böhme,
762
Bischoff, Zebitz, Rosenkranz and Wallner (2018) reported the presence of 26 and 73 different
763
pesticides in bee pollen from Brazil and Germany, respectively. The exposure of pesticide-
764
contaminated bee pollen to humans may result in several chronic diseases like the neurological
765
deficit, respiratory diseases, cancer, etc. (Mesnage & Seralini, 2018). The mycotoxin
766
contamination is a greater concern where ochratoxin A is among the hazardous toxic substances
767
generated by Aspergillus (Bogdanov, 2017). Echium vulgare, Symphytum officinale, and Senecio
768
jacobaea bee pollen reported the pyrrolizidine alkaloids associated with hepatotoxic 33
769
characteristics (Kempf et al., 2010). Moreover, allergic reactions including anaphylaxis are
770
usually the immediate IgE-mediated hypersensitivity reactions which are identified after pollen
771
intake because individual pollen grains are collected from insect-pollinated plants as well as
772
wind-pollinated weeds or trees which may cause the allergic reactions due to accidental intake of
773
airborne pollens (Makris et al., 2010; Jagdis & Sussman, 2012; Choi, Jang, Oh, Kim, & Hyun,
774
2015). Recently, McNamara and Pien (2019) reported the relation of exercise-induced
775
anaphylaxis with pollen consumption in atopic individuals due to the reduction of threshold for
776
mast cell degranulation during exercise on account of enhanced gastrointestinal permeability or
777
osmotic effects and recommended that such individuals after pollen intake should skip exercise
778
for 4 -6 hours. Taking everything into account, it may be said that primary risks behind allergy of
779
bee pollen are blending of bee pollen with airborne-pollen allergens, fungal cross-reactive
780
allergenic substances, contamination with pesticides and exercise quickly after its intake.
781
Various international organizations such as WHO, FAO, and WTO - World Trade
782
Organization are responsible for establishing food quality and safety standards; however, there
783
are no harmonized global standards for bee pollen safety to date. A few countries like Argentina,
784
Bulgaria, Brazil, and Poland have established their guidelines for improving the quality
785
surveillance of pollen to increase safety. There is an urgent need to revise the bee pollen
786
guidelines by evaluating the botanical source, maximum residue limits (MRL) for heavy metals
787
and pesticides, microbial load and processing techniques before introducing the bee pollen in the
788
market. Further, labeling of bee pollen and any food containing bee pollen should include the
789
allergenic risk statements to avoid the risks for allergic individuals. Legal requirements also need
790
to be established and adapted for processing systems from the farm scale to pilot scale industries,
34
791
producers, and bee pollen processing stages. Moreover, effective training of beekeepers is very
792
much necessary by competent authorities so that the safety of bee pollen can be ensured.
793
7. Future trends
794
The research work on characterizing the bee pollen, based on physico-chemical and
795
functional properties, has been increased rapidly from the last 5 years. This may be due to the
796
huge demand for natural and healthy dietary supplements like bee pollen. Moreover, the use of
797
geographical index has further enhanced the horizon of bee pollen global market particularly for
798
properly analyzed distinct bee pollen from botanical source and geographical origin. The plenty
799
of pollen studies are focused in Brazil, Colombia and Romania attributed to their botanical
800
diversity. However, bee pollen is still a new term in many developing countries where even the
801
beekeepers are unaware of its potential as healthy food or functional ingredient or dietary
802
supplement. Therefore, the food industries, governments, and private organizations should come
803
forward to encourage the beekeepers to harvest the bee pollen which must be properly examined
804
for their properties before using in food processing. Further, the comprehensive composition of
805
bee pollen should be examined with a focus on the botanical and geographic origins using the
806
novel and advanced techniques with higher sensitivity, resolution, and accuracy. However, the
807
determination of functional properties of bee pollen is essential for its valorization. Only a few
808
studies have been reported in the literature highlighting the functional characteristics, however,
809
these properties are also affected by the botanical diversity and location. Therefore, scientists and
810
researchers must pay attention to study the mono-floral bee pollen which has a unique
811
composition. Also, there is a strong need to carry more research work to identify the mono-floral
812
pollen up to species level which is necessary for establishing the international quality parameters
813
of bee pollen. 35
814
8. Conclusion
815
Bee pollen as per nutritional and physico-chemical composition is an excellent source of
816
vital amino acids, ω-3 fatty acids, B-complex vitamins, minerals, and polyphenols; however, the
817
huge variation in composition due to the different botanical and geographical origin is still a
818
challenge to promote the bee pollen market. Proteins and its composition followed by lipid
819
characterization are mostly studied by the scientists and researchers with a mere focus on the
820
functional properties. Summarizing the data, bee pollen exhibited significant differences in
821
nutritional and physico-chemical composition as well as functional properties. Emphasis should
822
be given to study the mono-floral pollen of varying geographical and plant sources for
823
establishing their uniqueness as well as safety in the diet. Further intensive research should be
824
conducted to enrich the diversity of bee pollen for promoting its application in food processing
825
industries.
826
Acknowledgements
827
The authors thankfully acknowledge Mr. Rishi Ravindra Naik and Ms. Kirty Pant from
828
Department of Food Engineering and Technology, Sant Longowal Institute of Engineering and
829
Technology, Longowal (Punjab) India for assisting in modifying the corrections.
830
Conflicts of interest
831
The authors declare that there are no conflicts of interest.
832
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833
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834
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1386
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1387
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1399
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1402
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1410
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1411
Phenolic Extracts from Rape Bee Pollen and Inhibitory Melanogenesis by
1412
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1413
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1414
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1415
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1416
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1417
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1418
of bee-pollens from major floral sources in Al-Ahsa, eastern Saudi Arabia. Saudi Journal
1419
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1420
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1425
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1427
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1428
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1429
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1430
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1431
Effects of weather conditions on phenolic content and antioxidant capacity in juice of
1432
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1434 1435
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1436
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1437
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1438
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1443
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1444
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1447
acids
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1449 1450
1451 1452
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1454
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1455
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1457
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1458
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1467
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1468
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1470
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1471
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1472
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1474
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1475
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1476
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1477
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1478 1479 1480 1481 1482 1483 1484 1485 1486 1487 1488 67
1489
Table 1
1490
Average bee pollen composition and nutritional requirements as Required Daily Intake (RDI).
Nutrients
1491 1492 1493 1494 1495
Amount (%)
Average RDI
% RDI for 50 g of bee pollen
Carbohydrates (Fructose, 13-55 320* 3.33-15.34 glucose, sucrose, fibre) Crude fibre 0.3 – 20 30* 1.00-60.03 Protein 10 – 40 50* 18.01-73.37 Fat 1 – 13 80* 0.33-13.34 † # Potassium 400 – 2000 2000 16.68-90.04 Phosphorus 80 – 600† 1000# 6.67-53.36 † # Calcium 20 – 300 1100 1.67-23.34 350# 6.67-76.71 Magnesium 20 – 300† Zinc 3 – 25† 8.5# 33.35-263.46 Manganese 2 – 11† 3.5# 50.02-283.47 Iron 1.1 – 17† 12.5# 6.67-123.39 Copper 0.2 – 1.6† 1.2# 13.34-120.06 0.9# 100.05-2001 β-Carotene 1 – 20† Tocopherol 4 – 32† 13# 26.68-220.11 Niacin 4 – 11† 15# 23.34-66.70 † # Pyridoxine 0.2 – 0.7 1.4 13.34-43.35 1.1# 50.03-106.72 Thiamine 0.6 – 1.3† Riboflavin 0.6 – 2† 1.3# 40.02-140.07 Pantothenic acid 0.5 – 2† 6# 6.67-30.02 Folic acid 0.3 – 1† 0.4# 66.7-223.45 Biotin 0.05 – 0.07† 0.045# 100.05-140.07 100# 6.67-50.025 Ascorbic acid 7 – 56† Bee pollen composition is according to Campos et al. (2008) and RDI are according to the Reports of the Scientific Committee for Food (2010) and Denisow and Denisow-Pietrzyk (2016). † : Amount is given in mg/100g *: RDI is given in g/day #: RDI is given in mg/day
68
1496
Table 2
1497 1498
Summary of studies on physico-chemical properties of bee pollen from different botanical origins throughout the world and International standards for bee pollen quality. Country
Botanical source
Worldwide Literature Reports Italy Hedera helix L, Cistus incanus, Cornus sanguinea L., Cruciferae Brassica, Castanea sativa Miller, Lamiaceae L form, Fraxinus ornus L, Helianthus annuus, Papaver rhoeas L., Crataegus monogyna Jacq., Prunus, Rubus ulmifolius Schott, Gleditsia triacanthos L., Hedysarum coronarium, Trifolium alexandrinum, and Coriandrum sativum (n=32, dried pollen) Turkey (n=1, fresh and dried pollen)
Chemical composition LP CF (%) TM (%) (%)
MC (%)
CHO (%)
PT (%)
–
–
13.60 40.70
–
–
8.8028
61.96 78.70
12.43 30.36
5.50 7.22
–
69
References pH
aw
–
–
–
Castiglioni et al. (2019)
2.142.18
–
–
Isik, Ozdemir, & Doymaz (2019)
Greece
Erica manipuliflora, – Morus sp., Robinia pseudoacacia, Eucalyptus sp., Vicia sp., Phacelia tanacetifolia, Trifolium sp., Zea mays, Platanus sp., Pinus sp., Eryngium campestre, Erica arborea, Ranunculus sp., Laurus nobilis, Chenopodium sp., Helianthus annuus, Acer sp., Actinidia chinensis, Veronica persica, Convolvulus arvensis, Lamium sp., Salix sp., Polygonum aviculare, Centaurea calcitrapa, Cistus sp., Olea europaea, Papaver rhoeas, Portulaca oleracea, Hedera helix, Verbascum sp., Centaurea sp., Asphodelous sp., Aesculus hippocastanum, Amorpha fruticosa, Inula viscosa,
–
–
1.15 13.6 0
70
–
–
–
–
Liolios et al. (2019b)
Slovenia
Brazil
centaurea solstitialis, Pyrus communis, Pastinaca sativa, Chondrilla juncea, Cirsium sp., Cichorium intybus, Brassica napus, Brassica nigra, Taraxacum officinale, Sisymbrium irio, and Echinops ritro (n=46, fresh pollen) 14.80Brassicaceae, Castanea sativa, 32.10 Hedera helix, Fagopyrum esculentum, and multi-floral (n=28, fresh pollen) Mimosa caesalpiniifolia, Eucalyptus, Rubiaceae, Astrocaryum aculeatissimum, C. nucifera, M. verrucosa, Myrcia, Alternanthera, Asteraceae,
–
–
–
–
10.1021.37
–
–
–
Bertoncelj et al. (2018)
54.90 – 82.80
7.90– 32.20
3.20 – 13.5 0
–
1.90– 3.60
–
–
de Melo et al. (2018a)
71
Columbia, Italy and Spain
Greece
Anadenanthera, and Brassica asmonofloraland other multi-floral samples (n=56, dried pollen) Alternanthera, Anadenanthera; Cocos nucifera; Mimosa caesalpiniaefolia; Myrcia; Mimosa scabrella, Mimosa scabrella and Mimosa scabrella (n=8, dried pollen) (n=25, fresh pollen)
–
Multi-floral (n=3, commerical pollen)
14.9015.50
Commerical bee pollen (Papaver rhoes, Chamomila recutita, Sinapis arvensis, Cistus sp., Trifolium sp., Dorycnium sp., Cichorium sp., Convolvulus sp., Circium sp., Malva sylvestris, Fumana
–
–
–
10.60 33.90
3.20 8.30
–
2.603.80
–
–
de Melo et al. (2018b)
18.50 4.509.90 45.00 37.70 14-24 44.10 61 17.60
2-6
–
–
4.90-5.90
–
2.50 -6
–
1.802.10
–
–
7
8.40
2.28
4.70
–
Duarte, Vasconcelos, Oda-Souza, Oliveira, & López (2018) Gardana, Del Bo, Quicazan, Corrrea, & Simonetti (2018) Karabagias, Karabagias, Gatzias, & Riganakos (2018)
72
Brazil
Romania
India
Brazil
Republic
sp., Eucalyptus camaldulensis, Anemone sp., Ononis sp., Asphodelus sp., Quercus ilex) (n=1, commercial pollen from Attiki Bee Culturing Co.-Alex Pittas S.A., Athens, Greece) Cocos nucifera (n=1, 24.40* dried pollen) Brassica sp, 16.92Carduus sp., 31.08 Helianthus annuus, Prunus L. sp., Crataegus monogyna and bifloral and multifloral (n=10, fresh pollen) Cocos nucifera, 12.72Coriandrum 19.59 sativum, Brassica napus and Multifloral (n=35, fresh pollen) Commercial bee 3.06pollen (n=62, dried 8.12 pollen) Actinidia arguta and
4.4-
–
13.15
2.70
–
2.54
4.00
–
23.31 48.63
13.16 24.14
1.33 5.47
–
1.342.81
–
–
46.16 42.33
19.63 25.39
7.14 12.3 8
3.054.31
2.273.45
–
15.49 34.73
–
1.914.61
–
–
de Arruda et al. (2017)
–
23.2-
3.25 10.9 6 7.0-
3.1-4.2
5.2-5.3
–
–
Ghosh and Jung
73
Negri, Barreto, Sper, Carvalho, & Campos (2018) Spulber et al. (2018)
4.74-5.48 0.39-0.47 Thakur and Nanda (2018a)
of Korea Italy
Brazil
Quercus (n=2, dried pollen) Rubus, Cistus, Castanea, and Hedera (n=5, fresh pollen) (n=2, dried pollen)
Eucalyptus, Asteraceae, Mimosa caesalpiniaefolia,Pip er, Elephantopus, Cyperaceae and Anacardiaceae (n=4, dried pollen) (n=21, fresh pollen) Italy
Serbia
Brazil
13.8
26.5
4.5
(2017)
8.529.5
44.861.3
21.328.7
0.91 -2.2
–
1.9-3.0
–
–
Sagona et al. (2017)
37.1253.39*
25.66 44.27
24.00 37.63
9.3013.65
2.744.03
3.343.70*
0.850.91*
Rebelo, Ferreira, & Carvalho-Zilse (2016)
–
–
8.311.4
6.47 10.8 1 6.68.2
–
–
–
–
de Melo et al. (2016)
36.0± 2† 10.7512.03
–
21±2
–
3.6±1. 4† –
4.9±0. 3† 2.552.85
3.49±0.0 4† –
0.86±0.0 2† –
Bárbara et al. (2015)
–
1.183.32
–
–
Kostic et al. (2015a)
-
1.7-2.3
–
–
Sattler et al. (2015)
Castanea, Rubus and Cistus (n=3, fresh pollen) Brassicaceae, Salix, 4.35Fabaceae and multi- 14.35 floral samples (n=3, fresh pollen) Andira, Rubiaceae, 16.1Asteraceae, 18 Mimosaceae, (fresh) Fabaceae, and Aquifoliaceae, 2.8Anacardiaceae, 3.6 Myrtaceae, (dried)
†
54.84 57.98 64.42 81.84
25.87 28.42 14.81 27.25
1.92 2.83 1.31 6.78
–
15.322.9
1.93.9
74
Gabriele et al. (2015)
Saudi Arabia
Colombia India, China, Romania, Spain, Bulgaria, Hungary and Poland
Brazil
Caesalpineaceae, Brassicaceae, and others (n=21, dried pollen) Cucurbita pepo Thunb, Phoenix dactylifera, Helianthus annuus., Brassica napus and Medicago sativa (n=5, dried pollen) Multi-floral (n=196, dried pollen)
Commercial bee pollen (n=9, commercial pollen)
Bee pollen samples collected during summer, spring, autumn and winter (n=48, dried pollen) Arecaceae, Cecropia, Cestrum, Cyperaceae, Eucalyptus, Ilex, Myrcia, Piper, Vernonia, and Trema (n=7, dried pollen)
9.1610.5
14.71 19.45
1.82 5.38
0.151.70
1.883.88
–
–
–
16.132.1
2.89.7
7.818.1
1.5-3.2
3.8 -5.4
–
2.09.1
–
15.826.1
4.98.0
4#
–
18.66 24.39
3.163.99
–
22.15 25.11
1.811.8
–
Taha (2015)
Fuenmayor et al. (2014)
8-14.5
1.5-4.3
4.3-5.4
–
2.26 4.95
1.814.05
–
–
–
Negrão et al. (2014)
4.57 6.13
–
2.773.24
–
–
de Arruda, Pereira, de Freitas, Barth, & de AlmeidaMuradian (2013a)
75
China
Egypt
Thailand
Portugal
Brassica napus, Citrullus lanatus, Camellia japonica, Dendranthema indicum, Fagopyrum esculentum, Helianthus annuus,Nelumbo nucifera Gaertn, Papaver rhoeas, Rosa rugosa, Schisandra chinensis, Vicia faba, and Zea mays (n=12, commercial pollen from Zhenzhou Kerun Apiculture Co., Ltd., Zhenzhou, Henan Province, People's Republic of China) Zea mays, Trifolium alexandrinum, and Phoenix dactylifera (n=3, fresh pollen) Z. mays (n=1, dried pollen) Multi-floral (n=10, dried pollen) Cistus and Multi-floral including
other
1.827.52
59.43 77.82
14.26 28.95
0.66 6.56
17.6031.26
1.675.01
–
–
Yang et al. (2013)
11.9128.15
–
12.35 38.06
0.41 1.09
–
1.727.75
–
–
Khider, Elbanna, Mahmoud, & Owayss (2013)
7.03
64.42
19.12
7.00
0.86
2.43
–
–
4.336.67
–
2.313.99
61.270.6
2.60 3.32 4.36.3
–
–
24.23 34.18 19.127.1
–
2-4
4.3–5.2
0.210.54
76
Chantarudee et al. (2012) 4.33-6.33 0.32-0.55 Estevinho et al. (2012) Feás et al. (2012)
Romania
Portugal and Spain
France
Boraginaceae, Rosaceae, Fagaceae, Asteraceae, Fabaceae, Ericaceae, Mimosaceae and Myrtaceae (n=22, dried pollen) (n=16, fresh pollen)
Cistaceae, Fabaceae, Ericaceae, Fagaceae, and Boraginaceae (n=8, commercial pollen) Zea mays, Papaver, Sinapis, Sorghum, Helianthus, Daucus/Ammi, Cichorium, Brassica napus, Hypericum, Polygonum, Plantago, Veronica, Reseda, Platanus, Elaeagnus, Berberis, Viburnum, Aesculus, Laurus, Tamaris, Vicia, Onobrychis, Taraxacum,
16.27 2.13 -8.93 26.50
–
1.753.25
–
69.68 84.25
12.50 25.15
2.35 3.06
-
0.503.16
4.235.17
–
16.70 29.90
7.50 24.4 0
–
–
–
17.5929.55
–
6.028.40
–
77
Mărgăoan, Al. Mărghitaş, Dezmirean, Bobiş, & Mihai (2012) 0.26-0.43 Nogueira, Iglesias, Feás, & Estevinho (2012) –
–
Odoux et al. (2012)
Spain
Brazil
Fraxinus, Liliaceae, Ficaria and Quercus (n=52, fresh pollen) Cistus ladanifer, multifloral and commercial bee pollen (n=5, fresh and dried pollen) Commercial bee pollen samples (n=154, dried pollen)
Colombia
Dry and wet Multifloral samples (n=2, dried pollen) Brazil Asteraceae and other multi-floral pollen (n=36, dried pollen) Brazil Mimosa caesalpiniaefolia, Myrtaceae and other multi-floral (n=6, dried pollen) International Standards Argentina – Brazil
–
France
–
–
–
17.64 16.08
2.86 3.71
14.5014.65
–
–
3.009.39
–
12.28 27.07
–
1.334.13
–
5.5719.90
–
16.323.8
6.908.60
–
4.6364.830
3.454.85
–
–
–
–
1.502.99
–
18.55 22.60 19.98 28.28
4.01 13.3 2 5.36 6.69 4.59 5.07 4.53 5.69
–
2.893.30
–
–
de Melo, Freitas, Barth, & AlmeidaMuradian (2009)
<8 (dried) <4 (dried) <30 (fresh) <6 (dried)
–
15-28
–
–
<4
4-6
–
–
>8
>1.8
–
<4
–
–
Alimentos azucarados (2010) Instrução normativa N.º 3 (2001)
–
10-41
1-10
–
2-6
78
0.100.66
DomínguezValhondo, Gil, Hernández, & González-Gómez (2011) – Martins, Morgano, Vicente, Baggio, & Rodriguez-Amaya (2011) 0.27-0.72 Bobadilla (2009)
0.37-0.38 Carpes et al.(2009)
–
de Arruda, Pereira, de Freitas, Barth, & de Almeida-
1499 1500 1501 1502 1503
Mexico
–
4.5-8
–
12-18
Switzerla nd
–
<6 (dried)
–
10-40
2.56.5 1-10
–
1.5-2.2
>4
–
–
2-6
–
–
MC: Moisture content, CHO: Carbohydrates, PT: Proteins, LP: Lipids, CF: Crude Fibre, TM: Total minerals, aw: water activity *: Fresh bee pollen #
: Fixed moisture content
†
: Average value±standard deviation
1504 1505 1506 1507 1508 1509 1510 1511 1512 1513 1514 1515 79
Muradian (2013a) Fuenmayor et al. (2014) Lebensmittelverordn ung 817.02 (2005)
1516
Table 3
1517
Summary of sugars and amino acid composition (g/100g) of bee pollen from different botanical origins throughout the world. Sugars (g/100g)
Country
Slovenia
Botanical source Brassicaceae, Castanea sativa, Hedera helix, Fagopyrum esculentum, and multi-floral
References Glucose
Fructose
Sucrose
Maltose
11.94-28.49
13.17-26.48
0.05-0.28
0.16- 6.03
Bertoncelj et al. (2018)
Columbia, Italy and Spain
Multi-floral
14‒16
17.1
5‒6
–
Gardana, Del Bo, Quicazan, Corrrea, & Simonetti (2018)
Greece
Actinidia chinensis, Castanea sativa, Chenopodium album, Cichorium intybus, Cistus creticus, Convolvulus arvensis, Ecballium elaterium, Erica manipuliflora, Inula viscosa, Hedera helix, Lamium amplexicaule, Marticaria chamomilla, Oryza sativa, Papaver rhoeas, Parthenocissus inserta, Phacelia tanacetifolia, Pinus halepensis, Polygonum aviculare, Portulaca oleracea, Ranunculus arvensis, Robinia pseudoacacia, Rubus ulmifolius, Salvia verbenaca, Silybum marianum, Sisymbrium irio, Sonchus asper, Tamarix parviflora, Taraxacum officinalis, Tilia intermedia, and Tribulus
13.59-27.69
15.53-33.48
0.10-8.24
0.26-3.66
Liolios et al. (2018)
80
terrestris
2.77-20.90
8.08-25.71
–
–
de Arruda et al. (2017)
13.3-18.2
18.7-26.9
–
–
de Melo et al. (2016)
Brazil
Andira, Rubiaceae, Asteraceae, Mimosaceae, Fabaceae, Aquifoliaceae, Anacardiaceae, Myrtaceae, Caesalpineaceae, Brassicaceae, and others
6.3-7
4.9-5.5
–
–
Sattler et al. (2015)
Colombia
Multi-floral
11.6-20.3
4.5-9.0
–
Fuenmayor et al. (2014)
Thailand
Z. mays
6.42
0.60
0.53
Chantarudee et al. (2012)
Brazil
Colombia
Commercial bee pollen Eucalyptus, Asteraceae, caesalpiniaefolia, Piper, Cyperaceae and Anacardiaceae
Mimosa Elephantopus,
18.1-21.3
7.16
Romania
-
4.37-16.14
8.44-15.39
–
–
Mărgăoan, Al. Mărghitaş, Dezmirean, Bobiş, & Mihai (2012)
Spain
Cistus ladanifer and commercial multifloral bee pollen
22.47-26.86
19.88-23.78
3.04-8.55
–
DomínguezValhondo, Gil,
81
Hernández, & GonzálezGómez (2011)
Brazil
Commercial bee pollen
6.99-21.85
12.59-23.62
–
–
Martins, Morgano, Vicente, Baggio, and RodriguezAmaya (2011)
Colombia
Dry and wet Multi-floral
11.94-20.27
15.65-20.34
4.42- 9.02
–
Bobadilla (2009)
Amino Acids Essential amino acids Country
Botanical source
References Arg
Saudi Arabia
Colombia, Spain and Italy
His
Summer squash, date palm, rape 0.28- 0.32sunflower, and alfalfa 0.42 0.63
Multi-floral
0.96- 0.494.64 0.68
Ile
Leu
Lys
0.460.72
0.970.13
0.64- 0.040.89 0.07
0180.64
0.471.34
82
Met
0.39- 0.190.87 0.21
Phe
Thr
Trp
Val
0.120.31
0.400.52
0.050.12
0.830.99
Taha et al. (2019)
0.290.70
Gardana, Del Bo, Quicazan, Corrrea, & Simonetti (2018)
0.440.87
0.100.31
0.110.15
India
Cocos nucifera, Coriandrum 0.97- 0.35sativum, Brassica napus and Multi1.19 1.23 floral
Republic of Korea
Actinidia arguta and Quercus
Brazil
Senna sp, Chamaecrista sp Mimosa tenuiflora
China
Brassica napus, Citrullus lanatus, Camellia japonica,Dendranthema indicum, Fagopyrum esculentum, 0.72- 0.42and Helianthus annuus, 2.58 0.93 Nelumbo nucifera Gaertn, Papaver rhoeas, Rosa rugosa, Schisandra chinensis, Vicia faba, and Z. mays
and
0.381.01
1.762.47
1.35- 0.122.01 0.47
0.920.65
0.531.04
0.260.46
0.711.03
Thakur and Nanda (2018a)
0.21.2
0.40.9
–
0.91.4
Ghosh and Jung (2017)
1.11.5
0.40.6
0.91.3
1.5-2
0.71.2
0.03
0.07
0.010.02
0.06
0.03- 0.010.05 0.02
0.030.04
0.020.03
–
0.030.04
da Silva et al. (2014)
0.561.33
0.792.06
0.70- 0.121.55 0.62
0.461.30
0.430.99
0.7014.80
0.641.57
Yang et al. (2013)
Ser
Tyr
Asn
Gln
0.710.89
0.130.29
–
–
Taha et al. (2019)
0.090.23
Gardana, Del Bo, Quicazan, Corrrea, & Simonetti
-–
Non-essential amino acids Ala Saudi Arabia
Colombia, Spain and Italy
Asp
Summer squash, date palm, rape 1.13- 1.42sunflower, and alfalfa 1.35 1.65
Multi-floral
0.43- 0.211.19 0.46
Cys
Glu
Gly
0.120.24
1.321.84
1.47- 0.031.76 0.06
0.070.09
0.130.29
83
Pro
0.08- 16.20.25 19.8
0.230.47
0.360.89
0.290.49
(2018) Cocos nucifera, Coriandrum 1.59- 2.32sativum, Brassica napus and Multi2.33 2.81 floral
India
Republic of Korea
Actinidia arguta and Quercus
Brazil
Senna sp, Chamaecrista sp Mimosa tenuiflora
China
Brassica napus, Citrullus lanatus, Camellia japonica,Dendranthema indicum, Fagopyrum esculentum, 0.87- 1.13Helianthus annuus, Nelumbo 1.45 2.58 nucifera Gaertn, Papaver rhoeas, Rosa rugosa, Schisandra chinensis, Vicia faba, and Z. mays
1518 1519 1520
and
1.11.4
1.62.7
0.09
–
0.190.25
2.353.03
0.22- 2.081.84 2.52
0.520.91
0.360.44
–
–
Thakur and Nanda (2018a)
0.10.3
2.12.2
0.91.2
0.7
0.91.1
0.6
–
–
Ghosh and Jung (2017)
–
–
0.04
0.951.18
0.370. 43
0.030.04
0.080.10
0.020. 02
da Silva et al. (2014)
0.150.30
1.112.87
0.55- 0.951.25 5.95
0.511.25
0.280.85
–
–
Yang et al. (2013)
Arg: Arginine, His: Histidine, Ile: Isoleucine, Leu: Leucine, Lys: Lysine, Met: Methionine, Phe: Phenylalanine, Thr: Threonine, Trp: Tryptophan, Val: Valine, Ala: Alanine, Asp: Aspartic acid, Cys: Cysteine, Glu: Glutamic acid, Pro: Proline, Ser: Serine, Tyr: Tyrosine, Asn: Asparagine, Gln: Glutamine
84
1521
Table 4
1522 1523
Summary of mineral (mg/kg) and vitamins (mg/100g) composition of bee pollen from different botanical origins throughout the world.
Countr y
Minerals (mg/kg) Botanical source K
Ca
P
Mg
–
31827376
14013724
32576886
7891744
38- 76
Mimosa caesalpiniifolia, Eucalyptus, Rubiaceae, Astrocaryum aculeatissimum, C. nucifera, M. verrucosa, Myrcia, Alternanthera, Asteraceae, Anadenanthera, and Brassica as monofloral and other heterofloral pollen
34009800
9004100
–
6002400
30101
Alternanthera, Anadenanthera; Cocos nucifera; Mimosa caesalpiniaefolia; Myrcia; Mimosa scabrella, Mimosa scabrella and Mimosa scabrella
57009100
8003900
–
9002300
50.0899.0
Romani Brassica sp, Carduus sp., Helianthus annuus, Prunus L. a sp., Crataegus monogyna and
19804284
294.12437
–
286.120.211505 59.57
Brazil
Brazil
Brazil
85
Zn
Fe
–
Mn
Cu
Na
–
–
–
46-1180
25-215
7.419.7
20374
78.91017.5
43.5314
10-17.1
38279.3
21.73150.9
–
–
–
Cr
Referenc es
–
Costa et al. (2019)
–
de Melo et al. (2018a)
–
de Melo et al. (2018b)
–
Spulber et a. (2018)
bifloral and multifloral
India
Turkey
Cocos nucifera, Coriandrum sativum, Brassica napus and Multi-floral
36004100
Commercial bee pollen
992.1 22894. 14
Republi c of Actinidia arguta and Quercus Korea
Turkey
Chestnut, buckwheat, oak and multi-floral pollen
Nigeria
-
Brazil
Caesalpineaceae, Brassicaceae, Eucalyptus, Carica, Machaerium and Rubiaceae
1600-2 000
32004600
491.851472.1 0
795.8 95246. 99
10267 11670
19475041
24204932
909.02380
–
133.6
991.5948.3
910.0826.6
–
643722
76665174
44305240
8401050
271.1 21278. 34
17582737
25.2753.82
82.40243
36.3070.81
7.8212.81
14.8339.07
28.60725.36
8.1554.63
3.7314.99
96102
624.225.941083 49.74 44.0 – 72.0
–
86
0.13.0
29 -43
322-345
44.79161.4
2.6-4.3
58-312
53- 204
28-47
12.3640.46
7.22213.42
0.1-0.4
28 -62
0.4-0.5
6.813.1
150284
0.651.79
Thakur and Nanda (2018a)
–
0.341.59
Altunatm az et al. (2017)
106567
–
Ghosh and Jung (2017)
54976223
2.817.94
Kalaycıo ğlu et al. (2017)
–
Odimba et al. (2016)
2-42
Sattler et al. (2016)
105.8111.2
–
Brazil
Eucalyptus, Asteraceae/Linguliflora, Mimosa caesalpiniaefolia,Piper, Elephantopus, Cyperaceae and Anacardiaceae
26005200
12001700
Serbia
Brassicaceae, Salix, Fabaceae and other multi-floral samples
24624236
Saudi Arabia
Cucurbita pepo Thunb, Phoenix dactylifera L., Helianthus annuus L., Brassica napus L. and Medicago sativa L.
6232. 798258. 50
Brazil
5918. Senna sp, Chamaecrista sp and 5Mimosa tenuiflora 13366 .6
Colomb Multi-floral ia India, China, Romani Commercial bee pollen a, Spain, Bulgari a,
3.06 7.62
36079542
–
8.113.3
30.450.2
–
de Melo et al. (2016)
44.10114.93
13.5292.23
5.26110.737
4.9554.88
0.1700.465
Kostic et al. (2015b)
31.9244.18
338.12562.06
16.6038.61
4.246.69
63458350. 27
–
Taha (2015)
–
975.4 – 2166. 1
36.4 71.2
16.433.5
35.175.0
0.8 – 1.9
–
–
da Silva et al. (2014)
–
3431542
19.870.6
23.2 126.6
–
8.9206
–
Fuenmay or et al. (2014)
–
4841194
26.153.2
28.8197.7
–
84379
–
Fuenmay or et al. (2014)
–
500900
63.6105.8
–
8562032
–
503964
31.7175.92
2086.3 65752.1 9
234.4 0468.0 5
2353. 114680. 53
1864.13424.9
1.092.41
4682376
87
–
–
Hungar y and Poland
China
Brazil
Brassica napus, Citrullus lanatus, Camellia japonica,Dendranthema indicum, Fagopyrum esculentum, Helianthus annuus,Nelumbo nucifera Gaertn, Papaver rhoeas, Rosa rugosa, Schisandra chinensis, Vicia faba, and Zea mays Commercial pollen
dehydrated
bee
23536358
8283053
21369587
3212777
14319910
8284670
21778165
3483621
28.2565.30
5.176.1
75.2207.8
11.1551.6
8.69357.4
8.3125.11
274.1846.4
12-211
3.225.4
< 0.0041466
–
Yang et al. (2013)
–
Morgano et al. (2012)
–
Cistus ladanifer and commercial multifloral bee pollen
4961. 795357. 82
Romani Helianthus annuus and Salix sp. a
3246. 50-
Spain
520.33792.60
3096. 703197. 29
352.2 2437.7 2
16.3020.21
20.1529.66
18.7038.33 ±
5.057.20
60.7464.77
1409.7 9-
–
2630. 67-
31.6140.06
27.42122.87
–
–
–
88
–
Domíngu ezValhond o, Gil, Hernánd ez, & González -Gómez (2011) Stanciu et al.
Brazil
Asteraceae and other multifloral pollen
5421. 85
2630.6 7
4773. 265383. 73
848.361179.0 5
1008. 28 6873. 407102. 29
679.0 1818.0 2
(2011)
45.0755.22
59.4886.66
42.6073.51
10.4112.05
191.0 2215.3 5
–
Carpes et al. (2009)
Vitamins (mg/100g) Fat-soluble Countr y
Botanical source
Vit. A (βcarote ne)
Water-soluble
Vit. K
Vit. B1
–
0.51.3
Vit. D
Vit. E
–
2.725.37
–
–
–
–
–
0.64– 1.01
1.77– 2.56
7.27– 14.43
Brazil
Eucalyptus, Asteraceae/Linguliflora, Mimosa caesalpiniaefolia,Piper, Elephantopus, Cyperaceae and Anacardiaceae
–
Brazil
Andira, Rubiaceae, Asteraceae, Mimosaceae, Fabaceae, Aquifoliaceae, Anacardiaceae, Myrtaceae, Caesalpineaceae, Brassicaceae, and others
0.0817.92
–
0.469.57
Brazil
Arecaceae, Cecropia, Cestrum, Cyperaceae, Eucalyptus, Ilex,
–
–
–
89
Vit. B2
0.4-0.6
Vit. B3
1.3-3.8
Referenc es
Vit. B5
Vit. B6
–
0.13.8
–
de Melo et al. (2016)
–
6.0379.70
Sattler et al. (2015)
0.33– 0.77
7-56
de Arruda,
–
Vit. C
Myrcia, Piper, Vernonia and Trema
Brazil
Arecaceae, Cecropia, Cestrum, Cyperaceae, Eucalyptus, Ilex, Myrcia, Piper, Vernonia and Trema
Pereira, de Freitas, Barth, & de AlmeidaMuradia n (2013a)
–
–
–
–
90
0.591.09
1.732.41
6.4315.34
0.500.79
–
de Arruda, Perei de Arruda, Pereira, Estevinh o, & de AlmeidaMuradia n (2013b)r a, Estevinh o, & de AlmeidaMuradia n (2013b)
Thailan Z. mays d
Brazil
Brazil
Brazil
1524 1525
Commercial bee pollen
1.530
0.319.92
Mimosa caesalpiniaefolia, Myrtaceae and other multi-floral
0.517.79
Arecaceae, Philodendron sp, Anadenanthera and Eucalyptus
5.6319.89
–
–
6.21
1.63-
–
–
0.20
–
0.50
–
7.03
–
0.39
–
–
Chantaru dee et al. (2012)
11.434.0
de Melo and AlmeidaMuradia n 2010)
–
11.434.0
de Melo, Freitas, Barth, & AlmeidaMuradia n (2009)
–
27.39 -56.03
Oliveira et al. (2009)
ND
–
4.30
–
1.63-
–
–
–
–
–
3.86
–
1.354.25
–
–
–
–
–
K: Potassium; Ca: Calcium; P: Phosphorus; Mg: Magnesium; Zn: Zinc; Fe: Iron; Mn: Manganese; Cu: Copper; Na: Sodium; and Cr: Chromium
1526 1527 1528 1529
91
1530
Table 5
1531 1532
Summary of total pheolic content (TPC), total flavonoid content (TFC) and phytochemical composition of bee pollen from different botanical origins throughout the world. Phenolic compound(s)
Country
Portugal
Botanical source
Cistus ladanifer, Echium sp. and Apiaceae
Total phenolic content (TPC)
35.05 mg GAE/g
References
Total flavonoid content (TFC)
Name
6.81 mg QE/g
Coumaroyl quinic acid, Myricetin-O-rutinoside, LuteolinO-dihexoside, Quercetin-O-dihexoside, Myricetin-Ohexoside, Myricetin-O-(malonyl)rutinoside, Isorhamnetin-O-dihexoside, Quercetin-O-hexosylpentoside, Quercetin-O-rutinoside isomer 1, Myricetin-O(malonyl)hexoside, Quercetin-O-rutinoside isomer 2, Luteolin-di-O-hexosyl-rhamosíde, Quercetin-O(malonyl)rutinoside, Isorhamnetin-O-rutinoside, Hydroxybenzoyl myricetin, Quercetin-O(malonyl)hexoside, Quercetin-O-rhamnoside, Isorhamnetin-O-(malonyl)hexoside isomer 1, Luteolin-O(malonyl)hexoside, Myricetin, Isorhamnetin-O(malonyl)hexoside isomer 2, Myricetin-Odihydroferuloyl protocatechuic acid, Myricetin-O-acetyl hydroxybenzoyl protocatechuic acid-isomer 1, MyricetinO-acetyl hydroxybenzoyl protocatechuic acid isomer 2, Quercetin-O-acetyl hydroxybenzoyl protocatechuic acid isomer 1, Myricetin-O-acetyl hydroxybenzoyl hydrobenzoic acid isomer 2, Quercetin-O-acetyl hydroxybenzoyl hydrobenzoic acid isomer 1, QuercetinO-acetyl hydroxybenzoyl hydrobenzoic acid isomer 2, Odihydroxybenzoyl acetyl malonyl coumaric acid flavonoid derivative 92
Anjos et al. (2019)
Serbia
Helianthus L.
Italy
Hedera helix L., Helianthus annuus L., Asteraceae T form, Cistus L., Cistus incanus/creticus, Brassica type, Gleditsia triacanthos L, Hedysarum coronarium L., Trifolium pratense gr., Castanea sativa Miller, Labiatae L. form, Magnolia, Fraxinus ornus L., Papaver rhoeas L., Crataegus monogyna Jacq., Prunus L., Rubus ulmifolius Schott., Daucus and Coriandrum gr.
Egypt
annuus
Trifolium alexanderinum L
2.91-3.82 mg GAE/g
4.2 - 29.6 mg GAE/g
0.8-2.3 mg GAE/g
0.84-0.87 mg QE/g
Protocatechuic acid, 5-O-Caffeoylquinic acid, Caffeic acid, p-Coumaric acid, Ferulic acid, Quercetin, Quercetin 3-O-galactoside, Quercetin 3-O-rhamnoside, Rutin, Kostić et al. Isorhamnetin, Isorhamnetin 3-O-glucoside, Narcissin, (2019) Kaempferol, Galangin, Luteolin, Apigenin, Acacetin, Genkwanin, Eriodictyol, Naringenin, Taxifolin, Phloretin, Aesculin
–
Cyanidin 3-O-xyloside/arabinoside, Delphinidin 3-O-(60 ’-p-coumaroyl-glucoside), Petunidin 3-O-arabinoside, Pelargonidin 3-O-glucoside, Delphinidin 3-O-glucoside, Delphinidin 3-O-glucosyl-glucoside, Delphinidin 3-Orutinoside, Cyanidin 3-O-sophoroside, Naringin 6'malonate, Naringin 4'-O-glucoside, Naringenin 7-Oglucoside, Apigenin 7-O-(6’-malonyl-apiosyl-glucoside), Tetramethylscutellarein, Luteolin 7-O-glucuronide, Rocchetti et Apigenin 6-C-glucoside, Kaempferol 3-O-glucuronide, al. (2019) Quercetin 3-O-rutinoside, Kamepferol 3,7-O-diglucoside, Quercetin 3-O-galactoside 7-O-rhamnoside, Quercetin 3O-rhamnosyl-galactoside, Kaempferol 3-O-sophoroside, 3,7-Dimethylquercetin, Dihydroquercetin, Formononetin, Genistin, Gallic acid ethyl ester, Syringic acid, Caffeic acid 4-O-glucoside, Caffeoyl glucose, Feruloyl glucose, Caffeic acid, Hydroxytyrosol 4-O-glucoside, Carnosic acid.
0.1-0.85 mg QE/g
93
AbdElsalam , Foda, Abdel-Aziz & El-Hady
(2018)
Brazil
Mimosa caesalpiniifolia, Eucalyptus, Rubiaceae, Astrocaryum aculeatissimum, C. nucifera, M. verrucosa, Myrcia, Alternanthera, Asteraceae, Anadenanthera, and Brassica asmonofloral and other multi-floral samples Alternanthera, Anadenanthera, Cocos nucifera, Mimosa caesalpiniaefolia, Myrcia, and Mimosa scabrella
–
6.5–29.2 mg GAE/g
5.6-29.7 mg GAE/g
6.9-21.0 mg GAE/g
0.3–17.5 mg QE/g
Gallic acid, Protocatechic acid, Chlorogenic acid, syringic acid, p-coumaric acid, Vanillic acid, Caffeic acid, ferulic acid, β-Resorcylic acid, rutin, naringenin, kaempferol, quercetin, catechin, naringin and epicatechin
de Melo et al. (2018a)
0.3-19 mg QE/g
Gallic acid, protocatechic acid, catechin, chlorogenic acid, vanillic acid, caffeic acid, epicatechin, b-resorcylic acid, syringic acid, p-coumaric acid, ferulic acid, synapic acid, naringin, rutin, cinnamic acid, naringenin, quercetin, kaempferol
de Melo et al. (2018b)
–
Duarte, Vasconcelo s, OdaSouza, Oliveira, & López (2018)
0.3-17 mg QE/g
94
Italy, Spain and Colombi a
Greece
Cistus ladanifer, Echium, Rubus ulmifolius, Parthenocissus quinquefolia Ampelopsis brevipedunculata, Brassica napus, Taraxacum officinale, and Trifolium pratense. Commerical bee pollen (Papaver rhoes, Chamomila recutita, Sinapis arvensis, Cistus sp., Trifolium sp., Dorycnium sp., Cichorium sp., Convolvulus sp., Circium sp., Malva sylvestris, Fumana sp., Eucalyptus camaldulensis, Anemone sp., Ononis sp., Asphodelus sp., and Quercus ilex)
–
5.050 mg GAE/ml
–
Tri-caffeoyl- and caffeoyl-di-p-coumaroyl spermidine derivatives
Gardana, Del Bo, Quicazan, Corrrea, & Simonetti (2018)
–
Isopimpinellin, quercetin 3-O-xylosyl-glucuronide, hydroxycaffeic acid, urolithin B, p-coumaroyl tyrosine, quercetin 3-O-rhamnosyl-galactoside, quercetin 3-Oxylosyl-glucuronide, isorhamnetin-3-O-glucoside 7-Orhamnoside, quercetin 3-O-rutinoside
Karabagias, Karabagias, Gatzias, & Riganakos (2018)
95
Brazil
Cocos nucifera
–
–
Greece
Cistus creticus
15.20-60.20 mg GAE/g
6.00- 57.60 mg QE/g
33.46-135.93 mg GAE/g
15.28-31.80 mg QE/g
Malaysia
–
6-O-caffeoyl glucoside, trihydroxycinnamic acid, quercetin-3-O-rhamnosylglucoside, isorhamnetin-di-3,7O-glucoside, Isorhamnetin-3-O-(2”,3”-Odirhamnosyl)glucoside, isorhamnetin-3-O-(2”-ONegri, rhamnosyl) glucoside, N’,N”,N’”-tris-caffeoyl Barreto, spermidine, quercetin-3-O-rhamnoside - (quercetrin), Sper, isorhamnetin-3-O-(2”-O-rhamnosyl acetyl) glucoside, Carvalho, & N’,N”-dicaffeoyl,N’”-coumaroyl spermidine, N’,N”Campos dicaffeoyl,N’”-feruloyl spermidine, N’-caffeoyl-N”(2018) feruloyl,N’”-coumaroyl spermidine, N’-caffeoyl-N”,N’”dicoumaroylspermidine, N’,N”,N’”-tris-p-coumaroyl spermidine, isorhamnetin-3-O-(6”-O-p-coumaroyl)glucoside, and N’,N”,N’”-tris-p-feruloyl spermidine Atsalakis, Chinou, Quercetin-7-rhamnoside, quercetin-3-neohesperidoside, Makropoulo u, kaempferol-3-neohesperidoside, myricetin-3neohesperidoside, kaempferol-3-glucoside and quercetin- Karabourni 3-glucoside oti, & Graikou (2017)
–
96
Fadzilah, , Jaapar, Jajuli, & Wan Omar (2017)
12.57 mg GAE/g
22.89 mg RE/g
Rutin, p-hydroxybenzoic acid , benzoic acid, resveratrol, quercetin, cinnamic acid, vanillin, kaempferol, protocatechuic acid, p-coumaric acid, gallic acid and catechin
Sun, Guo, Zhang, & Zhuang (2017)
–
Vasconcelo s et al. (2017)
China
Rapeseed
Brazil
Mimosa misera, Mimosa caesalpinifolia, Erythrina velutina, Ziziphus joazeiro, Prosopis juliflora, Maytenus rígida, Mimosa tenuiflora, Coutarea hexandra, Piptadenia macrocarpa, Coutarea hexandra, Hyptis suaveolens, and Coutarea hexandra
5.85-46.25 mg GAE/g
1.82-107.00 mg QE/g
–
3.5-23.3 mg GAE/g
–
Quercetin 3-O-sophoroside, quercetin dihexoside and Čeksteryté isorhamnetin 3-glucoside et al. (2016)
–
FatrcováŠramková et al. (2016)
Lithuania
Slovakia
Helianthus L.
annuus
0.69 – 0.80 mg GAE/g
Quercetin, kaempferol, luteolin, apigenin 97
China
Brassica campestris
–
Colombi a
–
24.79 -33.69 mg GAE/g
Brazil
–
40 mg GAE/g
Lithuania
Castanea, Rubus and Cistus –
13.53-24.75 mg GAE/g 24.4 - 38.9 mg
China
Rapeseed
–
Egypt
Zea mays
–
Echium plantagineum
–
Portugal
Watermelon, rape, camellia, corn poppy, corn, motherwort, buckwheat, sesame,
–
Italy
China
604 mg RE/g
Quercetin 3-O-glucoside, kaempferol 3-O-glucoside, naringenin, rutin, quercitrin, kaempferol, and isorhamnetin
Zhang et al. (2016)
Zuluaga et al. (2016) Bárbara et 1 mg CAE/g – al. (2015) 5.91-15.86 mg/g Gallic acid, 4-hydroxybenzoic acid, caffeic acid, and p– Domenici et CE coumaric acid al. (2015) 7.3–10.0 mg RE/g – Kaškonienė Lv et al. – Rutin, quercetin, kaempferol, and isohamnetin (2015) Gallic acid, Vanillic acid, Synringic acid, p-Coumaric acid, Ferulic acid, Caffeic acid 4.21 ± 0.22 11.4 ± 0.04 Quercitin 6.4 ± 0.30 2.24 ± 0.02 Rutin 3.46 ± 0.14 6.4 ± 0.11 Catechin 4.8 ± 0.18 2.1 ± 0.13 Epicatechin 2.1 ± Mohdaly et – 0.08 nd α-Catechin 0.58 ± 0.05 nd Kaempferol 1.65 ± al., (2015) 0.24 0.59 ± 0.19 Apigenin 2.4 ± 0.25 3.57 ± 0.21 3,4Dimethoxycinnamic acid 45.8 ± 0.16 nd Naringenin 3.34 ± 0.12 2.56 ± 0.28 Luteolin Kaempferol-3-O-(4″-rhamnosyl)-neohesperidoside, kaempferol-3-O-sophoroside, kaempferol-3-Oneohesperidoside, kaempferol-3-O-neohesperidoside-7O-rhamnoside, kaempferol-3-O-glucoside, kaempferol-3- Sousa et al. – O-rutinoside + kaempferol-3-O-(3″/4″-acetyl)(2015) neohesperidoside, delphinidin-3-O-glucoside, delphinidin-3-O-rutinoside, petunidin-3-O-glucoside, petunidin-3-O-rutinoside, and malvidin-3-O-rutinoside –
–
–
Quercetin-3-O-b-D-glucosyl-(2/l)-b-glucoside, kaempferol-3, 40-di-O-b-D-glucoside and kaempferol-3O-b-D-glucosyl-(2/l)-b-D-glucoside 98
Zhou et al.(2015)
broad bean and rose India
Brassica juncea
Portugal and Spain
Cistaceae, Fabaceae, Cistaceae, Ericaceae, Boraginaceae
Latvia , Lithuania , China, Spain and Turkey
Brazil
18.29 mg GAE/g
–
18.55-32.15 mgGAE/g
3.92-10.14 mg QE/g
-
24.1 - 45.5 mg RE/g
6.1 - 11.6 mg RE/g
–
44.07-124.10 mg GAE/g
–
20.22-48.76 mg GAE/g
6.58-28.43 mg QE/g
– 41.5 to 213.2 mg GAE/g
Brassicaceae, Asteraceae elephantopus, Asteraceae gochnatia, Myrtaceae eucalyptus, Asteraceae baccharis
and
Rutin, chrysin, kaempferol and quercetin
–
Ketkar et al., 2014 Pascoal, Rodrigues, Teixeira, Feás, & Estevinho (2014)
2-hydroxycinnamic acid, rutin, quercetin, naringenin, and Kaškonienė gallic, caffeic, and ferulic acids et al. (2014) Catechin, epicatechin, quercetin, rutin, and gallic, protocatechuic, p-hydroxybenzoic, chlorogenic, vanillic, caffeic, syringic, p-coumaric, ferulic, benzoic, ocoumaric, abscisic and trans-cinnamic acid
Ulusoy and Kolayli (2014)
Rutin, myricetin
Carpes et al. (2013)
–
o-, p-coumaric acid, ferulic acid, myricetin, cinnamic acid, quercetin, naringenin, hesperitin and kaempferol
Fanali et al. (2013)
–
Isoquercetin, myricetin, tricetin, quercetin, luteolin, selagin, kaempferol, and isorhamnetin
Freire et al. (2012)
and
Greece
–
Brazil
Cecropia, Eucalyptus, Elaeis, Mimosa pudica, Eupatorium, and
99
Portugal
USA
Scoparia Rosaceae, Cistaceae, Boraginaceae, Asteraceae, Fagaceae, Ericaeae, Myrtaceae and Fabaceae
Mesquite, yucca, palm, terpentine bush, mimosa, and chenopod
10.50–16.80 mg GAE/g
15.91- 34.85 mg GAE/g
–
–
Morais, Moreira, Feás, & Estevinho, 2011
2.66-5.48 mg QE/g
Naringenin, 4′,5-dihydroxy-7-methoxyflavanone, 7,8,2′,4′-tetrahydroxy isoflavone, benzene acetic acid, αoxo, methyl ester, anthraquinone derivative, 5-methoxy7-methyl-1,2-naphthoquinone, 7-hydroxy-1-indanone, 1p-tolyl-anthraquinone, 2-methyl-5-hydroxybenzofuran, 5methoxy-7-methyl-1,2-naphthoquinone, 1,2,3,4tetrahydro-2-(2-hydroxy-3-phenoxypropyl)-6,7dimethoxyisoquinoline, 1-)2-methoxy phenyl)-9,10anthracenedione, 2,6-Dihydroxy-6-methylbenzaldehyde, 2-formyloxy-1-phenylethanone, α-oxo, methyl ester, and 1,1-diphenyl-9-methyldeca-3,5-dien-1,9-diol-8-one
LeBlanc, Davis, Boue, de Lucca, & Deeby (2009)
1533 1534
100
1535
Figure Legends
1536
Fig. 1. The collection process of bee pollen by honeybees.
1537 1538 1539 1540
[1] Honeybee, [2] Flower with pollen, [3] Honeybee covered with microscopic pollen, [4] Honeybee carrying pollen pellet in her hind legs, [5] Honeybee ready to carry pollen pellet, [6] Hind-legs with pollen pellet, [7] Pollen trap at hive entrance, [8] Trap-tray for bee pollen collection and [9] Collected bee pollen
1541 1542
Fig. 2. Bee pollen of (a) several colors and (b) morphology and surface texture (examined using Scanning Electron Microscope, SEM) from diverse botanical origin.
1543 1544 1545 1546 1547 1548 1549 1550 1551 1552 1553 1554 1555 1556 1557 1558 1559
[1] Asphodelus tenuifolius: Dull orange color, [2] Brassica napus: Bright yellow color, [3] Castanea: Light yellow color, [4] Cistus: Dull yellow color, [5] Cocos nucifera: Creamish yellow color, [6] Coriandrum sativum: Pale brown color , [7] Pennisetum glaucum: Bright brown color, [8] Rubus: Yellow green color, [9] and [10] Multi-floral: Samples having different colors of pollen grain, [11] Zea mays: Monad, spherical and presence of germination pore, [12] Quercus sp: Monad, prolate and tricolpate (30x27µm), [13] Actinidia arguta: Monad, prolate, tricolporate, and oval (24.5x17.5 µm), [14] Elaeis guineensis: Monad, circular and tectate exine , [15] Camellia sinensis: Monad, triangular and radially symmetric, [16] Mimosa diplotricha: Rhomboidal tetrad, oval and reticulated exine , [17] Arecaceae sp: Monad, isopolar, prolate, tricolpate, presence of furrow and smooth surface, [18] Cocos nucifera: Monad, monocolpate, elliptical shape with smooth surface and furrow, [19] Coriandrum sativum: Long, stick-shaped, monad and had smooth surface along with furrows containing pores, [20] Brassica napus: Monad, prolate, and tricolpate along with distinct net-like pattern over exine, [21] Maytenus sp: Monad, tetrahedral, oblate and reticulated surface, [22] Aloe greatheadii: Monad, bilaterally symmetrical and elliptical shape with a deep furrow (44-50 µm), [23] Asteraceae eupatorium: Monad, spherical and spinules surface, and [24] and [25] Multi-floral: Samples containing individual pollen grain with different shapes and surface properties
1560 1561 1562
Adapted from: Chantarudee et al. (2012); Forcone, Calderón and Kutschker (2013); Human et al. (2013); Rebiai and Lanez (2013); Gabriele et al. (2015); de Florio Almeida et al. (2017); Ghosh and Jung (2017) and Peukpiboon, Benbow and Suwannapong (2017)
101
Fig. 1
(a)
(b) Fig. 2
Highlights •
Physicochemical and functional properties of bee pollen from varying sources are summarized.
•
Bee pollen has average 54.22% carbohydrates, 21.30% proteins, 5.31% lipids and 2.91% ash content.
•
Functional properties are reviewed as key elements for valorization of bee pollen.
•
Investigating the mono-floral bee pollen from diverse botanical and geographical origin is proposed.
•
The need of harmonized global standards for bee pollen safety is also addressed.