Composition and functionality of bee pollen: A review

Background: The food industry today is returning to natural foods after emphasizing the processed products due
to the higher consumer demand for foods which are well recognized by healthy nutrients. Bee pollen is known as
a natural super food due to its indispensable nutritional and medicinal properties. However, the physico-chemical
and nutritional properties of bee pollen are ambiguous which vary greatly due to the difference of botanical
and geographical origin

1. Contents lists available atScienceDirect
Trends in Food Science & Technology
journal homepage:www.elsevier.com/locate/tifs
Composition and functionality of bee pollen: A review
Mamta Thakur
∗
, Vikas Nanda
Department of Food Engineering and Technology, Sant Longowal Institute of Engineering and Technology (Deemed-to-be-University), Longowal, 148106, Punjab, India
ARTICLE INFO
Keywords:
Bee pollen
Essential amino and ω-3 fatty acids
B-complex vitamins
Polyphenols
Functional properties
Food applications
ABSTRACT
Background:The food industry today is returning to natural foods after emphasizing the processed products due
to the higher consumer demand for foods which are well recognized by healthy nutrients. Bee pollen is known as
a natural super food due to its indispensable nutritional and medicinal properties. However, the physico-che-
mical and nutritional properties of bee pollen are ambiguous which vary greatly due to the difference of bo-
tanical and geographical origin.
Scope and approach:The current study, therefore, presents an updated overview by critically reviewing the
literature for chemical constituents (sugars, amino acids, fatty acids, minerals, vitamins, and phenolic com-
pounds) of bee pollen since 2009 from more than 20 nations of the world. The functional properties of different
plant-derived bee pollen and their food applications are also discussed for the first time.
Key findings and conclusions:As per the systematic review of above 100 studies, the bee pollen contains average
54.22% (18.50–84.25%) carbohydrates, 21.30% (4.50–40.70%) proteins, 5.31% (0.41–13.50%) lipids, 8.75%
(0.15–31.26%) fibre, 2.91% (0.50–7.75%) ash, 13.41 g/100 g (2.77–28.49 g/100 g) glucose, 15.36 g/100 g
(4.9–33.48 g/100 g) fructose, 4.25 g/100 g (0.05–9.02 g/100 g) sucrose, 4951.61 mg/kg (3.06–13366.60 mg/
kg) potassium, 4157.86 mg/kg (234.40–9587.00 mg/kg) phosphorus, 1751.22 mg/kg (1.09–5752.19 mg/kg)
calcium, 1246.99 mg/kg (44.00–4680.53 mg/kg) magnesium, 46.97 mg/kg (0.10–105.80 mg/kg) zinc,
197.41 mg/kg (2.60–1180.00 mg/kg) iron, and 30.59 mg GAE/g (0.69–213.20 mg GAE/g) total phenolic
content. Bee pollen, based on its functional properties can be recommended as a natural food ingredient in
several processed food products. Further, the present paper strongly focuses to investigate the mono-floral bee
pollen from different geographical regions and related safety issues to establish the global pollen quality and
safety standards in coming years.
1. Introduction
Recently, the bee pollen has demonstrated great attention in food
processing as it is a paragon of wholesome nutrients (Sattler et al.,
2015; Thakur & Nanda, 2018a). It contains mainly lipids, proteins, and
micronutrients essential for honeybees whereas it exhibits the nu-
traceutical potential for humans, thereby preventing several diseases
(de Melo & Almeida-Muradian, 2010; Komosinska-Vassev, Olczyk,
Kafmierczak, Mencner, & Olczyk, 2015). For the heightened application
of bee pollen, its comprehensive characterization based on physico-
chemical, nutritional, and functional characteristics as per floral and
geographical source is need of the hour.
Basically, the pollen is the microscopic structure like grains, found
in the anther of stamen in the angiosperms (Steven, 2014). Worker
honeybees during visits attract the hundreds to thousands of pollen
grains using weak electrostatic field generated between flower (nega-
tively charged) and bee body (positively charged) (Clarke, Morley, &
Robert, 2017). The pollen grains are agglutinated using the several
combs and hairs of bee's hind legs which are moistened with salivary
secretions and nectar to form a pellet of size 1.4–4 mm i.e. character-
istically distinct from wind pollen (Saavedra, Rojas, & Delgado, 2013).
Thus bees carry the pollen as pellets using the pollen basket and stored
inside the alveoli for further consumption to fulfill the requirements for
protein and to synthesize the jelly in their food glands (Di Pasquale
et al., 2013). The bee colony can collect 50–250 g of pollen per day or
15–40 kg per year (Komosinska-Vassev et al., 2015).
Bee pollen, also known as apicultural or bee-collected or corbicular
pollen can be harvested with the help of trap, fixed at the entrance of
beehives. While returning home, the pollen is lost from the hind legs
and collected in the collection tray of the trap (Fig. 1). The nutrient-
dense pollen thus collected is high in moisture content and its proper-
ties initiate to degrade after the collection. Therefore, the bee pollen
must be consumed either fresh or quickly dried carefully to retain the
nutrients (Denisow & Denisow-Pietrzyk, 2016; Kieliszek et al., 2018).
https://doi.org/10.1016/j.tifs.2020.02.001
Received 16 November 2019; Received in revised form 5 January 2020; Accepted 3 February 2020
∗
Corresponding author.
E-mail address:[email protected](M. Thakur).
Trends in Food Science & Technology 98 (2020) 82–106
Available online 12 February 2020
0924-2244/ © 2020 Elsevier Ltd. All rights reserved.
T

2. The plant sources of bee pollen, as determined by palynological analysis
strongly affect its nutritional, physico-chemical, and functional prop-
erties (da Silva et al., 2014; Nogueira, Iglesias, Feás, & Estevinho, 2012;
Yang et al., 2013; Thakur & Nanda, 2018a). The pollen pellets from
unique botanical taxon or the ones having single predominant pollen
at > 90% frequency or containing no accessory pollen at > 60% fre-
quency are considered as mono-floral (Barth et al., 2010). However, in
case of inadequate flora surrounding the hive, the honeybee will visit
the flower of other botanical sources and thus the microscopic pollen
grains are mixed, resulting in the pellet known as multi-floral pollen
when there is no predominance and may present accessory pollen
varying from 15 to 45% (Barth et al., 2010). The flower from plant
species affects the color of pollen grain ranging from white or creamish
white and yellow to orange, red, green, gray and dark brown. The
physico-chemical, functional and sensory properties are usually fixed
for mono-floral pollen of a particular botanical origin whereas the
multi-floral pollen loads vary in the properties (Barth et al., 2010). Even
after a similar plant source, pollen composition may vary due to sea-
sonal and regional variations (de Melo, Freitas, Barth, & Almeida-
Muradian, 2009).
Bee pollen contains carbohydrates (13–55%), proteins (10–40%),
lipids (1–13%), crude fibre (0.3–20%) and ash content (2–6%) (Campos
et al., 2008). In addition, it is composed of all essential amino and fatty
acids, free amino acids, vitamins mainly B-complex, essential minerals,
carotenoids and flavonoids (Mărgăoan et al., 2014; de Melo et al., 2016;
Ghosh & Jung, 2017; Thakur & Nanda, 2018a). Fructose followed by
glucose and sucrose is the major sugar and nearly 1% of remaining
sugars in pollen include arabinose, isomaltose, melibiose, melezitose,
ribose, trehalose, and turanose (Chantarudee et al., 2012; Liolios et al.,
2018). It is acclaimed for its excellent nutrition and therapeutic prop-
erties, and currently, commercially consumed as a dietary supplement.
Bee pollen has been acknowledged by law as a food additive in Ar-
gentina, Brazil, and Switzerland where its standard norms of physico-
chemical and microbiological quality have been officially instituted.
Likewise, several other countries have established the physico-chemical
parameters of pollen for its healthy intake (Canale et al., 2016;
Fuenmayor et al., 2014). Therefore, a vast research interest has been
observed about bee pollen and numerous studies have been conducted
for characterizing the pollen of varying floral origins from different
regions of numerous countries like Brazil, China, Greece, India, Por-
tugal, Romania, Spain, South Africa, Saudi Arabia, etc. to identify the
peculiarities (Yang et al., 2013; Liolios et al., 2016; Sagona et al., 2017;
de Melo et al., 2018a; de Melo et al., 2018b; Gardana, Del Bo, Quicazan,
Corrrea, & Simonetti, 2018; Liolios et al., 2018; Thakur & Nanda,
2018a; Isik, Ozdemir, & Doymaz, 2019; Liolios et al., 2019a,b). How-
ever, as per the literature survey, a detailed review of bee pollen still
lacks its physico-chemical and functional properties. Globally, a generic
quality criterion for pollen was suggested byCampos et al. (2008)
whereasPuerto, Prieto, and Castro (2015)focused on the phytochem-
icals reported in pollen contributing to antioxidant potential. As per the
literature, the biological and medicinal activities of pollen were dis-
cussed byDenisow and Denisow-Pietrzyk (2016); the extraction tech-
niques of pollen derived bioactive compounds were analyzed byAres,
Valverde, Bernal, Nozal, and Bernal (2018)andLi et al. (2018)studied
the nutritional and biological properties of pollen from a limited bo-
tanical and geographical sources. Further, the metabolism of bee pollen
derived natural metabolites and food safety of pollen were discussed in
many studies which seems to be unsatisfactory without the detailed
knowledge of bee pollen composition and functionality. This paper,
therefore, aims to present a comprehensive and updated summary of
researches from the previous 10 years on physico-chemical composition
and functionality of bee pollen from diverse botanical and geographic
roots of more than 20 countries which will fortify the existing knowl-
edge about the bee pollen composition.
2. Nutritional value
Today the health-conscious consumers prefer to consume the value-
added products which allow replacing the conventional food in-
gredients with high-nutritional value component to supplement the
existing processed products. The human diet should provide the energy
and other essential nutrients required for physical and mental devel-
opment and health in amounts that meet standards (Kieliszek et al.,
2018). Due to the excellent nutrient profile, bee pollen can supplement
the human diet and provides a significant daily intake of nutrients.
Average bee pollen composition, as reviewed byCampos et al. (2008)is
compared with nutritional requirements for an average adult inTable 1.
The share of major nutritional components particularly carbohydrates
and fats are comparatively small; however, the crude fiber and protein
can contribute significantly up to 60% and 70% of required daily intake
(RDI), respectively based on the floral source and location. Further, the
daily intake of 50 g bee pollen provides all essential vitamins (except
Fig. 1.The collection process of bee pollen by hon-
eybees. [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.
M. Thakur and V. Nanda Trends in Food Science & Technology 98 (2020) 82–106
83

3. pyridoxine and pantothenic acid) and minerals (except calcium) suffi-
cient to meet above 50% requirement of RDI. Bee pollen intake can be
increased by adding them in routine foods, for instance, mixing in milk,
smoothies, yogurt, bread, cookies, fruit juices, etc. as seen in case of
flaxseed addition in bakery products (Kaur, 2011; Kaur et al., 2018;
Čukelj et al., 2017). According to Nagai et al. (2007), the free amino
acids, required by the body are adequately provided even by 15 g
Spanish pollen. Some studies even reported that bee pollen intake is
enough for human survival (Nogueira et al., 2012). The vitamins from
bee pollen contribute to the nutrition greatly and almost all the es-
sential minerals are reported in bee pollen in good amounts. However,
RDI can vary according to the difference in bee pollen composition. The
pollen derived nutrients are digested and assimilated in a better way
which improves the immune system against pathogens, and physical
and chemical agents. Chinese rape bee pollen is employed as the im-
munity enhancer of the organism against cancer diseases (Omar, Azhar,
Fadzilah, & Kamal, 2016). Bee pollen, when administered daily in 40 g
to heart patients, caused a decrease in their cholesterol level, blood
viscosity and fibrinogen and fibrin (Campos, Frigerioc, Lopes, &
Bogdanov, 2010). Bee pollen also decreases the lipid content in blood
serum which is considered to link with the level of hormones like in-
sulin, testosterone, and thyroxine (Komosinska-Vassev et al., 2015).
However, the bee pollen failed to substantiate health claims under EFSA
Regulation (EC) No. 1924/2006 EU (Mateescu. 2011; Onisei, Mateescu,
& Răscol, 2018).
3. Physico–chemical properties
3.1. Physical properties
3.1.1. Weight, shape, and size
The average weight of bee pollen pellet is approximately 7.5–8 mg
that varies according to the pollen accessibility during the visit. The
pollen from a single floral source may be significantly dissimilar in
shape and size thereby affecting the pollen-packing efficiency
(Komosinska-Vassev et al., 2015). The anemophilous plants provide
lighter and dried pollen resulting in larger and loosely arranged pellets
whereas the entomophilous plants are responsible for smaller and more
compacted form pollen (Friedman & Barrett, 2009).
The fresh pollen may be cylindrical, round, triangular, or bell-shaped
whereas the dried pollen pellets having diameter 0.01–0.05 mm are
usually spherical or spindle-shaped (Barene, Daberte, & Siksna, 2015).
Thakur and Nanda (2018b)evaluated the pollen pellets fromCocos nu-
cifera, Coriandrum sativum, Brassica napusand multi-floral source of India
and reported the variation in length, width, equivalent diameter, thou-
sand pollen pellet weight, sphericity, surface area, bulk and true density,
volume, porosity and angle of repose due to their moisture content. On
the other hand,Bleha, Shevtsova, Kružík, Brindza, and Sinica (2019)
reported the pollen loads (Brassica napus, Helianthus annuus, Papaver
somniferum, Phacelia tanacetifolia, Robinia pseudoacacia, Trifolium repens)
of mean 11.85 g weight, 3.10 mm height, and 3.55 mm width, from the
Slovak Republic. Further, the surface texture of pollen grains provides a
hint of their botanical composition due to distinct exine structure and
properties (Fig. 2) which are representative of particular plant species
(Wang & Dobritsa, 2018). For instance, the maize has thicker exine
covered fully with tectum, exine inBrassicais thinner having a re-
ticulated surface andHibiscuscontains exines densely covered with long-
pointed spines (Basarkar, 2017; Wang & Dobritsa, 2018).
3.1.2. Color
The pollen quality can be roughly judged based on its color which is
linked to plant pigments like carotenoids and anthocyanins, inherently
found in different concentrations in pollen (Sattler et al., 2015). The
natural brightness of anther pollen decreases due to the addition of
moisture particularly nectar to form a pollen pellet. The bee pollen
contains all shades of color from white to black (Fig. 2), however, the
pollen collected from the same plant source may have different color
and sometimes, the bee pollen from various botanical origins can be of
similar color.Modro, Silva, Luz, and Message (2009)reported that such
differences arise from the state of flower thecae which may be either
already open or split by honeybees.
Color is affected by chemical composition also, as revealed by in-
strumental color analysis exhibiting the correlation between color va-
lues and Ca, Mg and Fe contents (Yang et al., 2013). Likewise, color
values of Brazilian pollen were recommended as indices byde Melo
et al. (2016)to determine the total phenolic content and antioxidant
and antimicrobial potential by observing the correlation among these
parameters. Further, the processing conditions also influence the color
values, particularly L* and b* and grinding of pollen pellets after de-
hydration results in the supremacy of yellow color and higher positive
values of b*. This may be due to oxidation reactions of some com-
pounds like polyphenols during drying (Silva, Rosa, & Vilas Boas,
2009).
3.2. Chemical properties
3.2.1. Moisture content and water activity
The concentration of water is a major factor that affects the amount
of remaining constituents in any product while the quality and storage
life is closely associated with the water activity (a
w) (Nogueira et al.,
2012). The higher a
wstimulate the growth of microorganisms, parti-
cularly yeasts and molds, producing the mycotoxins and ochratoxins
and enzyme activities in bee pollen which may be a fundamental cause
of pollen toxicity, creating a risk to consumer (Feás, Vazquez-Tato,
Estevinho, Seijas, & Iglesias, 2012). However, the legislations have not
yet fixed the standards for its value. Usually, the various perspectives of
food quality and safety including moisture sorption, enzymatic activ-
ities, etc. are affected by higher a
w, thereby increasing the significance
of hygienic conditions during handling, drying, and processing of bee
Table 1
Average bee pollen composition and nutritional requirements as Required Daily
Intake (RDI).
Nutrients Amount (%) Average RDI % RDI for 50 g of bee
pollen
Carbohydrates (Fructose,
glucose, sucrose, fibre)
13–55 320
b
3.33–15.34
Crude fibre 0.3–20 30
b
1.00–60.03
Protein 10–40 50
b
18.01–73.37
Fat 1–13 80
b
0.33–13.34
Potassium 400–2000
a
2000
c
16.68–90.04
Phosphorus 80–600
a
1000
c
6.67–53.36
Calcium 20–300
a
1100
c
1.67–23.34
Magnesium 20–300
a
350
c
6.67–76.71
Zinc 3–25
a
8.5
c
33.35–263.46
Manganese 2–11
a
3.5
c
50.02–283.47
Iron 1.1–17
a
12.5
c
6.67–123.39
Copper 0.2–1.6
a
1.2
c
13.34–120.06
β-Carotene 1–20
a
0.9
c
100.05–2001
Tocopherol 4–32
a
13
c
26.68–220.11
Niacin 4–11
a
15
c
23.34–66.70
Pyridoxine 0.2–0.7
a
1.4
c
13.34–43.35
Thiamine 0.6–1.3
a
1.1
c
50.03–106.72
Riboflavin 0.6–2
a
1.3
c
40.02–140.07
Pantothenic acid 0.5–2
a
6
c
6.67–30.02
Folic acid 0.3–1
a
0.4
c
66.7–223.45
Biotin 0.05–0.07
a
0.045
c
100.05–140.07
Ascorbic acid 7–56
a
100
c
6.67–50.025
Bee pollen composition is according toCampos et al. (2008)and RDI are ac-
cording to the Reports of the Scientific Committee for Food (2010) andDenisow
and Denisow-Pietrzyk (2016).
a
Amount is given in mg/100 g.
b
RDI is given in g/day.
c
RDI is given in mg/day.
M. Thakur and V. Nanda Trends in Food Science & Technology 98 (2020) 82–106
84

4. pollen to minimize the likelihood of man-derived contaminations.
Table 2showed the data about moisture content and a
wof pollen of
varying plant sources and countries.
Fresh bee pollen may contain at least 7% and maximum up to 30%
moisture content and is hence always at the risk of fungal contamina-
tion due to its highly hygroscopic nature thus questioning the safety of
Fig. 2.Bee pollen of (a) several colors and (b) morphology and surface texture (examined using Scanning Electron Microscope, SEM) from diverse botanical origin.
[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] Quercussp: Monad, prolate and
tricolpate (30 × 27μm), [13]Actinidia arguta:Monad, prolate, tricolporate, and oval (24.5 × 17.5 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]Arecaceaesp: 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]Maytenussp: 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.Adapted from:Chantarudee et al. (2012); Forcone, Calderon, 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)andPeukpiboon, Benbow, and
Suwannapong (2017). (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.)
M. Thakur and V. Nanda Trends in Food Science & Technology 98 (2020) 82–106
85

5. Table 2
Summary of studies on physico-chemical properties of bee pollen from different botanical origins throughout the world and International standards for bee pollen quality.
CountryBotanical sourceChemical compositionReferences
MC (%)CHO (%) PT (%) LP (%) CF (%) TM (%) pHa
w
Worldwide Literature Reports
ItalyHedera helixL,Cistus incanus ,Cornus sanguinea
L., CruciferaeBrassica ,Castanea sativaMiller,
Lamiaceae L form,Fraxinus ornusL,Helianthus
annuus ,Papaver rhoeasL.,Crataegus monogyna
Jacq.,Prunus ,Rubus ulmifoliusSchott,Gleditsia
triacanthosL.,Hedysarum coronarium ,Trifolium
alexandrinum , andCoriandrum sativum
(n = 32, dried pollen)
––13.60–40.70 –––––Castiglioni et al. (2019)
Turkey(n = 1, fresh and dried pollen)8.80–2861.96–78.70 12.43–30.36 5.50–7.22 –2.14–2.18 ––Isik et al. (2019)
GreeceErica manipuliflora, Morussp.,Robinia
pseudoacacia ,Eucalyptussp.,Viciasp.,Phacelia
tanacetifolia, Trifoliumsp.,Zea mays, Platanus
sp.,Pinussp.,Eryngium campestre, Erica
arborea, Ranunculussp.,Laurus nobilis,
Chenopodiumsp.,Helianthus annuus ,Acersp.,
Actinidia chinensis, Veronica persica, Convolvulus
arvensis ,Lamiumsp.,Salixsp.,Polygonum
aviculare, Centaurea calcitrapa, Cistus sp.,Olea
europaea, Papaver rhoeas, Portulaca oleracea,
Hedera helix, Verbascumsp.,Centaureasp.,
Asphodeloussp.,Aesculus hippocastanum,
Amorpha fruticosa, Inula viscosa, centaurea
solstitialis, Pyrus communis, Pastinaca sativa,
Chondrilla juncea ,Cirsiumsp.,Cichorium
intybus, Brassica napus, Brassica nigra,
Taraxacum officinale ,Sisymbrium irio , and
Echinops ritro(n = 46, fresh pollen)
–––1.15–13.60 ––––Liolios et al. (2019b)
SloveniaBrassicaceae ,Castanea sativa ,Hedera helix ,
Fagopyrum esculentum , and multi-floral
(n = 28, fresh pollen)
14.80–32.10 –––10.10–21.37 –––Bertoncelj et al. (2018)
BrazilMimosa caesalpiniifolia, Eucalyptus, Rubiaceae,
Astrocaryum aculeatissimum ,C. nucifera, M.
verrucosa, Myrcia, Alternanthera, Asteraceae,
Anadenanthera,andBrassicaas monofloral and
other multi-floral samples (n = 56, dried
pollen)
–54.90–82.80 7.90–32.20 3.20–13.50 –1.90–3.60 ––de Melo et al. (2018a)
Alternanthera, Anadenanthera; Cocos nucifera;
Mimosa caesalpiniaefolia; Myrcia; Mimosa
scabrella, Mimosa scabrellaandMimosa
scabrella(n = 8, dried pollen)
––10.60–33.90 3.20–8.30 –2.60–3.80 ––de Melo et al. (2018b)
(n = 25, fresh pollen)–18.50–45.00 4.50–9.90 2–6 ––4.90–5.90 –Duarte, Vasconcelos, Oda-Souza,
Oliveira, and López (2018)
Columbia, Italy and
Spain
Multi-floral (n = 3, commerical pollen) 14.90–15.50 37.70–44.10 14–24 2.50–6 –1.80–2.10 ––Gardana et al. (2018)
(continued on next page )
M. Thakur and V. Nanda Trends in Food Science & Technology 98 (2020) 82–106
86

6. Table 2(continued )
CountryBotanical sourceChemical compositionReferences
MC (%)CHO (%) PT (%) LP (%) CF (%) TM (%) pHa
w
GreeceCommerical bee pollen ( Papaver rhoes,
Chamomila recutita, Sinapis arvensis, Cistus sp.,
Trifoliumsp.,Dorycniumsp.,Cichoriumsp.,
Convolvulussp.,Circiumsp.,Malva sylvestris,
Fumanasp.,Eucalyptus camaldulensis, Anemone
sp., Ononissp.,Asphodelussp.,Quercus ilex )
(n = 1, commercial pollen from Attiki Bee
Culturing Co.-Alex Pittas S.A., Athens, Greece)
–6117.60 78.40 2.28 4.70–Karabagias et al. (2018)
BrazilCocos nucifera(n = 1, dried pollen)24.40
a
–13.15 2.70 –2.54 4.00–Negri, Barreto, Sper, Carvalho, and
Campos (2018)
RomaniaBrassicasp,Carduussp.,Helianthus annuus ,
PrunusL. sp.,Crataegus monogynaand bifloral
and multi-floral (n = 10, fresh pollen)
16.92–31.08 23.31–48.63 13.16–24.14 1.33–5.47 –1.34–2.81 ––Spulber, Dogaroglu, Babeanu, and
Popa O. V. I. D. I. U (2018)
IndiaCocos nucifera, Coriandrum sativum, Brassica
napus andmulti-floral (n = 35, fresh pollen)
12.72–19.59 46.16–42.33 19.63–25.39 7.14–12.38 3.05–4.31 2.27–3.45 4.74–5.48 0.39–0.47Thakur and Nanda (2018a)
BrazilCommercial bee pollen (n = 62, dried pollen) 3.06–8.12 –15.49–34.73 3.25–10.96 –1.91–4.61 ––de Arruda et al. (2017)
Republic of KoreaActinidia argutaandQuercus(n = 2, dried
pollen)
4.4–13.8–23.2–26.5 7.0–4.5 3.1–4.2 5.2–5.3 ––Ghosh and Jung (2017)
ItalyRubus, Cistus, Castanea , andHedera(n = 5,
fresh pollen)
8.5–29.544.8–61.3 21.3–28.7 0.91–2.2 –1.9–3.0 ––Sagona et al. (2017)
Brazil(n = 2, dried pollen)37.12–53.39
a
25.66–44.27 24.00–37.63 6.47–10.81 9.30–13.65 2.74–4.03 3.34–3.70
a
0.85–0.91
a
Rebelo, Ferreira, and Carvalho-Zilse
(2016)
Eucalyptus, Asteraceae, Mimosa
caesalpiniaefolia, Piper, Elephantopus,
Cyperaceae and Anacardiaceae(n = 4, dried
pollen)
––8.3–11.4 6.6–8.2 ––––de Melo et al. (2016)
(n = 21, fresh pollen)36.0 ± 2
c
–21 ± 2
c
–3.6 ± 1.4
c
4.9 ± 0.3
c
3.49 ± 0.04
c
0.86 ± 0.02
c
Bárbara et al. (2015)
ItalyCastanea, RubusandCistus(n = 3, fresh
pollen)
10.75–12.03 54.84–57.98 25.87–28.42 1.92–2.83 –2.55–2.85 ––Gabriele et al. (2015)
SerbiaBrassicaceae, Salix, Fabaceaeand multi-floral
samples (n = 3, fresh pollen)
4.35–14.35 64.42–81.84 14.81–27.25 1.31–6.78 –1.18–3.32 ––Kostić, Barać et al., 2015
BrazilAndira , Rubiaceae, Asteraceae, Mimosaceae,
Fabaceae, Aquifoliaceae, Anacardiaceae,
Myrtaceae, Caesalpineaceae, Brassicaceae, and
others (n = 21, dried pollen)
16.1–18 (fresh)
and 2.8–3.6
(dried)
–15.3–22.9 1.9–3.9 –1.7–2.3 ––Sattler et al. (2015)
Saudi ArabiaCucurbita pepo Thunb ,Phoenix dactylifera ,
Helianthus annuus ,Brassica napusandMedicago
sativa(n = 5, dried pollen)
9.16–10.5 –14.71–19.45 1.82–5.38 0.15–1.70 1.88–3.88 ––Taha (2015)
ColombiaMulti-floral (n = 196, dried pollen)1.8–11.8–16.1–32.1 2.8–9.7 7.8–18.1 1.5–3.2 3.8–5.4 –Fuenmayor et al. (2014)
India, China, Romania,
Spain, Bulgaria,
Hungary and
Poland
Commercial bee pollen (n = 9, commercial
pollen)
2.0–9.1–15.8–26.1 4.9–8.0 8–14.5 1.5–4.3 4.3–5.4 –
BrazilBee pollen samples collected during summer,
spring, autumn and winter (n = 48, dried
pollen)
4
b
–18.66–24.39 2.26–4.95 1.81–4.05 –––Negrão, Barreto, and Orsi (2014)
Arecaceae, Cecropia, Cestrum, Cyperaceae,
Eucalyptus, Ilex, Myrcia, Piper, Vernonia , and
Trema(n = 7, dried pollen)
3.16–3.99 –22.15–25.11 4.57–6.13 –2.77–3.24 ––de Arruda, Pereira, de Freitas,
Barth, & de Almeida-Muradian
(2013)
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87

7. Table 2(continued )
CountryBotanical sourceChemical compositionReferences
MC (%)CHO (%) PT (%) LP (%) CF (%) TM (%) pHa
w
ChinaBrassica napus, Citrullus lanatus ,Camellia
japonica, Dendranthema indicum ,Fagopyrum
esculentum, Helianthus annuus,Nelumbo nucifera
Gaertn ,Papaver rhoeas, Rosa rugosa ,Schisandra
chinensis ,Vicia faba , andZea mays(n = 12,
commercial pollen from Zhenzhou Kerun
Apiculture Co., Ltd., Zhenzhou, Henan
Province, People's Republic of China)
1.82–7.52 59.43–77.82 14.26–28.95 0.66–6.56 17.60–31.26 1.67–5.01 ––Yang et al. (2013)
EgyptZea mays, Trifolium alexandrinum,andPhoenix
dactylifera(n = 3, fresh pollen)
11.91–28.15 –12.35–38.06 0.41–1.09 –1.72–7.75 ––Khider, Elbanna, Mahmoud, and
Owayss (2013)
ThailandZ. mays(n = 1, dried pollen)7.0364.42 19.12 7.00 0.86 2.43 ––Chantarudee et al. (2012)
PortugalMulti-floral (n = 10, dried pollen)4.33–6.67 –24.23–34.18 2.60–3.32 –2.31–3.99 4.33–6.33 0.32–0.55Estevinho, Rodrigues, Pereira, and
Feás (2012)
Cistusand other multi-floral including
Boraginaceae, Rosaceae, Fagaceae, Asteraceae,
Fabaceae, Ericaceae, Mimosaceae and Myrtaceae
(n = 22, dried pollen)
–61.2–70.6 19.1–27.1 4.3–6.3 –2–4 4.3–5.2 0.21–0.54Feás et al. (2012)
Romania(n = 16, fresh pollen)17.59–29.55 –16.27–26.50 2.13–8.93 –1.75–3.25 ––Mărgăoan, Al. Mărghitaş,
Dezmirean, Bobiş, and Mihai
(2012)
Portugal and SpainCistaceae, Fabaceae, Ericaceae, Fagaceae, and
Boraginaceae(n = 8, commercial pollen)
6.02–8.40 69.68–84.25 12.50–25.15 2.35–3.06 –0.50–3.16 4.23–5.17 0.26–0.43Nogueira et al. (2012)
FranceZea 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, Fraxinus, Liliaceae,
FicariaandQuercus(n = 52, fresh pollen)
––16.70–29.90 7.50–24.40 ––––Odoux et al. (2012)
SpainCistus ladanifer,multi-floral and commercial
bee pollen (n = 5, fresh and dried pollen)
––17.64–16.08 2.86–3.71 14.50–14.65 ––0.10–0.66Domínguez-Valhondo, Gil,
Hernández, and González-Gómez
(2011)
BrazilCommercial bee pollen samples (n = 154,
dried pollen)
3.00–9.39 –12.28–27.07 4.01–13.32 –1.33–4.13 ––Martins et al. (2011)
ColombiaDry and wet Multi-floral samples (n = 2, dried
pollen)
5.57–19.90 –16.3–23.8 5.36–6.69 6.90–8.60 –4.636–4.830 0.27–0.72Bobadilla (2009)
BrazilAsteraceaeand other multi-floral pollen
(n = 36, dried pollen)
3.45–4.85 –18.55–22.60 4.59–5.07 –––0.37–0.38Carpes, Mourão, Alencar, and de
Masson, (2009)
BrazilMimosa caesalpiniaefolia ,Myrtaceaeand other
multi-floral (n = 6, dried pollen)
1.50–2.99 –19.98–28.28 4.53–5.69 –2.89–3.30 ––de Melo et al. (2009)
International Standards
Argentina–< 8 (dried) –15–28 ––< 4 4–6–Alimentos azucarados (2010)
Brazil–< 4 (dried)
< 30 (fresh)
–> 8 > 1.8 –< 4 ––Instrução normativa N.° 3 (2001)
France–< 6 (dried) –10–41 1–10 –2–6–de Arruda, Pereira, de Freitas, et al.
(2013)
Mexico–4.5–8–12–18 2.5–6.5 –1.5–2.2 > 4–Fuenmayor et al. (2014)
Switzerland–< 6 (dried) –10–40 1–10 –2–6 ––Lebensmittelverordnung 817.02
(2005)
MC: Moisture content, CHO: Carbohydrates, PT: Proteins, LP: Lipids, CF: Crude Fibre, TM: Total minerals, a
w
: water activity.
a
Fresh bee pollen.
b
Fixed moisture content.
c
Average value ± standard deviation.
M. Thakur and V. Nanda Trends in Food Science & Technology 98 (2020) 82–106
88

8. Table 3
Summary of sugars and amino acid composition (g/100 g) of bee pollen from different botanical origins throughout the world.
CountryBotanical sourceSugars (g/100 g)References
GlucoseFructoseSucroseMaltose
SloveniaBrassicaceae ,Castanea sativa ,Hedera helix ,Fagopyrum
esculentum , and multi-floral
11.94–28.4913.17–26.480.05–0.280.16–6.03Bertoncelj et al. (2018)
Columbia, Italy and Spain Multi-floral14–1617.15–6–(Gardana et al. (2018) )
GreeceActinidia 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,andTribulus terrestris
13.59–27.6915.53–33.480.10–8.240.26–3.66Liolios et al. (2018)
BrazilCommercial bee pollen2.77–20.908.08–25.71––de Arruda et al. (2017)
ColombiaEucalyptus, Asteraceae, Mimosa caesalpiniaefolia, Piper,
Elephantopus, CyperaceaeandAnacardiaceae
13.3–18.218.7–26.9––de Melo et al. (2016)
BrazilAndira, Rubiaceae, Asteraceae, Mimosaceae, Fabaceae,
Aquifoliaceae, Anacardiaceae, Myrtaceae, Caesalpineaceae,
Brassicaceae,and others
6.3–74.9–5.5––Sattler et al. (2015)
ColombiaMulti-floral11.6–20.318.1–21.34.5–9.0–Fuenmayor et al. (2014)
ThailandZ. mays6.427.160.600.53Chantarudee et al. (2012)
Romania-4.37–16.148.44–15.39––Mărgăoan et al. (2012)
SpainCistus ladaniferand commercial multi-floral bee pollen 22.47–26.8619.88–23.783.04–8.55–Domínguez‐Valhondo
et al. (2011)
BrazilCommercial bee pollen6.99–21.8512.59–23.62––Martins et al. (2011)
ColombiaDry and wet multi-floral11.94–20.2715.65–20.344.42–9.02–Bobadilla (2009)
Amino Acids
CountryBotanical sourceEssential amino acidsReferences
ArgHisIle Leu LysMet Phe Thr TrpVal
Saudi Arabia Summer squash, date palm, rape sunflower, and
alfalfa
0.28–0.42 0.32–0.63 0.46–0.72 0.97–0.13 0.64–0.89 0.04–0.07 0.12–0.31 0.40–0.52 0.05–0.12 0.83–0.99Taha et al. (2017)
Colombia,
Spain and
Italy
Multi-floral0.96–4.64 0.49–0.68 018–0.64 0.47–1.34 0.39–0.87 0.19–0.21 0.44–0.87 0.10–0.31 0.11–0.15 0.29–0.70Gardana et al. (2018)
IndiaCocos nucifera, Coriandrum sativum, Brassica napus
andMulti-floral
0.97–1.19 0.35–1.23 0.38–1.01 1.76–2.47 1.35–2.01 0.12–0.47 0.92–0.65 0.53–1.04 0.26–0.46 0.71–1.03Thakur and Nanda
(2018a)
Republic of
Korea
Actinidia argutaandQuercus1.1–1.5 0.4–0.60.9–1.3 1.5–2 0.7–1.2 – 0.2–1.2 0.4–0.9 –0.9–1.4Ghosh and Jung (2017)
BrazilSenna sp, Chamaecrista spandMimosa tenuiflora0.030.070.01–0.02 0.06 0.03–0.05 0.01–0.02 0.03–0.04 0.02–0.03 –0.03–0.04da Silva et al. (2014)
ChinaBrassica napus, Citrullus lanatus ,Camellia
japonica,Dendranthema indicum ,Fagopyrum
esculentum,andHelianthus annuus,
Nelumbo nucifera Gaertn ,Papaver rhoeas, Rosa
rugosa ,Schisandra chinensis ,Vicia faba , andZ.
mays
0.72–2.58 0.42–0.93 0.56–1.33 0.79–2.06 0.70–1.55 0.12–0.62 0.46–1.30 0.43–0.99 0.70–14.80 0.64–1.57Yang et al. (2013)
Non-essential amino acids
AlaAspCys Glu GlyPro SerTyr AsnGln
Saudi Arabia Summer squash, date palm, rape sunflower, and
alfalfa
1.13–1.35 1.42–1.65 0.12–0.24 1.32–1.84 1.47–1.76 0.03–0.06 0.71–0.89 0.13–0.29 ––Taha et al. (2017)
Colombia,
Spain and
Italy
Multi-floral0.43–1.19 0.21–0.46 0.07–0.09 0.13–0.29 0.08–0.25 16.2–19.8 0.23–0.47 0.36–0.89 0.29–0.49 0.09–0.23Gardana et al. (2018)
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M. Thakur and V. Nanda Trends in Food Science & Technology 98 (2020) 82–106
89

9. bee pollen (Carpes et al., 2009). Sun or shade drying should be avoided
due to the enhancement of microbial growth and drying below 3%
moisture is also undesirable due to discoloration and generation of off-
flavor derived from increased rate of chemical reactions like Maillard
browning, fructose dehydration, loss of aroma compounds and lipids
oxidation (Nogueira et al., 2012). Therefore, the dried pollen must have
moisture content varying from 5 to 9% and humidity level after drying
should be kept in a range of 4–8% which retains the pollen nutrients
and ensures the safety (de Arruda, Pereira, de Freitas, et al., 2013).
Freezing is another technique to preserve the pollen nutrients but
pollen should be processed quickly after thawing, using lyophilization,
desiccation, and microwave-assisted drying (Conte et al., 2017).
3.2.2. Carbohydrates and sugars
Carbohydrates are the largest constituent of bee pollen which ac-
counts for nearly 2/3
rd
of the total pollen dry weight (Li et al., 2018).
The higher amount of carbohydrates is due to the incorporation of
honey or nectar during pellet formation thus enhancing the carbohy-
drates however, the plant species, growth and harvesting conditions are
important factors affecting its amount. The carbohydrates show a huge
variation from 18.50 to 82.80% in pollen throughout the world
(Table 2).
Pollen consists of monosaccharides - fructose and glucose and dis-
accharides - sucrose, turanose, maltose, trehalose, and erlose, with the
fructose/glucose ratio varying between 1.20 and 1.50. The higher
amount of reducing sugars is reported in bee collected pollen (Table 3)
which makes it distinct from plant pollen (Carpes et al., 2009). Liolios
et al. (2018)reported an average of 42.10% total sugars in thirty
monofloral pollen samples from Greece which varied from 34.70% to
63.50%. Among polysaccharides, the sporopollenin is present in exine –
the outer layer of a pollen grain, furnishing a rigid and sculptured
framework and is highly resistant to non-oxidative physical, biological
and chemical degradation processes including acetolysis thus con-
tributing to encapsulate and protect the pollen contents including
bioactive compounds. The inner layer of pollen known as intine consists
of cellulose and pectin andXu, Sun, Dong, and Zhang (2009)stated the
structural resemblance between intine and plant cell wall. However,
these polysaccharides are not responsible for contributing any nutri-
tional value but important in the regulation of several biological
functions.
3.2.3. Proteins and amino acids
Proteins are the largest component in pollen after carbohydrates
and fulfill the honeybee nutritional requirements. It is highly varying in
pollen collected from diverse plant sources (Table 2). However, protein
content even varies in uni-floral pollen of distinct countries:Brassica
napus- 19.63% (India), 23% (Brazil), 27.3% (China);Cocos nucifera-
25.39% (India), 10.3–20.3 (Brazil); andZea mays– 14.86% (Greece),
17.9% (China), 23.3% (Egypt) (de Melo et al., 2018a; Liolios et al.,
2016; Thakur & Nanda, 2018a; Yang et al., 2013). One the other hand,
the commercial bee pollen of Attiki Bee Culturing Co.-Alex Pittas S.A.,
Athens, Greece contained 17.60% protein (Karabagias, Karabagias,
Gatzias, & Riganakos, 2018). The possible reason for this is the mixing
of nectar in bee pollen. Moreover, bee pollen on drying may contain
2.5–62% protein depending on the botanical origin and such a high
amount signifies the role of this macronutrient as a novel dietary sup-
plement, particularly for vegetarians (Campos, Frigerioc, Lopes, &
Bogdanov, 2010).
Bee pollen dominantly contains bound-form amino acids and 1/
10th of total proteins are available as free amino acids whose compo-
sition is also affected by botanical origin and processing and storage
conditions (Domínguez‐Valhondo et al., 2011). The plant species affects
the amino acid composition more in terms of quantity rather than
quality (Table 3). Glutamic acid and in some studies proline as well as
aspartic acid are major amino acids reported in pollen from plant
species of different countries. The honeybees are directly responsible
Table 3(continued )
CountryBotanical sourceSugars (g/100 g)References
GlucoseFructoseSucroseMaltose
IndiaCocos nucifera, Coriandrum sativum, Brassica napus
andMulti-floral
1.59–2.33 2.32–2.81 0.19–0.25 2.35–3.03 0.22–1.84 2.08–2.52 0.52–0.91 0.36–0.44 ––Thakur and Nanda
(2018a)
Republic of
Korea
Actinidia argutaandQuercus1.1–1.4 1.6–2.70.1–0.3 2.1–2.2 0.9–1.2 0.7 0.9–1.1 0.6 ––Ghosh and Jung (2017)
BrazilSenna sp, Chamaecrista spandMimosa tenuiflora0.09–– – 0.04 0.95–1.18 0.37–0.43 0.03–0.04 0.08–0.10 0.02–0.02da Silva et al. (2014)
ChinaBrassica napus, Citrullus lanatus ,Camellia
japonica,Dendranthema indicum ,Fagopyrum
esculentum, Helianthus annuus, Nelumbo nucifera
Gaertn ,Papaver rhoeas, Rosa rugosa ,Schisandra
chinensis ,Vicia faba , andZ. mays
0.87–1.45 1.13–2.58 0.15–0.30 1.11–2.87 0.55–1.25 0.95–5.95 0.51–1.25 0.28–0.85 ––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.
M. Thakur and V. Nanda Trends in Food Science & Technology 98 (2020) 82–106
90

10. for the proline level which seems to increase during storage due to its
synthesis in the presence of glutamate dehydrogenase from glutamic
acid (Verslues & Sharma, 2010). Free amino acid content should be a
minimum 2% which is essential for the standardization of bee pollen in
the European market. Besides this, the “proline index” must be < 80%,
critical to indicate the pollen freshness (Canale et al., 2016). The bee
pollen also contains a higher level of essential amino acids (EAAs)
which furnishes the high nutritional value for honeybees and humans
(Yang et al., 2013; da Silva et al., 2014). According to the previous
studies, among EAAs, leucine and lysine were reported in the greatest
quantities from several countries (Table 3). In the viewpoint of human
nutrition, lysine – the limiting amino acid in cereals is present in ade-
quate amount and interestingly, tryptophan is reported in surprisingly
higher amount (0.70–14.80 g/100 g) in Chinese bee pollen which is
otherwise the limiting amino acid in pulses (Yang et al., 2013). Pollen
also contains the threonine - the second rate-limiting amino acid which
is along with isoleucine and phenylalanine is known as glucogenic as
well as the ketogenic amino acid, respectively (Dong et al., 2018). Being
the precursor of arserine, carnosine, and histamine, the histidine is also
important owing to the response of synthesized histamine for allergic
reactions and plays a great role in the dilation and blood vessels con-
traction (Peachey, Scott, & Gatlin III, 2018). Arginine is considered as
an essential amino acid in the present paper which is critical for child
nutrition only. Thus, all EAAs are reported in bee pollen (except a few
studies) ranging from 12 to 45.02% of total amino acid content which is
comparable to the supply of essential amino acids (33.9%) as per FAO
reference protein (Komosinska-Vassev et al., 2015; Thakur & Nanda,
2018a).
3.2.4. Lipids and fatty acids
After carbohydrates and proteins, lipids are the third-largest con-
stituent of bee pollen which are vital for the generation of royal jelly
(Sattler et al., 2015). Pollen from some botanical species contains total
lipid content, varying from 1 to 13% of pollen dry weight (Campos
et al., 2008), however, Martins, Morgano, Vicente, Baggio, and
Rodriguez-Amaya (2011), Odoux et al. (2012), de Melo et al. (2018a)
andLiolios et al. (2019b)revealed even higher lipid content up to
13.32, 24, 13.50 and 13.60%, respectively as shown inTable 2. They
are usually comprised of triglycerides, carotenoids, and sterols in bee
pollen (Mărgăoan et al., 2014; Sattler et al., 2015). However, a few
investigations focused on the sterols profile in bee pollen (Mărgăoan
et al., 2014) and most research work in the literature focused on the
estimation of total pollen lipid content (Table 2). The relative propor-
tion and level of certain fatty acids are very important in determining
the quality of lipids because honeybees require fatty acids for re-
production, development, and nutrition. The bactericidal and anti-
fungal properties of linoleic, linolenic, myristic, and lauric acids pri-
marily hinder the multiplication ofPaenibacillusandMelissococcus
pluton– the spore-forming bacteria and other microorganisms which
may colonize the brood combs otherwise, thus contributing to colony
hygiene (Dong, Yang, Wang, & Zhang, 2015). The human also requires
lipids due to fraction of essential fatty acids (EFAs) and antioxidant
substances for growth, development and prevention of diseases (Glick &
Fischer, 2013). Many biological functions require EFAs for regulated
levels of plasma lipids, insulin activity, cardiovascular, and immune
function, etc. to ensure better health (Glick & Fischer, 2013; Kaur,
Chugh, & Gupta, 2014).
Conte et al. (2017)reported a higher amount of phospholipids, to-
copherols, and phytosterols, recommending an intensive lipolytic pro-
cess as the pollen characterization parameter. In bee pollen, a strong
correlation was suggested between the fatty acids (FAs) composition
and botanical species, however, Brazilian pollen ofMimosa caesalpi-
niaefoliaandCestrumshowed a negative association (de Melo et al.,
2009; Mărgăoan et al., 2014; Sattler et al., 2015). These findings sug-
gested the association of certain pollen with more or fewer lipids con-
centrations. Moreover, huge variations are reported in lipid content of
mono-floral pollen from different countries:Brassica napus- 4.7%
(Brazil), 6.6% (China), 7.76% (Greece), 12.38% (India);Cistussp.
−1.9% (Italy), 3.80% (Greece), 7.2% (Spain);Cocos nucifera–10.43%
(India), 4.6–5.1% (Brazil) (Table 2) (de Melo et al., 2018b; Domínguez-
Valhondo et al., 2011; Liolios et al., 2019b; Sagona et al., 2017; Thakur
& Nanda, 2018a; Yang et al., 2013).
Nearly 20 FAs were reported in bee pollen from C4 to C24 among
which ω-3 fatty acids are dominating (Table S1). Myristic, stearic and
palmitic acids are the major saturated fatty acids while α-linolenic, li-
noleic and oleic acids are the most prevalent unsaturated fatty acids
reported in bee pollen. According to the literature, bee pollen of several
countries contains α -linolenic, palmitic, and linoleic acids in higher
amount along with significant levels of arachidonic, behenic, capric,
caproic, caprylic, 11-eicosenoic, elaidic, lauric, lignoceric, myristic,
oleic, and stearic acids (Table S1). Zea Mays(mono-floral) pollen from
China contained α-linolenic (52%) and palmitic (25%) acids as pre-
dominant fatty acids while the same origin pollen from Egypt was rich
in oleic (42%) and myristic (40%) acid. Likewise, the γ-linolenic acid
(29.08%) and eicosatrienoic acid (13.83%) were reported prevalent in
IndianBrassica napuspollen whereas the α-linolenic acid (30.82%) and
myristic acid (20.70%) were present in higher amount in bee pollen of
the same origin from China (Yang et al., 2013; Thakur & Nanda,
2018a). Keeping in view the previous studies, it is observed that fatty
acids are the same in different pollen but their proportion varies ac-
cording to the floral sources or even within the same species and geo-
graphical regions. It is believed that honeybees prefer the pollens which
contain a higher amount of unsaturated fatty acids compared to satu-
rated ones.Thakur and Nanda (2018a)reported the values of un-
saturated: saturated fatty acid (UFA to SFA ratio) of bee pollen ranging
from 2.2 to 6.7 which refers to the high quality of bee pollen lipids. A
higher value of UFA/SFA demonstrates the reduced levels of fats and
cholesterol, thereby preventing cardiovascular disease, but if the value
is below 1, the UFA/SFA ratio then exhibits the degradation of un-
saturated fatty acids during the time due to the storage and dehydration
process. The UFAs are an important component of membrane phos-
pholipids and therefore helps to maintain the membrane fluidity which
will thus improve the membrane functionality and also cell metabolism
(Mărgă; oan et al., 2014). Among fatty acids, the saturated, mono-
unsaturated and polyunsaturated fatty acids represented the
4.29–71.47%, 1.29–53.24%, and 4.33–75.71%, respectively in pollen
whereas ω-3 fatty acids varied from 8.07 to 44.1% and ω-6 fatty acids
ranged from 1.77 to 38.25% as reported in several studies summarized
inTable S1. Any fresh food is said to be the “source of ω-3 FAs” if ω-3
fats are found in concentration 300 mg/100 g under the regulation EC
1924/06 of Europe; therefore, bee pollen can be regarded as a sig-
nificant ω-3 FAs source for improved human nutrition (Li et al., 2018).
Further, the ω-6: ω-3 FAs ratio performs a critical role in the eicosa-
noids synthesis in the human body thereby regarded as beneficial to
health. ω-6:ω-3 ratio is an important criterion to evaluate the health
properties of food and it must be 5:1 or less (Simopoulos &
DiNicolantonio, 2016). Bee pollen contained this ratio varied from
0.059 to 3.090; thereby it is an essential source of ω-3 FAs in the human
diet (Mărgăoan et al., 2014; Thakur & Nanda, 2018a).
Bee pollen is the potential source of EFAs: α-linolenic and linoleic
acid, however, its amount varies according to the botanical origins
(Komosinska-Vassev et al., 2015). The amount of linoleic acid differed
greatly like 3.25–11.32 g/100 g in bee pollen from India, 7.62–33.21 g/
100 g from Romania and 2.66–24.38 g/100 g from China, while the α-
linolenic acid ranged from 0.5 to 16.28 g/100 g from Indian bee pollen,
20.28–46.93 g/100 g in Romanian bee pollen, and 4.11–58.52 g/100 g
in Chinese bee pollen (Yang et al., 2013; Mărgăoan et al., 2014; Thakur
& Nanda, 2018a). Both EFAs are important to carry the metabolic
processes and also being present as the component of cell membranes
thus improves the brain function (Perini et al., 2010). Docosahexenoic
acid, simply DHA (C22:6n-3) usually present in fish oil is also reported
in bee pollen. Nervonic acid – an important constituent of the white
M. Thakur and V. Nanda Trends in Food Science & Technology 98 (2020) 82–106
91

11. Table 4
Summary of mineral (mg/kg) and vitamins (mg/100 g) composition of bee pollen from different botanical origins throughout the world.
CountryBotanical sourceMinerals (mg/kg)
KCaPMgZn
Brazil–3182–73761401- 37243257- 6886789–174438–76
BrazilMimosa caesalpiniifolia, Eucalyptus,
Rubiaceae, Astrocaryum aculeatissimum ,C.
nucifera, M. verrucosa, Myrcia,
Alternanthera, Asteraceae, Anadenanthera,
andBrassicaas monofloral and other
heterofloral pollen
3400–9800900–4100–600–240030–101
BrazilAlternanthera, Anadenanthera, Cocos
nucifera, Mimosa caesalpiniaefolia, Myrcia,
Mimosa scabrella, Mimosa scabrellaand
Mimosa scabrella
5700–9100800–3900–900–230050.08–99.0
RomaniaBrassicasp,Carduussp.,Helianthus annuus ,
PrunusL. sp.,Crataegus monogynaand
bifloral and multi-floral
1980–4284294.1–2437–286.1–150520.21–59.57
IndiaCocos nucifera, Coriandrum sativum,
Brassica napusand multi-floral
3600–41001600-20003200–4600840–105025.27–53.82
TurkeyCommercial bee pollen992.12–2894.14491.85–1472.10795.89–5246.99271.12–1278.3414.83-39.07
Republic of KoreaActinidia argutaandQuercus10267-116701947–50417666–51741758–273796–102
TurkeyChestnut, buckwheat, oak and multi-floral
pollen
2420–4932909.0–2380–624.2–108325.94–49.74
Nigeria–910.0–826.6133.6991.5–948.344.0–72.00.1–3.0
BrazilCaesalpineaceae, Brassicaceae, Eucalyptus,
Carica, MachaeriumandRubiaceae
–643–7224430–5240–29–43
BrazilEucalyptus, Asteraceae/Linguliflora, Mimosa
caesalpiniaefolia,Piper, Elephantopus,
CyperaceaeandAnacardiaceae
2600–52001200–1700–500–90063.6–105.8
SerbiaBrassicaceae, Salix, Fabaceaeand other
multi-floral samples
2462–4236856–2032–503–96431.71–75.92
Saudi ArabiaCucurbita pepo Thunb ,Phoenix dactylifera
L.,Helianthus annuusL.,Brassica napusL.
andMedicago sativaL.
6232.79–8258.502086.36–5752.19234.40–468.052353.11–4680.5331.92–44.18
BrazilSenna sp, Chamaecrista spandMimosa
tenuiflora
5918.5–13366.61864.1–3424.9–975.4–2166.136.4–71.2
ColombiaMulti-floral3.06–7.621.09–2.41–343–154219.8–70.6
India, China, Romania,
Spain, Bulgaria,
Hungary and Poland
Commercial bee pollen3607–9542468–2376–484–119426.1–53.2
ChinaBrassica 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
2353–6358828–30532136–9587321–277728.25–65.30
BrazilCommercial dehydrated bee pollen1431–9910828–46702177–8165348–36215.1–76.1
SpainCistus ladaniferand commercial multi-
floral bee pollen
4961.79–5357.82520.33–792.603096.70–3197.29352.22–437.7216.30–20.21
RomaniaHelianthus annuusandSalix sp.3246.50–5421.851409.79–2630.67–2630.67–1008.2831.61–40.06
BrazilAsteraceaeand other multi-floral pollen4773.26–5383.73848.36- 1179.056873.40–7102.29679.01–818.0245.07–55.22
Vitamins (mg/100 g)
Fat-solubleWater-soluble
CountryBotanical sourceVit. A (β-carotene)Vit. DVit. EVit. KVit. B1
(continued on next page )
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92

12. Table 4(continued )
CountryBotanical sourceMinerals (mg/kg)
KCaPMgZn
BrazilEucalyptus, Asteraceae/Linguliflora, Mimosa
caesalpiniaefolia,Piper, Elephantopus,
CyperaceaeandAnacardiaceae
––2.72–5.37–0.5–1.3
BrazilAndira, Rubiaceae, Asteraceae, Mimosaceae,
Fabaceae, Aquifoliaceae, Anacardiaceae,
Myrtaceae, Caesalpineaceae, Brassicaceae,
and others
0.08–17.92–0.46–9.57––
BrazilArecaceae, Cecropia, Cestrum, Cyperaceae,
Eucalyptus, Ilex, Myrcia, Piper, Vernonia
andTrema
––––0.64–1.01
BrazilArecaceae, Cecropia, Cestrum, Cyperaceae,
Eucalyptus, Ilex, Myrcia, Piper, Vernonia
andTrema
––––0.59–1.09
ThailandZ. mays1.530–6.21–0.20
BrazilCommercial bee pollen0.31–9.92–1.63–4.30––
BrazilMimosa caesalpiniaefolia ,Myrtaceaeand
other multi-floral
0.51–7.79–1.63–3.86––
BrazilArecaceae, Philodendron sp, Anadenanthera
andEucalyptus
5.63–19.89–1.35–4.25––
CountryMinerals (mg/kg)References
FeMnCuNaCr
Brazil–––––Costa, Morgano,
Ferreira, and
Milani (2019)
Brazil46–118025–2157.4–19.720–374–de Melo et al.
(2018a)
Brazil78.9–1017.543.5–31410–17.138–279.3–de Melo et al.
(2018b)
Romania21.73–150.9––––Spulber et al.
(2018)
India82.40–24336.30–70.817.82–12.81150–2840.65–1.79Thakur and Nanda
(2018a)
Turkey28.60–725.368.15–54.633.73–14.99–0.34–1.59Altunatmaz et al.
(2017)
Republic of Korea322–34553–20428–47106–567–Ghosh and Jung
(2017)
Turkey44.79–161.412.36–40.467.222–13.425497–62232.81–7.94Kalaycıoğlu et al.
(2017)
Nigeria2.6–4.30.1–0.40.4–0.5105.8–111.2–Odimba, Azu, and
Oko (2016)
Brazil58–31228–626.8–13.1–2–42Sattler et al.
(2016)
Brazil––8.1–13.330.4–50.2–de Melo et al.
(2016)
Serbia44.10–114.9313.52–92.235.261–10.7374.95–54.880.170–0.465Kostić, Pešić et al.,
2015
Saudi Arabia338.12–562.0616.60–38.614.24–6.696345–8350.27–Taha (2015)
Brazil16.4–33.535.1–75.00.8–1.9––da Silva et al.
(2014)
(continued on next page )
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93

13. Table 4(continued )
CountryMinerals (mg/kg)References
FeMnCuNaCr
Colombia23.2126.6––8.9–206–Fuenmayor et al.
(2014)
India, China, Romania,
Spain, Bulgaria,
Hungary and Poland
28.8–197.7––84–379–Fuenmayor et al.
(2014)
China75.2–207.88.69–357.48.31–25.11274.1–846.4–Yang et al. (2013)
Brazil11.1–551.612–2113.2–25.4< 0.004–1466–Morgano et al.
(2012)
Spain20.15–29.6618.70–38.33 ±5.05–7.2060.74–64.77–Domínguez‐Valho-
ndo et al. (2011)
Romania27.42–122.87––––Stanciu et al.
(2011)
Brazil59.48–86.6642.60–73.5110.41–12.05191.02–215.35–Carpes et al.
(2009)
Vitamins (mg/100 g)
Water-solubleReferences
CountryVit. B2Vit. B3Vit. B5Vit. B6Vit. C
Brazil0.4–0.61.3–3.8–0.1–3.8–de Melo et al.
(2016)
Brazil––––6.03–79.70Sattler et al.
(2015)
Brazil1.77–2.567.27–14.430.33–0.777–56de Arruda, Pereira,
de Freitas, et al.
(2013)
Brazil1.73–2.416.43–15.340.50–0.79–de Arruda, Pereira,
Estevinho, & de
Almeida-Muradian
(2013)
Thailand0.507.030.39ND–Chantarudee et al.
(2012)
Brazil––––11.4–34.0de Melo and
Almeida-Muradian
(2010)
Brazil––––11.4–34.0de Melo et al.
(2009)
Brazil––––27.39–56.03Oliveira et al.
(2009)
K: Potassium; Ca: Calcium; P: Phosphorus; Mg: Magnesium; Zn: Zinc; Fe: Iron; Mn: Manganese; Cu: Copper; Na: Sodium; and Cr: Chromium.
M. Thakur and V. Nanda Trends in Food Science & Technology 98 (2020) 82–106
94

14. matter of animal brains is mainly obtained from lipids of fish and crab
eggs but its presence in bee pollen from different botanical origins of
multiple countries is a novel finding (Table S1), revealing the pollen
significance in human's nervous system and brain development.
Bee pollen also contains minute levels of phospholipids and plant
sterols (mainly β-sitosterol) (1.5 and 1.1%, respectively) wherein β-si-
tosterol and triterpene compounds such as oleanolic and ursolic acid
reduces the cholesterol absorption in intestines and generation of tumor
diseases, respectively (Komosinska-Vassev et al., 2015).
3.2.5. Dietary fiber
The dietary fiber, also known as roughage refers to the portion of
food which remains intact throughout the stomach and small intestine
thus contributing nothing to the nutritional value of food but is es-
sential to human health. The dietary fibers are basically of two types:
soluble and insoluble. The soluble dietary fiber (SDF) reduces the blood
cholesterol and glucose levels whereas the insoluble dietary fiber (IDF),
also called resistant starch, supports the passage of food through the
digestive system thus increasing the stool bulk and preventing the ir-
regular stools or constipation.
The dietary fiber comes from sporopollenin, cellulose, hemi-
cellulose, and pectin found in the outer-covering of bee pollen while the
starch and other insoluble polysaccharides such as callose, cellulose,
lignin, etc. constitute the crude fiber. However, the highest and lowest
values of crude fiber alter considerably (Table 2) due to various ana-
lytical methods and plant sources. Enzymes hydrolyze the complicated
fibrous pollen structures and release sugars to harness as a source of
carbon for bacterial fermentation (Bobadilla, 2009). However, the
change in fiber concentration due to fermentation is not significant
from the nutritional quality viewpoint.
Bee pollen is a useful fiber source for food, with cellulose and callose
as the main portion. Total dietary fiber (TDF) ranged from 17.60 to
31.26% while the IDF and SDF values varied from 73 to 82% and
0.86–5.92% of TDF in pollen from China (Yang et al., 2013). Likewise,
the Colombian pollen contained IDF contents higher (8.0–13.9 g/100 g)
than the SDF (1.3–2.3 g/100 g) with TDF of 9.9–15 g/100 g (Bobadilla,
2009). However, Fuenmayor et al. (2014)reported a higher amount of
SDF 2.7 ± 1.8 g/100 g compared to IDF (11.7 ± 3.3 g/100 g) in
Colombian pollen with TDF of 14.5 g/100 g. On the other hand,
Domínguez-Valhondo et al. (2011)studied the Spanish bee pollen
which showed no remarked variations in their dietary fiber
(14.50–14.65% dry weight) and suggested the exploration of pollen
fiber in processed foods to reduce the lack of dietary fiber.
3.2.6. Minerals
The mineral or ash content is essential for retaining the cell pro-
tection, activities, homeostasis, and health. For instance, calcium (Ca),
phosphorus (P), and magnesium (Mg), in combination, assists in the
development and maintenance of bone tissue and regulating the blood
as well as intercellular and cellular fluids osmotic pressure while cobalt
(Co), copper (Cu), iron (Fe), manganese (Mn), and zinc (Zn) are crucial
for the body growth, development, reproduction, and blood formation.
Hence, the insufficiency of these bio-elements may cause diverse me-
tabolic disorders, acute growth defects and even result in mortal ill-
nesses (Prashanth, Kattapagari, Chitturi, Baddam, & Prasad, 2015;
Quintaes & Diez-Garcia, 2015).
The day-to-day mineral requirements for humans were recorded:
Ca: 0.8–0.9 g, Cu: 1–3 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, selenium (Se):
60–120 μg, and Zn: 6–22 mg (Tayar & Cibik, 2011; Demirci, 2014)
whereas the following daily mineral specifications have been suggested
by Brazilian laws: Ca: 1000 mg, chromium (Cr): 35 μg, Cu: 900 μg, Fe:
14 mg, K: 4700 mg, Mg: 260 mg, Mn: 2.3 mg, P: 700 mg, Se: 0.034 mg
and Zn: 7 mg for an adult of 19–30 years age (Sattler et al., 2016). The
bee pollen possesses 2.5–6.5% ash content (Table 2) wherein above 25
minerals are present in it but the amount of each essential mineral
varies as per different floral sources and countries (Table 4). Ca, Cu, Cr,
Fe, K, Mg, Mn, Na, P, and Zn were commonly reported in bee pollen
globally and other minerals like boron (B), molybdenum (Mb) and se-
lenium (Se) are rarely present in bee pollen of few origins ranging from
8.2 to 14, 0.1–4.6 and < 0.01–4.5 mg/kg, respectively (Altunatmaz,
Tarhan, Aksu, Barutçu, & Or, 2017; Sattler et al., 2016; Yang et al.,
2013).
Ash content is largely affected by many factors, mainly soil, climate,
geographical origin, and botanical species in terms of plant capacity to
accumulate the mineral salts in its pollen (Carpes, 2008). Formicki,
Greń, Stawarz, Zyśk, and Gał (2013)andYang et al. (2013)have sug-
gested that soil type is the main cause for variation in element com-
position of pollen.Liolios et al. (2019a)had analyzed the similar pollen
taxa (Sinapis arvensisandCistus creticus) from ten different regions of
Greece and found significant differences in mineral content, particu-
larly K and Ca thus proving evidence of the effect of soil on the mineral
content of bee pollen. Another important reason for the mineral var-
iation is the addition of nectar to pollen which may alter the level of
certain minerals (Kostić, Pešić et al., 2015). However, the drying pro-
cess did not show any effect on the amount of Ca, Cu, K, Mg, Na, and
Zn, as observed byde Melo et al. (2016).
The mono-floralBrassica napuspollen from India and China con-
tained K as 4700 and 3825 mg/kg, respectively, whereas the
Brassicaceae based monofloral pollen from Serbia contained the K
content of 3200 mg/kg (Kostić, Pešić et al., 2015; Thakur & Nanda,
2018a; Yang et al., 2013). These days, Na consumption is increased
among the population because of the raised intake of processed foods.
But, bee pollen doesn't contain accelerated Na content (Thakur &
Nanda, 2018a). According to the literature, 25 g of bee pollen supplies a
maximum of 10% of the suggested intake of Na (2 g/day) by the World
Health Organization (WHO, 2012). Generally, most studies reported Na
content below 1000 mg/kg but this value reached to 1466, 6223 and
8350 mg/kg in Brazilian, Turkish and Saudi Arabian bee pollen, re-
spectively (Kalaycıoğlu, Kaygusuz, Döker, Kolaylı, & Erim, 2017;
Morgano et al., 2012; Taha, 2015). However, Na level was less than
400 mg/kg from more than 75% Brazilian pollen samples (de Melo
et al., 2016; Morgano et al., 2012). Therefore, pollen contains a higher
K: Na ratio owing to higher K and lower Na levels which is essential to
maintain the optimum electrolytic balance in the body (Carpes et al.,
2009).
According to theInstitute of Medicine (US) (2011), the daily Ca
intake of 1000 mg is suggested for a person of age 19–50 years and in
the literature, the maximum Ca content (5752 mg/kg) was reported by
Taha (2015). Bee pollen from Brazil had Ca content varying from 643 to
4670 g/kg (Carpes et al., 2009; de Melo et al., 2016; Morgano et al.,
2012). Through the phosphate (PO
4
−3) salts, Ca plays an important
part in blood coagulation, neuromuscular functions, the liberation of
hormones, a large number of enzyme-mediated mechanisms and bone
and tooth formation beyond being an enzyme component. Investiga-
tions supported that an adult may get 2–45% of recommended Mg in-
take which is 260 mg/day from 25 g bee pollen. Recent pieces of evi-
dence suggested that osteoporosis and related bone damages, artery
hardening or calcification is the result of elevated Ca and low Mg in-
takes (Lee, Kim, Kim, Seo, & Song, 2014). Likewise, Fe when consumed
in inadequate amounts, causes the behavioral and developmental dis-
orders, anemia, and poor immune system. Bee pollen is a good source of
iron and studies revealed that pollen in 25 g may supply 2–220% of the
recommended Fe intake i.e. 14 mg/day. Fe is greater in bee pollen than
other regular foods like bamboo shoot, cabbage, cassava, cauliflower,
mung beans, soybeans, and animal originated foodstuffs (de Melo et al.,
2018a; Yang et al., 2013). Similarly, bee pollen (25 g) can satisfy re-
quirements of Zn to a maximum of 120% otherwise its daily suggested
consumption for an adult is 7 mg. Bee pollen also contains the elevated
Cu content and the positive association between levels of Zn and Cu and
antioxidant capacity (determined by DPPH and ORAC methods) was
noted, however, Zn and Cu are not considered antioxidant compounds.
M. Thakur and V. Nanda Trends in Food Science & Technology 98 (2020) 82–106
95

15. The reason for this may be an antioxidant enzyme named Cu–Zn su-
peroxide dismutase (Cu–Zn SOD) which is commonly found as cofactors
in crops (Mondola, Damiano, Sasso, & Santillo, 2016). Therefore, the
presence of Zn and Cu may be considered as an index for the existence
of Cu–Zn SOD enzymes in bee pollen also. The lack of Mn may cause
deficiency diseases particularly in females which can be reduced by
incorporating Mn-rich bee pollen thus supplementing the diet
(Panziera, Dorneles, Durgante, & Silva, 2011). Se is the constituent of
proteins that have a significant part in metabolic activities of thyroid
hormone, synthesis of DNA, reproduction and prevent the infection or
injury caused due to oxidative stress (Fairweather-Tait et al., 2011). Se
content ranged from < 0.001 to 0.445 mg/100 g in 154 Brazilian bee
pollen samples; however, it was not reported in Chinese bee pollen
(Morgano et al., 2012; Yang et al., 2013).
Further,Taha (2015)recommended the mineral constituents of
pollen as distinct markers to trace the floral source and regulate its
quality. However, sometimes due to insufficient cleaning methods,
impurities may present in pollen thus enhancing the ash content.
Therefore, the each mineral must be examined for its level in bee pollen
using advanced and reliable techniques like inductively coupled
plasma-optical emission spectrometry (ICP-OES), microwave plasma or
inductively coupled argon plasma - atomic emission spectroscopy (MP-
AES or ICP-AES) and total reflection X-ray fluorescence (TXRF) which is
an important quality index (Yang et al., 2013; Kostić, Pešić et al., 2015;
Formicki et al., 2013; da Silva et al., 2014; Thakur & Nanda, 2018a).
3.2.7. Vitamins
Vitamins have a major part to synthesize the vital cofactors, en-
zyme, and coenzymes based metabolic reactions (Mellidou et al., 2019).
They can be found in their original form in nature or exist as precursors
or pro-vitamins. Bee pollen usually contains a higher amount of water-
soluble vitamins and carotenoids, presented inTable 4. On part of In-
ternational Honey Commission (IHC), the specifications for vitamin
composition of pollen were suggested to be: 0.6–1.3 mg/100 g thia-
mine, 0.6–2 mg/100 g riboflavin, 4–11 mg/100 g niacin, and
0.2–0.7 mg/100 g pyridoxine whereas the vitamin B complex was also
discussed byMărgăoan, Mărghitaş, Dezmirean, Mihai, and Bobiş (2010)
and they reported the following levels of thiamine: 0.6–1.3 mg/100 g,
riboflavin: 0.6–2.0 mg/100 g, niacin: 4.0–11.0 mg/100 g, pantothenic
acid: 0.5–2.0 mg/100 g and pyridoxine: 0.2–0.7 mg/100 g.
Very few studies (Table 4) have been conducted about the vitamin
composition of bee pollen, focused on Brazil and Thailand only. A high
concentration of B-complex vitamins was reported byde Arruda,
Pereira, de Freitas, et al. (2013)andde Arruda, Pereira, Estevinho, et al.
(2013)in bee pollen from Brazil. Riboflavin, with involvement in the
metabolism of lipids, carbohydrates, proteins, pyridoxine, folic acid,
and cobalamin has a significant function in cellular respiration (Pinto &
Zempleni, 2016). Niacin after riboflavin is the dominating among B-
complex vitamins, thus indicating it a promising supplement for pel-
lagra (Chantarudee et al., 2012). Some authors reported the insignif-
icant amount of lipid-soluble vitamins and vitamin C. However,Sattler
et al. (2015)revealed the higher amount of ascorbic acid
(6.03–79.70 mg/100 g) in Brazilian bee pollen, till date and determined
four tocopherols - α, β, γ, and delta-tocopherol with their respective
mean values of 328, 0.21, 0.46 and 0.63 mg/100 g. Vitamin E has been
shown to correlate strongly with b* value, and thus yellow-colored
pollen might probably be linked with α-tocopherol (Sattler et al.,
2015).
β-carotene, also known as provitamin A has 1/6th biological ac-
tivity of vitamin A and is one of the antioxidant vitamins. Vitamin A in
terms of β-carotene was reported in corn bee pollen from Thailand
(1.530 mg/100 g) (Chantarudee et al., 2012) and Southeastern Brazil
(5.63–19.89 mg/100 g) (Oliveira et al., 2009). The difference in vi-
tamin levels may be employed as an indicator of the determination of
plant source of pollen; however, the botanical origin, season and pro-
cessing conditions affect the vitamin composition (Farag & El-Rayes,
2016). Further, the vitamin compounds due to their complexity and low
concentration are quite difficult to detect and quantify. Instead of op-
timizing the efficient extraction and purification process, however, the
development and validation of the quantification technique may sig-
nificantly reduce the analysis time, generate less waste and improve the
quantification of certain compounds (de Arruda, Pereira, de Freitas,
et al., 2013).
3.2.8. Polyphenols
Polyphenolic compounds refer to the main secondary plants’ me-
tabolites ranging from anthocyanins, flavonoids, flavonols, flavonones,
tannins, etc. to phenolic acids. The phenolic compounds exhibit several
biological properties like anti-tumor, anti-aging, anti-inflammatory,
anti-diabetic, anti-cancer, etc. due to their function of regulating the
enzymatic activity and signal transduction, scavenging the free radicals,
chelating the metal ions, and activating the transcription factors and
gene expression (Działo et al., 2016).
Usually, bee pollen of Portugal, USA, Brazil, China, Egypt, New
Zealand, and Greece had total phenolic content (TPC) and total flavo-
noid content (TFC) values ranging from 0.50 to 213 mg GAE/g and
1.00–5.50 mg QE/g, respectively (de Melo & Almeida-Murandian,
2017; Karabagias et al., 2018). Likewise, 56 bee pollen samples from
four different regions of Brazil had TPC and TFC values of
6.50–29.20 mg GAE/g and 0.30–17.50 mg QE/g, respectively (de Melo
et al., 2018a). TPC and TFC of bee pollen from different botanical
sources of several nations are summarized inTable 5. Recently, Kostić
et al. (2019)reported TPC and TFC in sunflower (Helianthus annuus) bee
pollen of Serbia varying from 2907 to 3816 mg/kg GAE and
843–865 mg/kg QE, respectively which were higher than detected for
the same bee pollen of Slovakia (Fatrcová-Šramková, Nôžková,
Máriássyová, & Kačániová, 2016). The possible reason for this would be
the variation in climatic conditions and geographical origin which in-
fluence the levels of phenolic compounds in plants (Tolić et al., 2017).
When pollen is exposed to poor air or cold conditions, there would be
an improvement in the biosynthesis of flavonoids during pollen gen-
eration and growth (Mohammadrezakhani, Hajilou, & Rezanejad, 2018;
Rezanejad, 2012).
The phenolic composition of bee pollen of distinct countries differs
in geographical and botanical backgrounds and possesses the flavonoids
such as apigenin, epicatechin, hesperetin, isorhamnetin, catechin,
kaempferol, luteolin, quercetin, naringenin, etc. and phenolic acids like
chlorogenic acid, ferulic acid, caffeic acid, gallic acid, vanillic acid,
syringic acid, p-coumaric acid, etc. (Table 5). The rape bee pollen from
China contained following biologically active compounds: iso-
rhamnetin, kaempferol, and its 3-O-glucosides, naringenin, rutin and
quercetin and its 3-O-glucosides (Zhang, Yang, Jamali, & Peng, 2016)
whereas the same biologically active compounds (except naringenin
and rutin) were reported in Spain originatedCistussp. pollen
(Maruyama, Sakamoto, Araki, & Hara, 2010). On the other hand, the
apigenin, catechin, epicatechin, kaempferol, luteolin, naringenin, rutin,
and quercetin were detected in bee pollen from Egypt (Mohdaly,
Mahmoud, Roby, Smetanska, & Ramadan, 2015). The bee pollen of
Echium plantagineumfrom Spain possessed the glucosides of anthocya-
nins, delphinidin, petunidinm, and malvidin (Sousa, Andrade, &
Valentão, 2016).Silva et al. (2009) reported isorhamnetin-3-O-(6″-O-E-
p-coumaroyl)-β-
D-glucopyranoside, for the first time, in pollen collected
byMelipona rufiventris– the stingless bee. Bee pollen usually contains
the following phenolic acids and their ester derivatives: caffeic, p-
coumaric, ferulic, p-hydroxybenzoic, gallic, protocatechuic, syringic,
and vanillic acid.de Florio Almeida et al. (2017)andNegri et al. (2011)
revealed the complex rosmarinic acid dihexoside and amide derivatives
of hydroxycinnamic and ferulic acids whileKarabagias et al. (2018)
reported the presence of isopimpinellin (furancoumarins), urolithin B
(hydroxycoumarins) and flavononols 3-O- or 7-O-glucosides (quercetin
3-O-rhamnosyl-galactoside, quercetin 3-O-xylosyl-glucuronide, iso-
rhamnetin-3-O-glucoside 7-O rhamnoside, and quercetin 3-O-
M. Thakur and V. Nanda Trends in Food Science & Technology 98 (2020) 82–106
96

16. Table 5
Summary of total pheolic content (TPC), total flavonoid content (TFC) and phytochemical composition of bee pollen from different botanical origins throughout the world.
CountryBotanical sourcePhenolic compound(s)References
Total phenolic
content (TPC)
Total flavonoid
content (TFC)
Name
PortugalCistus ladanifer ,Echiumsp. and
Apiaceae
35.05 mg GAE/g 6.81 mg QE/g Coumaroyl quinic acid, Myricetin-O-rutinoside, Luteolin-O-dihexoside, Quercetin-O-dihexoside,
Myricetin-O-hexoside, Myricetin-O-(malonyl)rutinoside, Isorhamnetin-O-dihexoside, Quercetin-O-
hexosyl-pentoside, 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-O-dihydroferuloyl protocatechuic
acid, Myricetin-O-acetyl hydroxybenzoyl protocatechuic acid-isomer 1, Myricetin-O-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, Quercetin-O-acetyl hydroxybenzoyl hydrobenzoic acid
isomer 2, O-dihydroxybenzoyl acetyl malonyl coumaric acid flavonoid derivative
Anjos et al. (2019)
SerbiaHelianthus annuusL.2.91–3.82 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, Isorhamnetin, Isorhamnetin 3-O-
glucoside, Narcissin, Kaempferol, Galangin, Luteolin, Apigenin, Acacetin, Genkwanin, Eriodictyol,
Naringenin, Taxifolin, Phloretin, Aesculin
Kostić et al. (2019)
ItalyHedera 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., Daucusand
Coriandrum gr.
4.2–29.6 mg GAE/g –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-O-rutinoside, Cyanidin 3-O-sophoroside, Naringin 6′-malonate, Naringin 4′-
O-glucoside, Naringenin 7-O-glucoside, Apigenin 7-O-(6′-malonyl-apiosyl-glucoside),
Tetramethylscutellarein, Luteolin 7-O-glucuronide, Apigenin 6-C-glucoside, Kaempferol 3-O-
glucuronide, Quercetin 3-O-rutinoside, Kamepferol 3,7-O-diglucoside, Quercetin 3-O-galactoside 7-O-
rhamnoside, Quercetin 3-O-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.
Rocchetti, Castiglioni,
Maldarizzi, Carloni,
and Lucini (2019)
EgyptTrifolium alexanderinumL0.8–2.3 mg GAE/g 0.1–0.85 mg QE/g –AbdElsalam, Foda,
Abdel-Aziz, and El-
Hady (2018)
BrazilMimosa caesalpiniifolia, Eucalyptus,
Rubiaceae, Astrocaryum aculeatissimum ,
C. nucifera, M. verrucosa, Myrcia,
Alternanthera, Asteraceae,
Anadenanthera,andBrassicaas
monofloral and other multi-floral
samples
6.5–29.2 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)
Alternanthera, Anadenanthera, Cocos
nucifera, Mimosa caesalpiniaefolia,
Myrcia,andMimosa scabrella
5.6–29.7 mg GAE/g 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)
–6.9–21.0 mg GAE/g 0.3–17 mg QE/g –Duarte et al. (2018)
Italy, Spain and
Colombia
Cistus ladanifer, Echium, Rubus
ulmifolius, Parthenocissus quinquefolia
Ampelopsis brevipedunculata, Brassica
napus, Taraxacum officinale,and
Trifolium pratense.
––Tri-caffeoyl- and caffeoyl-di-p-coumaroyl spermidine derivativesGardana et al. (2018)
GreeceCommerical bee pollen ( Papaver rhoes,
Chamomila recutita, Sinapis arvensis,
Cistussp.,Trifoliumsp.,Dorycniumsp.,
Cichoriumsp.,Convolvulussp.,Circium
sp.,Malva sylvestris, Fumanasp.,
Eucalyptus camaldulensis, Anemonesp.,
5.050 mg GAE/ml –Isopimpinellin, quercetin 3-O-xylosyl-glucuronide, hydroxycaffeic acid, urolithin B, p-coumaroyl
tyrosine, quercetin 3-O-rhamnosyl-galactoside, quercetin 3-O-xylosyl-glucuronide, isorhamnetin-3-O-
glucoside 7-O-rhamnoside, quercetin 3-O-rutinoside
Karabagias et al.
(2018)
(continued on next page )
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97

17. Table 5(continued )
CountryBotanical sourcePhenolic compound(s)References
Total phenolic
content (TPC)
Total flavonoid
content (TFC)
Name
Ononissp.,Asphodelussp., andQuercus
ilex )
BrazilCocos nucifera––6-O-caffeoyl glucoside, trihydroxycinnamic acid, quercetin-3-O-rhamnosylglucoside, isorhamnetin-
di-3,7-O-glucoside, Isorhamnetin-3-O-(2″,3″-O-dirhamnosyl)glucoside, isorhamnetin-3-O-(2″-O-
rhamnosyl) glucoside, N′,N″,N‴-tris-caffeoyl spermidine, quercetin-3-O-rhamnoside - (quercetrin),
isorhamnetin-3-O-(2″-O-rhamnosyl acetyl) glucoside, N′,N″-dicaffeoyl,N‴-coumaroyl spermidine,
N′,N″-dicaffeoyl,N‴-feruloyl spermidine, N′-caffeoyl-N″-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
Negri et al. (2018)
GreeceCistus creticus15.20–60.20 mg
GAE/g
6.00–57.60 mg QE/
g
Quercetin-7-rhamnoside, quercetin-3-neohesperidoside, kaempferol-3-neohesperidoside, myricetin-
3-neohesperidoside, kaempferol-3-glucoside and quercetin-3-glucoside
Atsalakis, Chinou,
Makropoulou,
Karabournioti, and
Graikou (2017)
Malaysia–33.46–135.93 mg
GAE/g
15.28–31.80 mg
QE/g
–Fadzilah, Jaapar,
Jajuli, and Wan Omar
(2017)
ChinaRapeseed12.57 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, and
Zhuang (2017)
BrazilMimosa 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
–Vasconcelos, Duarte,
Gomes, Silva, and
López (2017)
Lithuania–3.5–23.3 mg GAE/g –Quercetin 3-O-sophoroside, quercetin dihexoside and isorhamnetin 3-glucosideČeksteryté et al. (2016)
SlovakiaHelianthus annuusL.0.69–0.80 mg GAE/g –Quercetin, kaempferol, luteolin, apigeninFatrcová-Šramková
et al. (2016)
ChinaBrassica campestris–604 mg RE/g Quercetin 3-O-glucoside, kaempferol 3-O-glucoside, naringenin, rutin, quercitrin, kaempferol, and
isorhamnetin
Zhang et al. (2016)
Colombia–24.79–33.69 mg
GAE/g
––Zuluaga et al. (2016)
Brazil–40 mg GAE/g 1 mg CAE/g –Bárbara et al. (2015)
ItalyCastanea, RubusandCistus13.53–24.75 mg
GAE/g
5.91–15.86 mg/g CE Gallic acid, 4-hydroxybenzoic acid, caffeic acid, and p–coumaric acidDomenici et al. (2015)
Lithuania–24.4–38.9 mg GAE/g 7.3–10.0 mg RE/g –Kaškonienė, Kaškonas,
and Maruška (2015)
ChinaRapeseed––Rutin, quercetin, kaempferol, and isohamnetinLv, Wang, He, Wang,
and Suo (2015)
EgyptZea mays––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 ± 0.08 nd α-Catechin 0.58 ± 0.05 nd Kaempferol
1.65 ± 0.24 0.59 ± 0.19 Apigenin 2.4 ± 0.25 3.57 ± 0.21 3,4-Dimethoxycinnamic acid
45.8 ± 0.16 nd Naringenin 3.34 ± 0.12 2.56 ± 0.28 Luteolin
Mohdaly et al. (2015)
PortugalEchium plantagineum––Kaempferol-3-O-(4″-rhamnosyl)-neohesperidoside, kaempferol-3-O-sophoroside, kaempferol-3-O-
neohesperidoside, kaempferol-3-O-neohesperidoside-7-O-rhamnoside, kaempferol-3-O-glucoside,
kaempferol-3-O-rutinoside + kaempferol-3-O-(3″/4″-acetyl)-neohesperidoside, delphinidin-3-O-
glucoside, delphinidin-3-O-rutinoside, petunidin-3-O-glucoside, petunidin-3-O-rutinoside, and
malvidin-3-O-rutinoside
Sousa et al. (2015)
ChinaWatermelon, rape, camellia, corn
poppy, corn, motherwort, buckwheat,
sesame, broad bean and rose
––Quercetin-3-O-b-
D
-glucosyl-(2/l)-b-glucoside, kaempferol-3, 40-di-O-b-D-glucoside and kaempferol-
3-O-b-
D
-glucosyl-(2/l)-b-D-glucoside
Zhou et al. (2015)
(continued on next page )
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98

18. Table 5(continued )
CountryBotanical sourcePhenolic compound(s)References
Total phenolic
content (TPC)
Total flavonoid
content (TFC)
Name
IndiaBrassica juncea18.29 mg GAE/g –Rutin, chrysin, kaempferol and quercetinKetkar et al. (2014)
Portugal and SpainCistaceae, Fabaceae, Cistaceae,
Ericaceae,andBoraginaceae
18.55–32.15 mgGAE/
g
3.92–10.14 mg QE/
g
–Pascoal, Rodrigues,
Teixeira, Feás, and
Estevinho (2014)
Latvia, Lithuania,
China, Spain
and
-24.1–45.5 mg RE/g 6.1–11.6 mg RE/g 2-hydroxycinnamic acid, rutin, quercetin, naringenin, and gallic, caffeic, and ferulic acidsKaškonienė,
Ruočkuvienė,
Kaškonas, Akuneca,
and Maruška (2014)
Turkey–44.07–124.10 mg
GAE/g
–Catechin, epicatechin, quercetin, rutin, and gallic, protocatechuic, p-hydroxybenzoic, chlorogenic,
vanillic, caffeic, syringic, p-coumaric, ferulic, benzoic, o-coumaric, abscisic and trans-cinnamic acid
Ulusoy and Kolayli
(2014)
BrazilBrassicaceae, Asteraceae elephantopus,
Asteraceae gochnatia, Myrtaceae
eucalyptus , andAsteraceae baccharis
20.22–48.76 mg
GAE/g
6.58–28.43 mg QE/
g
Rutin, myricetinCarpes et al. (2013)
Greece–––o-, p-coumaric acid, ferulic acid, myricetin, cinnamic acid, quercetin, naringenin, hesperitin and
kaempferol
Fanali, Dugo, and
Rocco (2013)
BrazilCecropia, Eucalyptus, Elaeis, Mimosa
pudica, Eupatorium,andScoparia
41.5–213.2 mg GAE/
g
–Isoquercetin, myricetin, tricetin, quercetin, luteolin, selagin, kaempferol, and isorhamnetinFreire et al. (2012)
PortugalRosaceae, Cistaceae, Boraginaceae,
Asteraceae, Fagaceae, Ericaeae,
MyrtaceaeandFabaceae
10.50–16.80 mg
GAE/g
––Morais, Moreira, Feás,
and Estevinho (2011)
USAMesquite, yucca, palm, terpentine bush,
mimosa,andchenopod
15.91–34.85 mg
GAE/g
2.66–5.48 mg QE/g Naringenin, 4′,5-dihydroxy-7-methoxyflavanone, 7,8,2′,4′-tetrahydroxy isoflavone, benzene acetic
acid, α-oxo, methyl ester, anthraquinone derivative, 5-methoxy-7-methyl-1,2-naphthoquinone, 7-
hydroxy-1-indanone, 1-p-tolyl-anthraquinone, 2-methyl-5-hydroxybenzofuran, 5-methoxy-7-methyl-
1,2-naphthoquinone, 1,2,3,4-tetrahydro-2-(2-hydroxy-3-phenoxypropyl)-6,7-dimethoxyisoquinoline,
1-)2-methoxy phenyl)-9,10-anthracenedione, 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, and Deeby
(2009)
M. Thakur and V. Nanda Trends in Food Science & Technology 98 (2020) 82–106
99

19. rutinoside) in commercial Greek pollen.
Polyphenolic compounds in bee pollen protect from biotic (micro-
bial growth) and abiotic (high temperature, synthesis of reactive
oxygen species and UV radiation) stress by their capacity to neutralize
the free radicals. Polyphenol metabolism includes the breaking of fla-
vonoids into monomeric units in the stomach. Sometimes, in the small
intestine, few flavonoid glycosides would be absorbed as whole by Na-
dependent glucose transporter 1 (SGLT1) (Williamson, 2017). The fla-
vonoids are mainly metabolized in the small intestine due to the ex-
istence of metabolizing enzymes like lactase phlorizin hydrolase, broad-
specific-β-glucosidase, and UDP-glucuronosyl transferase which pro-
duce the metabolites like sulfates, glucuronides, and O-methylated
aglycones including epicatechin, hesperetin, luteolin, naringenin, and
quercetin (Rzepecka-Stojko et al., 2015). These metabolites enter the
liver through membranes of the small intestine resulting in multiple
positive health effects. The remaining absorption of flavonoids carries
in colon containing gut microflora based enzymes which would de-
compose the flavonoids into phenolic acids (Li et al., 2018). Being
simpler in structures, the phenolic acids are easily metabolized or ab-
sorbed in the liver. However, the metabolism of polyphenols is quite
unclear and further research work must be conducted focusing the
polyphenol metabolism in humans.
3.2.9. pH and titratable acidity
pH and titratable acidity are critical factors during pollen storage
because they can influence the stability and shelf life. Both values also
indicate the dynamic microbial activity in food (Nogueira et al., 2012).
The increased levels of pH and titratable acidity in food are caused due
to fermentation, particularly by Gram-positive bacteria. The pH value
varied from 3.49 to 6.33 showing the natural slightly acidic nature of
bee pollen. Portuguese, Greek, and Indian bee pollen had almost similar
pH values of 4.3–5.2, 4.70, and 4.74–5.48, respectively (Feás et al.,
2012; Karabagias et al., 2018; Thakur & Nanda, 2018a). However, the
free acidity ranged from 128 to 294 meq/kg which exhibited the acidic
character of Brazilian bee pollen (Martins et al., 2011) while Colombian
bee pollen contained 155–402 meq/kg free acidity (Fuenmayor et al.,
2014) which provides information regarding conversion of sugars into
organic acids. However, the free acidity was not acclaimed byCampos
et al. (2008)as a product quality index.
Furthermore, no substantial pH (4.11) and titratable acidity (256.9
meq/kg) difference was caused while drying (60 °C) the pollen com-
pared to fresh bee-pollen (pH- 4.16; titratable acidity-245.6 meq/kg)
but difference was significant for both variables when drying was car-
ried out at 40 °C (pH - 4.02; acidity - 305.8 meq/kg) and 50 °C (pH -
4.04; acidity - 283.2 meq/kg). This recommends that the temperatures
below 60 °C may support some microbial activity that raises titratable
acidity and decreases pH values owing to their metabolic action
(Zuluaga-Domínguez, Serrato-Bermudez, & Quicazán, 2018).
4. Functional properties
The functional properties refer to the attribute(s) of food compo-
nents or ingredients except for its nutritional value which affects its
utilization (Thakur & Nanda, 2018b). These properties affect the fin-
ished product in terms of appearance, taste, and texture and conse-
quently, acceptance of the product. Bee pollen is typically multi-com-
ponent colloidal system, made up of biopolymers and a variety of
particles, such as oil droplets, gaseous bubbles, lipid crystals, etc.
The nature and strength of interactions of active surface compo-
nents with themselves and other pollen compounds (lipids, ash, and
carbohydrates) affect the properties of pollen system (Dickinson, 2013).
Bee pollen is known to have outstanding emulsifying characteristics,
higher carbohydrate solubility, and oil retention capacity. However,
variation in pollen composition owing to diverse botanical and geo-
graphical origin may alter the functional properties. Recently, the ad-
dition of bee pollen in different food products, as reported in few
studies, was successful efforts for processing the pollen (Krystyjan,
Gumul, Ziobro, & Korus, 2015; Zuluaga et al., 2016; Conte, Del Caro,
Balestra, Piga, & Fadda, 2018; Thakur & Nanda, 2019). However, its
role as a functional component in the food industry relies on the pollen
functional characteristics which therefore must be discussed in detail.
4.1. Solubility
The dissolution ability of any substance in water, called as solubility
followed the following process: (1) wettability of product, (2) disin-
tegration of product into primary particles, (3) material discharge from
particles into the aqueous phase and consistent destruction of surface
layer simultaneously until the complete particle breakdown and (4)
thorough dissolution of all materials (Mimouni, Deeth, Whittaker,
Gidley, & Bhandari, 2010).
Bee pollen has solubility ranging from 84.91 to 87.56% which is
majorly influenced by nature and composition of protein and carbo-
hydrates based on proportion between soluble (e.g. salivary secretions,
simple sugars, lower molecular weight proteins (50–25 kDa), vitamins,
etc.) and insoluble (e.g. cellulose, lignin, sporopollenin, lipids, higher
molecular weight proteins, etc.) constituents and corresponding inter-
linkages (Kostić, Barać et al., 2015; Thakur & Nanda, 2018b). The
pollen protein and carbohydrate solubility varied between 2.8 – 25.9%
and 31.2–75%, respectively (Kostić, Barać et al., 2015). Protein solu-
bility in pollen is similar to commercial concentrated and isolated soy
protein flours and also affects the other functional properties like
emulsification, foaming, and gelation (Kostić, Barać et al., 2015). It is
positively correlated to the carbohydrates level however; the lipid and
ash contents adversely affect the protein solubility. It is also associated
with the protein composition, conformation, their interaction with
other constituents and processing conditions.Kostić, Barać et al.,
(2015)reported the three limitsviz. higher (80-50 kDa), moderate (50-
25 kDa) and lower range (25-10 kDa) molecular weight proteins which
accounted for 13.40–32.20, 22.20–43.60 and 32.90–63.40% of soluble
proteins (Kostić, Barać et al., 2015). The higher levels of 80-50 kDa
molecular weight proteins were reported to negatively affect the pro-
tein solubility. Compared to protein solubility, the carbohydrate solu-
bility was higher in bee pollen due to the presence of nectar (com-
prising mainly water-soluble sugars), starch and pectin and it can be
affected by the proportion of soluble and insoluble carbohydrates and
their association with other components. The correlation test showed
the positive association of protein and lipid content with carbohydrate
solubility (Kostić, Barać et al., 2015).
Another important factor affecting solubility is wettability and dis-
persibility which were examined byThakur and Nanda (2018b)and
varied between 285.67 and 1909.46s and 34.10–51.06%, respectively.
The enormous difference in pollen wettability and dispersibility is
caused due to pollen chemical constituents, surface area properties,
variation in cultivar, and arrangement, texture, and configuration of
each pollen grains. The correlation studies byThakur and Nanda
(2018b)exhibited a strong negative relationship between the surface
area and wettability of bee pollen.
4.2. Water and oil holding capacity (WHC)
It is essential for products where the retention of moistness is as-
sociated with quality. Food ingredients that have high WHC may make
the product dry and brittle, mainly during storage. WHC of bee pollen
ranged from 0.47 to 2.25 g/g and this difference in WHC is mainly due
to hydrophilic components such as polar groups of insoluble proteins
and carbohydrates which are reported in 3-D structures and corre-
spondingly bind the water molecules through capillary action (Kostić,
Barać et al., 2015; Thakur & Nanda, 2018b). Further, the lipid mole-
cules which have polar and charged regions may account for improved
water holding. Therefore, variation in the composition of protein, car-
bohydrate, and lipid indicates the significant differences in WHC of
M. Thakur and V. Nanda Trends in Food Science & Technology 98 (2020) 82–106
100

20. pollen.
Oil holding capacity (OHC) is the degree of physical capture of oil
by food constituents on the grounds of composite capillary-attraction
process and ranged from 1.00 to 3.53 g/g in bee pollen (Kostić,
Barać et al., 2015; Thakur & Nanda, 2018b). Thakur and Nanda
(2018b)revealed the strong correlation between OHC and cohesiveness
of bee pollen. OHC is affected by several inherent variables like amino
acid composition, hydrophobicity and protein conformation. Further,
the sporopollenin is structurally similar to fatty acid-lignin-like material
entangles the oil in the matrix thus contributing to OHC. The higher
value of OHC in any product would enhance its applications.Thakur
and Nanda (2018b)recommended the coconut pollen to improve
mouthfeel and retain the flavor which showed its probability to utilize
in different formulations as a functional component.
WHC to OHC ratio, (known as water-oil holding index - WOHI)
reveals the equilibrium between hydrophilic and lipophilic constituents
of pollen and is lower than 1 which indicates its superior lipophilic
properties. Moreover, no correlation of WHC or OHC was obtained with
other functional properties and carbohydrates, lipids or protein con-
tents which demonstrate the complexity of interactions among them
(Kostić, Barać et al., 2015; Thakur & Nanda, 2018b).
4.3. Emulsifying properties
Emulsion usually provides the desired mouthfeel and is essential in
the structural development of foods such as frozen desserts, beverages,
coffee whiteners, mayonnaise, etc. (Serdaroğlu, Öztürk, & Kara, 2015).
Emulsifying properties of bee pollen including emulsion activity and
stability ranged from 44.83 to 46.76% and 21.62–26.32%, respectively
(Thakur & Nanda, 2018b). The emulsifying properties are influenced by
amount, conformation, hydrophobicity, and solubility of proteins; size
and distribution of liquid droplets; phase volume ratio; pH, temperature
and salt level of solvents and continuous phase viscosity (Avramenko,
Low, & Nickerson, 2013). The correlation studies by Kostić, Barać et al.,
(2015)reported the significant positive association between emulsion
stability and protein solubility while emulsion activity was negatively
linked to protein solubility. The protein with molecular weight 50-
25 kDa account for the emulsion stability while higher molecular
weight proteins are negatively linked thus indicating that oil/water
interface can adsorb smaller protein molecules better to produce
stronger interfacial layers compared to larger molecules (Kostić,
Barać et al., 2015). Further, emulsion stability and activity shared a
negative correlation due to stabler emulsions formation having greater
adsorbed substances at the interface.
Usually, natural food emulsifiers are proteins but polar lipids may
have good potential for better emulsifying properties. The interfacial
material of oil/water emulsion is comprised of proteins, phospholipids,
monoglycerides, esters of lipid acids, or mixture thereof. All these
compounds are present in pollen but in varying proportions due to plant
sources (Liang, Zhang, Shu, Liu, & Shu, 2013). Further, pollen contains
bioelements like K, Ca and other complex carbohydrates that blend
with interfacial compounds to create either stabilization or destabili-
zation properties. Hence, the main reason for lower coefficient values of
associations of pollen emulsion activity/stability with protein solubility
is the surface-active elements and their interactions (Kostić, Barać et al.,
2015).
4.4. Foaming properties
Foam refers to the systems which are formed by entrapping the gas
molecules in large amount inside the thin film of liquid or solid. Several
food products like bread, cakes, ice-cream, and whipped toppings are
dependent on the foam to maintain the structure and texture. The re-
tention of foam in the definite state is a tough task than emulsions due
to the different microstructure of foam bubble and its surroundings
than an emulsion droplet (Green, Littlejohn, Hooley, & Cox, 2013).
The bee pollen from Serbia did not possess any foam producing
capacity while the Indian bee pollen had foam capacity and stability
ranged from 6.21 to 8.69% and 17.50–20.00% (Kostić, Barać et al.,
2015; Thakur & Nanda, 2018b). Foaming capacity is strongly associated
with proteins that can reduce the water-air interface surface tension
and produce a constant cohesive film within the foam surrounding the
air bubbles (Kaushal, Kumar, & Sharma, 2012). Thakur and Nanda
(2018b)recommended the use of Indian bee pollen in foam derived
formulations such as marshmallows, cakes, ice-creams, mousses,
whipped cream, etc., whereasKostić, Barać et al., (2015)suggested the
pollen utilization as a foam depressant.
5. Food applications of bee pollen
Owing to its well-recognized nutritional and therapeutic properties,
bee pollen is usually consumed as a natural dietary supplement either in
fresh or dried form. Recently, the researchers have focused to utilize the
bee pollen in food systems, not only as a nutritious ingredient but also
as a functional component to enhance the product quality character-
istics.Yerlikaya (2014)incorporated the bee pollen into fermented milk
beverages and reported that antimicrobial activity was exhibited by
pollen when added in range 10–20 mg/mL. The supplementation of
fermented beverages with pollen also enhanced the probiotic viability
and beverage viscosity without affecting the sensorial attributes. Si-
milarly, acidophilus milk and probiotic yoghurt were also enriched with
bee pollen (0.6% w/w) wherein the lactic acid production was in-
creased, regardless of fat level (Glušac, Stijepić, Milanović; Đurđević-
Milošević, 2015). The use of bee pollen in bakery products is trending
whereKrystyjan et al. (2015)had fortified the biscuits andConte et al.
(2018)supplemented the gluten-free bread using bee pollen. Wheat
flour when substituted with 10% bee pollen, the prepared biscuits
contained significantly increased levels of protein, sugar, ash, fiber
polyphenols, and antioxidant potential; however, 5% of pollen was
needed to provide taste similar to the control samples of biscuits
(Krystyjan et al., 2015). On the other hand, Conte et al. (2018)showed
an improvement of techno-functional properties, decreased rate of
staling, and an increase in overall organoleptic acceptability of bread
without any destruction to dough development and leavening attributes
when enriched with bee pollen from 3 to 5%. These studies can provide
a base for further exploration of bee pollen as a promising ingredient in
other bakery products.
Some recent studies recommended the bee pollen as a natural an-
tioxidant substitute to inhibit the fat oxidation in black pudding and
refrigerated pork sausages which are attributed to the increased anti-
oxidant potential and higher levels of phenolic compounds (de Florio
Almeida et al., 2017; Anjos et al., 2019). Zuluaga et al. (2016)revealed
an increase in bioactive compounds, mainly carotenoids and anti-
oxidant potential of pineapple juice under pressure (400 MPa for
15 min) whereasKarabagias et al. (2018)reported an increase in total
phenolic content and antioxidant capacity of bee pollen yogurt in ad-
dition to improvement of end product cohesion and organoleptic
characteristics. Similarly,Thakur and Nanda (2019)developed the
polyphenol-rich vacuum-dried milk powder using rapeseed bee pollen
which may have potential in the formulation of processed products as a
functional component. Further applications of bee pollen in food pro-
ducts are thus based on thorough assurance about its nutritional value,
bioactive compounds, techno-functionalities, organoleptic attributes,
and safety. There is also a need to compare the effect of adding the
monofloral and multifloral bee pollen to food products for better un-
derstanding the impact of botanical source on product quality.
6. Safety aspects of bee pollen
Bee pollen intake is highly recommended as a natural dietary sup-
plement on account of its outstanding nourishing and healthy nutrients;
however, few risks are also associated with its intake due to the
M. Thakur and V. Nanda Trends in Food Science & Technology 98 (2020) 82–106
101

21. presence of potential contaminants like bacterial and fungal toxins,
heavy metals, pesticides, and allergic response. The poor and un-
hygienic production and storage conditions of bee pollen may favor the
microbial spoilage due to yeasts, molds, total viable count, lactic acid
bacteria and Enterobacteriaceae, which grows optimally at moderate
temperatures. This increases the health risk linked to intake of fresh
pollen whereas the bee pollen after drying are reported as micro-
biologically safe (Mauriello, De Prisco, Di Prisco, La Storia, & Caprio,
2017). On exposing to the environment (anthropogenic pollution,
water, and soil), the bee pollen may accumulate toxic heavy metals.
Several investigations reported the presence of heavy metals like ar-
senic (As), cadmium (Cd), mercury (Hg), lead (Pb) and strontium (Sr)
(Dinkov & Stratev, 2016; Kostić, Pešić et al., 2015; Roman, 2009).
de Oliveira, do Nascimento Queiroz, da Luz, Porto, and Rath (2016)
andBöhme, Bischoff, Zebitz, Rosenkranz, and Wallner (2018)reported
the presence of 26 and 73 different pesticides in bee pollen from Brazil
and Germany, respectively. The exposure of pesticide-contaminated bee
pollen to humans may result in several chronic diseases like the neu-
rological deficit, respiratory diseases, cancer, etc. (Mesnage & Seralini,
2018). The mycotoxin contamination is a greater concern where
ochratoxin A is among the hazardous toxic substances generated by
Aspergillus (Bogdanov, 2017). Echium vulgare, Symphytum officinale,
andSenecio jacobaeabee pollen reported the pyrrolizidine alkaloids
associated with hepatotoxic characteristics (Kempf et al., 2010).
Moreover, allergic reactions including anaphylaxis are usually the im-
mediate IgE-mediated hypersensitivity reactions which are identified
after pollen intake because individual pollen grains are collected from
insect-pollinated plants as well as wind-pollinated weeds or trees which
may cause the allergic reactions due to accidental intake of airborne
pollens (Choi, Jang, Oh, Kim, & Hyun, 2015; Jagdis & Sussman, 2012;
Makris et al., 2010). Recently, McNamara and Pien (2019)reported the
relation of exercise-induced anaphylaxis with pollen consumption in
atopic individuals due to the reduction of threshold for mast cell de-
granulation during exercise on account of enhanced gastrointestinal
permeability or osmotic effects and recommended that such individuals
after pollen intake should skip exercise for 4–6 h. Taking everything
into account, it may be said that primary risks behind allergy of bee
pollen are blending of bee pollen with airborne-pollen allergens, fungal
cross-reactive allergenic substances, contamination with pesticides and
exercise quickly after its intake.
Various international organizations such as WHO, FAO, and WTO -
World Trade Organization are responsible for establishing food quality
and safety standards; however, there are no harmonized global stan-
dards for bee pollen safety to date. A few countries like Argentina,
Bulgaria, Brazil, and Poland have established their guidelines for im-
proving the quality surveillance of pollen to increase safety. There is an
urgent need to revise the bee pollen guidelines by evaluating the bo-
tanical source, maximum residue limits (MRL) for heavy metals and
pesticides, microbial load and processing techniques before introducing
the bee pollen in the market. Further, labeling of bee pollen and any
food containing bee pollen should include the allergenic risk statements
to avoid the risks for allergic individuals. Legal requirements also need
to be established and adapted for processing systems from the farm
scale to pilot scale industries, producers, and bee pollen processing
stages. Moreover, effective training of beekeepers is very much neces-
sary by competent authorities so that the safety of bee pollen can be
ensured.
7. Future trends
The research work on characterizing the bee pollen, based on
physico-chemical and functional properties, has been increased rapidly
from the last 5 years. This may be due to the huge demand for natural
and healthy dietary supplements like bee pollen. Moreover, the use of
geographical index has further enhanced the horizon of bee pollen
global market particularly for properly analyzed distinct bee pollen
from botanical source and geographical origin. The plenty of pollen
studies are focused in Brazil, Colombia and Romania attributed to their
botanical diversity. However, bee pollen is still a new term in many
developing countries where even the beekeepers are unaware of its
potential as healthy food or functional ingredient or dietary supple-
ment. Therefore, the food industries, governments, and private orga-
nizations should come forward to encourage the beekeepers to harvest
the bee pollen which must be properly examined for their properties
before using in food processing. Further, the comprehensive composi-
tion of bee pollen should be examined with a focus on the botanical and
geographic origins using the novel and advanced techniques with
higher sensitivity, resolution, and accuracy. However, the determina-
tion of functional properties of bee pollen is essential for its valoriza-
tion. Only a few studies have been reported in the literature high-
lighting the functional characteristics, however, these properties are
also affected by the botanical diversity and location. Therefore, scien-
tists and researchers must pay attention to study the mono-floral bee
pollen which has a unique composition. Also, there is a strong need to
carry more research work to identify the mono-floral pollen up to
species level which is necessary for establishing the international
quality parameters of bee pollen.
8. Conclusion
Bee pollen as per nutritional and physico-chemical composition is
an excellent source of vital amino acids, ω-3 fatty acids, B-complex
vitamins, minerals, and polyphenols; however, the huge variation in
composition due to the different botanical and geographical origin is
still a challenge to promote the bee pollen market. Proteins and its
composition followed by lipid characterization are mostly studied by
the scientists and researchers with a mere focus on the functional
properties. Summarizing the data, bee pollen exhibited significant dif-
ferences in nutritional and physico-chemical composition as well as
functional properties. Emphasis should be given to study the mono-
floral pollen of varying geographical and plant sources for establishing
their uniqueness as well as safety in the diet. Further intensive research
should be conducted to enrich the diversity of bee pollen for promoting
its application in food processing industries.
CRediT authorship contribution statement
Mamta Thakur:Writing - original draft.Vikas Nanda:Writing -
review & editing.
Declaration of competing interest
The authors declare that there are no conflicts of interest.
Acknowledgements
The authors thankfully acknowledge Mr. Rishi Ravindra Naik and
Ms. Kirty Pant from Department of Food Engineering and Technology,
Sant Longowal Institute of Engineering and Technology, Longowal
(Punjab) India for assisting in modifying the corrections.
Appendix A. Supplementary data
Supplementary data to this article can be found online athttps://
doi.org/10.1016/j.tifs.2020.02.001.
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