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Denisow Pietrzyket Al-2016-Journal of The Science of Food and Agriculture1
Denisow Pietrzyket Al-2016-Journal of The Science of Food and Agriculture1
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Abstract
Natural products, including bee products, are particularly appreciated by consumers and are used for therapeutic purposes
as alternative drugs. However, it is not known whether treatments with bee products are safe and how to minimise the
health risks of such products. Among others, bee pollen is a natural honeybee product promoted as a valuable source of
nourishing substances and energy. The health-enhancing value of bee pollen is expected due to the wide range of secondary
plant metabolites (tocopherol, niacin, thiamine, biotin and folic acid, polyphenols, carotenoid pigments, phytosterols), besides
enzymes and co-enzymes, contained in bee pollen. The promising reports on the antioxidant, anti-inflammatory, anticariogenic
antibacterial, antifungicidal, hepatoprotective, anti-atherosclerotic, immune enhancing potential require long-term and large
cohort clinical studies. The main difficulty in the application of bee pollen in modern phytomedicine is related to the wide
species-specific variation in its composition. Therefore, the variations may differently contribute to bee-pollen properties and
biological activity and thus in therapeutic effects. In principle, we can unequivocally recommend bee pollen as a valuable dietary
supplement. Although the bee-pollen components have potential bioactive and therapeutic properties, extensive research is
required before bee pollen can be used in therapy.
© 2016 Society of Chemical Industry
honeybees (Apis sp.) and utilised as valuable food.7,15 b 1st Military Clinical Hospital in Lublin, Poland
J Sci Food Agric 2016; 96: 4303–4309 www.soci.org © 2016 Society of Chemical Industry
www.soci.org B Denisow, M Denisow-Pietrzyk
antibacterial,27,34 antifungicidal,35 hepatoprotective,36 and ber of defence systems against ROS, i.e. endogenous antioxidants:
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Bee pollen and medicine www.soci.org
Figure 1. Potential therapeutic properties of bee pollen and plausible biological mechanisms by which the pollen compounds act. Abbreviations: NF-𝜅B,
nuclear factor kappa-light-chain-enhancer of activated B cells; ROS, reactive oxygen species; TNF-𝛼, tumour necrosis factor alpha; IgE, immunoglobulin E;
Fc𝜀RI, Fc epsilon receptor for immunoglobulin; ALA, 𝛼-linolenic acid; ↓, decrease/inhibition; ↑, increase/activation.
enzymes – catalase (CAT), superoxide dismutase (SOD), and per- Anti-inflammatory effects
oxidases. In many studies, the oxidative stress reduction by exoge- Substantial evidence suggests that pollen compounds (e.g.
nous dietary antioxidants has been well documented.41,42 polyphenols or flavonoids) may exert beneficial effects on numer-
Antioxidative effects (= inactivation of oxygen radicals) of ous cells (i.e. macrophages, T cells, B cells, NK cells, hepatocytes,
bee pollen is perhaps attributable to the activity of antioxidant mast cells, basophils, neutrophils, eosinophils), which play a crucial
enzymes as well as to the content of secondary plant metabolites role in host defence against invading pathogens and in inflam-
such as phenolic substances, carotenoids, vitamin C, vitamin E, matory processes.22,27 The anti-inflammatory action of flavonoids
and glutathione.41 Flavonoids are the most abundant and most may result from the activity of quercetin, which is known to inhibit
frequently studied class of polyphenols of low molecular weight. the arachidonic acid metabolism.28 A decrease in the arachidonic
Bee pollen contains, among others, quercetin, caffeic acid, caffeic acid level reduces the level of proinflammatory prostaglandins
acid phenethyl ester (CAPE), rutin, pinocembrin, apigenin, chrysin, and provides the anti-inflammatory effect.43 As a result, good
galangin, kaempferol and isorhamnetin.21,26 It has been shown
effects for the local pain elimination and prevention of platelet
that flavonoids present in bee pollen are capable of inactivation of
aggregation are observed after application of bee pollen.7,47
electrophiles, scavenge free radicals, ROS, and accordingly prevent
Another important mechanism of the action of bee pollen bio-
them from becoming mutagens.27 The hydrogen from the phe-
compounds on cell function may be the capacity to stimulate
nolic hydroxyl groups of flavonoids captures the free radical chain
or inhibit protein phosphorylation and thereby to modify cell
oxidation; thereby, they form stable end-products, which inhibit
signalling pathways, including inhibition of cell proliferation.1,26
further oxidation.19,20,23 Flavonoids also bind metal ions and in
this way may remove toxic metals from the body.21 Flavonoids Flavouring substances of bee pollen (e.g. anethole) are recog-
support the defence against free radicals and serve as a defence nised as a potent inhibitor of tumour necrosis factor (TNF)-induced
factor against genotoxic substances or carcinogens.31,43,44 In an nuclear factor (NF)-𝜅B activation. The nuclear factor (NF)-𝜅B path-
experimental clinical study, Duclos et al. documented weakened way has been considered a proinflammatory signalling pathway
oxidative stress and increasing antioxidation in prostatic secretion by expression of proinflammatory genes including cytokines and
and semen after application of extracts from bee pollen.45 adhesion molecules. The anti-inflammatory property of bee pollen
The flavonoid content significantly increases in ethanol, is thus expressed by inhibition of the proinflammatory NF-𝜅B
methanol/water, and water extracts from bee pollen.18 Con- pathway.28
sequently, pollen extracts exhibit higher antiradical activity The mechanism of the anti-inflammatory effect is also related to
compared to bee-collected pollen. However, the antioxidant the presence of fatty acids and phytosterols, which are active in
effect of bee pollen is species-specific and differs consider- the anti-inflammatory process.10,48 Particularly beneficial effects of
ably between plants.3 In the study of Fatrcová-Šramková et al., bee pollen in removing swellings of cardiovascular and renal origin
the antioxidant effect decreased in the following order: Bras- have been reported.49 Generally, the anti-inflammatory activity of
sica napus subsp. napus (Brassicaceae) > Papaver somniferum bee pollen is compared to such non-steroidal anti-inflammatory
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(Papaveraceae) > Helianthus annuus (Asteraceae).46 drugs as naproxen, analgin, phenylbutazone or indomethacin.10
J Sci Food Agric 2016; 96: 4303–4309 © 2016 Society of Chemical Industry wileyonlinelibrary.com/jsfa
www.soci.org B Denisow, M Denisow-Pietrzyk
Complementation of conventional therapy with bee pollen no antimicrobial effects on bacteria (Bacillus cereus, Bacillus subtilis,
improves the condition of patients with asthma.50 Escherichia coli, Salmonella typhimurium, Staphylococcus aureus,
Yersinia enterocolitica, Enterococcus faecalis and Listeria monocyto-
genes) and fungi (Saccharomyces cerevisiae and Candida rugosa,
Anticarcinogenic activity
Aspergillus niger and Rhizopus oryzae) treated at concentrations
Several studies have shown that bee pollen has greater or lesser
from 0.02% to 2.5% (v/v).57 Therefore, antimicrobial activity of bee
antimutagenic properties in certain types of cancer.23,33,51 The anti-
pollen is concentration dependent.
carcinogenic activities may be derived from its antioxidant prop-
The antibacterial effect of pollen is probably associated with the
erties, i.e. suppression of oxygen reactive species (ROS) formation
property of glucose oxidase, an enzyme produced by honeybees.
and removal or inactivation of oxygen reactive species.15,27,31 There
It is added to pollen when pollen granules are formed.19 It has
are also reports about the ability of bee pollen to induce apoptosis
also been shown that microbiological activity is related to phenolic
and stimulate secretion of tumour necrosis factor-alpha (TNF-𝛼).52
acids and flavonoids.57 The mechanism of the action of flavonoids
Thus, bee pollen may be considered to have cytotoxic activity on
and phenols against bacterial and fungal cells is degradation of the
cells by inhibiting their development.27
cytoplasm membrane, which leads to loss of potassium ions and
The effect of bee pollen extracts on inhibition of different cell
initiation of cell autolysis.
lines was reported for K-562 cells,51 leukaemia cells,53 or prostate
cancer PC-3 cells.44 The inhibition of respiratory burst within can-
cer cell lines treated with bee pollen extracts is probably associated Hepatoprotective and detoxifying activity
with their antioxidant potential.10 Strong cytotoxicity by trigger- In several studies on animals, pollen bioactive substances
ing apoptosis in human prostate cancer PC-3 cells was revealed improved liver function.58 Pollen extracts lowered pathologi-
after application of a steroid fraction of a chloroform extract from cal levels of enzymes (e.g. alanine, aspartate transaminase, acid
bee pollen harvested from Brassica campestris (Brassicaceae).52 phosphatase) and bilirubin present in the blood of individuals
The beneficial effects of bee pollen extracts in prostatic conditions poisoned with organic compounds (ethanol, carbon tetrachloride
are thought to arise from their presumed anti-inflammatory and and trichlorethylene, ethionine, ammonium fluoride) or with
anti-androgen effects.43 Pollen of Cistus ladaniferus (Cistaceae) drugs (paracetamol and hydrocortisone).59 The detoxifying pollen
has been reported to exhibit an anabolic and stimulatory impact activity is associated with polyphenols, mainly flavonoids and
on bone tissues in rats in vitro and in vivo54 and possess high phenolic acids.60 A detoxification effect of bee pollen has been
antioxidative and scavenging abilities.55 Saric et al. found that shown in rats intoxicated with heavy metals or pesticides (carbaryl,
antioxidant enzyme activity in the livers, brains and lysates of ery- protuxor).10 Therefore, bee pollen extracts are recommended in
throcytes in mice could be modulated by bee pollen extracts.56 For acute and chronic inflammatory conditions, initial degenerative
example, bee pollen extracts decreased the peroxidative break- conditions, and cholestatic liver diseases as well as in toxic and
down of membrane lipids in murine hepatic cells. Good results of post-traumatic damage to this organ.61
treatment with bee pollen have been reported in patients with
chronic non-bacterial prostate syndrome as well as in prostatic Anti-atherosclerotic effect
hyperplasia.6 Improvement in patients with benign prostatic Pollen extracts are reported to have hypolipidaemic activity by
hyperplasia (BPH) and patients with prostate cancer in the initial decreasing the content of total lipids, triacylglycerol, and choles-
stage was found after application of bee pollen [rye pollen extract, terol. Therefore, beneficial effects in cardiovascular disease have
Glycine max (soy), Prunus mexicana]. However, it has to be under- been reported.62,63 In patients with cardiovascular disease, intake
lined that in patients with prostate cancer the pollen application of bee pollen reduces blood viscosity and is effective in reduc-
was complementary to chemotherapeutic treatment.45 In accor- ing the intensity of atherosclerotic plaque formation and decreas-
dance with results obtained in cell cultures, it can be suggested ing platelet aggregation.10,64 These effects of bee pollen are
that bee pollen extracts with different types of compounds, espe- related to free forms of fatty acids (omega-3, a-ALA) present
cially phenolic acids and flavonoids (e.g. kaempferol, apigenin), in bee pollen (more than 50%), which act as a precursor for
help to control cell growth.51 Beneficial effects are also expected prostaglandin-3, the main inhibitor of platelet aggregation. More-
via enhancing and strengthening the immune system. over, increased fibrinolytic system activity has been confirmed
after pollen consumption.64 Such a property protects from heart
Antibacterial and antifungal effects diseases and brain strokes.7,63
Certain antimicrobial effects of commercial Spanish and Por-
tuguese bee pollen have been demonstrated, for example against Immune regulatory and anti-allergenic effect
Staphylococcus aureus and Candida glabrata.10 Antibacterial activ- Bee pollen is reported to strengthen the immune system. Qin
ity of monofloral bee pollen against pathogenic bacteria was and Sun documented improved cell immune response in mice
determined by Fatrcová-Šramková et al.46 For example, Staphylo- after application of an ethanol extract of pollen typhae (EEPT).65
coccus aureus was the most sensitive bacteria to an ethanol extract Stimulation of humoral immune response (an increase in specific
(70%) of poppy pollen (Papaver, Papaveraceae), and Salmonella IgM and IgG levels) was noted in rabbits.66 The immunosuppres-
enterica was the most sensitive bacteria to a methanol extract sive activity of bee pollen is presumably attributed to flavonoids,
(70%) of rape bee pollen (Brassica napus, Brassicaceae) and an steroids, and volatile oil compounds. Ishikawa et al. revealed that
ethanol extract (70%) of sunflower (Helianthus annus, Asteraceae). bee pollen might enhance the anti-allergic reaction by inhibiting
Listeria monocytogenes, Pseudomonas aeruginosa and Escherichia activation of mast cells, and thus exert an impact on both the early
coli were less sensitive to bee pollen extracts. The antibacte- and late phase of allergic reactions.67 The anti-allergic bee pollen
rial effect of an ethanol extract (80%) of bee pollen was shown activity is expressed by prevention of IgE binding to its receptor
against Staphylococcus aureus, Bacillus subtilis, Klebsiella sp. and (Fc𝜀RI) and inhibition of histamine secretion, the main stimulator
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Bee pollen and medicine www.soci.org
cloprid) or allergenic compounds or have life-threatening side profiles. Phytochem Anal 8:181–185 (1997).
J Sci Food Agric 2016; 96: 4303–4309 © 2016 Society of Chemical Industry wileyonlinelibrary.com/jsfa
www.soci.org B Denisow, M Denisow-Pietrzyk
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