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Файл:Ординатура / Хирургия / Библиотека им академика М.И. Перельмана / Книга_6035_Библиотеки_им_академика_М_И_Перельмана.pdf
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FIGURE 16.2 Acacia honey.
Source: Photographed by J. Ćirić.
FIGURE 16.3 Nectar in the frame.
Source: Photographed by J. Ćirić.
⏎
414
neochlorogenic, chlorogenic, protocatechuic, caffeic, sinapic, 3,4-di-O-caffeoylquinic,
and protocatechuic acid-O-hexoside acids), and one compound belonged to ellagic acid
(Sawicki et al., 2022).
FIGURE 16.4 Honey in the frame.
Source: Photographed by J. Ćirić.
⏎
Table 16.1 shows the polyphenolic compounds in the different honey samples as
reported by different researchers.
Chlorogenic acid, sinapic acids, gallic acid, ellagic acid, neochlorogenic, and protocatechuic acid were detected in honey in different studies (Yucel et al., 2016; Habryka
et al., 2021; Sawicki et al., 2022). Similarly, in the honey samples, sakuranetin dimer,
caffeic acid, and quercetin were also determined. Similarly, Habryka et al. (2021) detected
phenolic acids and avonoids (kaempferol, chrysin, galangin, and quercetin) in Polish
honey samples. The content number detected is related to the region of honey origin. Also,
previous studies have shown a relationship between the prole of volatile compounds in
honey samples and their geographic area of origin (Yucel et al., 2016; Habryka et al., 2021;
Sawicki et al., 2022).
Table 16.2 depicts the antioxidant activity of honey as determined by the ABTS and
DPPH assays and the PCL method. The order of average antioxidant activity for the
honey was as follows: ABTS > antioxidant capacity of lipid (ACL) (lipophilic antioxidant
capacity) > antioxidant capacity of water (ACW) (hydrophilic antioxidant capacity) >
DPPH. The multioral honey samples were also tested by Sawicki et al. (2022) for the
415
ability to scavenge superoxide anion radicals. The higher hydrophilic antioxidant capacity
of honey has been noticed in comparison to its lipophilic antioxidant capacity. The results
pertaining to honey’s antioxidant activity are consistent with the ndings from similar
studies examining multioral Polish honey (Wesołowska and Dżugan, 2017).
TABLE 16.1 The Polyphenolic Compounds in the Different Honey Samples
Polyphenolic Compound Concentration (µg/g)
Gallic acid 69.2 3.05 217.00
Ellagic acid 6.60 ND ND
Neochlorogenic acid 1.50 ND ND
Chlorogenic acid 13.20 ND ND
Protocatechuic acid 0.20 7.08 70.00
Sakuranetin dimer 4.60 ND ND
Caffeic acid 0.80 79.90 20.00
Rutin ND 56.66 ND
Sinapic acid 1.80 ND ND
Isorhamnetine 3-O-rutinoside
3,4-Di-O-caffeoylquinic acid ND ND ND
Quercetin 3-O-glucuronide
Orientin ND ND ND
Vitexin ND ND ND
Quercetin 2.20 ND ND
Epicatechin ND ND ND
Kaempferol ND 67.10 49.00
Protocatechuic acid-O-hexoside
Pinobanksin ND ND ND
Apigenin ND ND ND
ND ND ND
ND 247.40 40.00
ND ND ND
⏎
ND: not detected.
Source:
Reported by Habryka et al. (2021) and Sawicki et al. (2022).
TABLE 16.2 The Antioxidant Activity and Reducing Potential (FRAP assay) of Honey as Reported by
Different Researchers.
Assay Activities (µmolTrolox/g)
Reference
ACL (lipophilic antioxidant capacity) 1.53 ND
ACW (hydrophilic antioxidants) 4.72 ND
DPPH (1,1-diphenyl-2-picrylhydrazyl) 0.18 0.20
ABTS (2,2′-azinobis(3-ethylbenzothiazoline-6-sulfonic acid)) 15.6 1.78
FRAP (ferric reducing antioxidant power) 35.36 233.9
ND: Not detected.
⏎
Sawicki et al. (2022) Habryka et al. (2021)
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Honey content of different avonoids originates from pollen, nectar, or propolis (Khalil
et al., 2012). According to Bogdanov et al. (2008), the main avonoids found in honey are
pinocembrin, apigenin, campferol, quercetin, pinobanksin, luteolin, galangin, hesperetin,
and isorhamnetin. Table 16.3 shows the content of phenolic compounds and avonoids
in different honey samples by botanical origin and year of production. Kaškonienė et al.
(2009) show that heather honey contains 201.2 ±5.5 μg/g phenolic compounds. Similar
results were found in the study by Khalil et al. (2011), where the total content of phenolic
compounds in the Tualang honey ranged between 20.99 ± 0.13 μg/g and 42.23 ± 0.64
μg/g. Lianda et al. (2012) found that multioral honey has the highest content of phenolic
compounds as compared to other honey types. The highest avonoid content was identied
in heather honey (44.5 ±3.2 μg/g) followed by buckwheat honey (41.7 ±2.1 μg/g), lime
honey (32.0 ±1.7 μg/g) and rape honey (13.5 ±1.3 μg/g) (Kaškonienė et al., 2009). Cheung
et al. (2019) determined the contents of phenol compounds and avanoids in different
samples of honey. They did not detect avonoids in wolfberry honey, acacia honey, and
loquat honey . The highest total content of phenolic compounds was found in Manuka honey
(250.18 ± 14.39 μg/g). On the other hand, eucalyptus honey showed the highest content of
phenolic compounds (41.65 ± 10.35 μg/g) (Table 16.3).
16.3 BEE BREAD (PERGA)
The bee bread mainly includes pollen, honey, and secretions of bees’ salivary glands
(Figure 16.5 and Figure 16.6). Bee bread is a high source of different compounds, which
exhibit antioxidant activity . The main phenolic compounds in bee bread include quercetin,
kaempferol, myricetin, and luteolin. Bee breads are well known for their nutritional and
medicinal values and have been employed since prehistoric times for different therapeutic
purposes. Bee bread also acts as a functional food in preventing COVID-19, since bee
bread possesses unique criteria as a phytomedicine that could help to protect against, fight,
and alleviate severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) that causes
COVID-19 infection (Mohammad et al., 2020).
One of the most important differences between bee bread and bee pollen is that bee
bread is of higher biological value, better digestibility, and chemical composition than
bee pollen (Kieliszek et al., 2018). Honey bees inoculate this mixture (pollen, glandular
secretions, and nectar from crop) with their own microbiota. Inside the beehive, pollen
is stored in the bee wax cells, where fermentation by lactic acid bacteria (Lactobacillus,
Enterococcus, Lactococcus, Leuconostoc, Pediococcus, Streptococcus, Carnobacterium,
Aerococcus, Vagococcus, Oenococcus, Tetragenococcus, and Weissella) and yeasts started
(Ćirić et al., 2022).
During this fermentation process, pollen-added bee enzymes as well as enzymes
produced by the bee-bread microbiome increase its nutritional value. Also, it is tempting
to assume that the diverse bee-bread microbiota produces biological high compounds, thus
enhancing the bioactivity of bee bread (Kieliszek et al., 2018).
Table 16.4 summarizes the phenolic compounds available in bee bread. Phenolic
compounds are dened as secondary plant metabolites with protective mechanisms.
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TABLE 16.3 Contents of Phenolic Compounds and Flavonoids in Different Honey Samples (Mean ± SD)
Honey’s Origin Phenolic Compounds
Content(μg/g)
Buckwheat 201.60 ± 16.80 41.70 ± 2.10
Heather 201.20 ± 5.50 44.50 ± 3.20
Lime 153.10 ± 5.50 32.00 ± 1.70
Rape 71.70 ± 1.30 13.50 ± 1.30
Tualang honey 1 28.87 ± 0.41 20.52 ± 0.21
Tualang honey 2 20.99 ± 0.13 21.73 ± 0.43
Tualang honey 3 42.23 ± 0.64 25.31 ± 0.37
Gelam honey 20.20 ± 0.56 19.47 ± 0.23
Borneo tropical honey 15.21 ± 0.51 11.52 ± 0.27
Honey “B” 18.59 ± 0.47 15.40 ± 0.49
Manuka honey 52.63 ± 1.21 34.55 ± 0.45
Multifloral 78.20 ± 2.70 ND
Multifloral 42.80 ± 1.90 0.25 ± 0.03
Multifloral 57.20 ± 2.40 1.60 ± 0.16
Multifloral 54.00 ± 2.30 4.27 ± 0.43
Citrus sp.
Citrus sp.
Citrus sp.
Citrus sp.
Citrus sp.
Wolfberry honey 139.30 ± 14.07 ND
Acacia honey 52.60 ± 6.61 ND
Loquat honey 22.90 ± 3.22 ND
Manuka honey 250.18 ± 14.39 14.68 ± 1.20
Beech forest honey 188.13 ± 14.59 22.03 ± 6.03
45° South clover honey 76.36 ± 7.31 5.56 ± 0.55
Eucalyptus honey 175.05 ± 11.60 41.65 ± 10.35
Orange blossom honey 74.57 ± 6.68 17.37 ± 3.91
Wildflower honey 110.46 ± 8.39 33.66 ± 5.74
Black forest honey 135.22 ± 12.49 2.92 ± 0.48
35.70 ± 2.40 0.30 ± 0.03
38.80 ± 3.60 0.28 ± 0.04
53.20 ± 2.90 ND
40.10 ± 2.90 ND
34.00 ± 1.80 0.24 ± 0.01
Flavonoid’s Content
(μg/gRutinEquivalent)
Reference
Kaškonienė et al. (2009)
Khalil et al. (2011)
Lianda et al. (2012)
Cheung et al. (2019)
⏎
They include a large number of phenolic acids, avonoids, proanthocyanidins, and so on
(Mohammad et al., 2020). Several studies have detected the phenolic content of bee bread
(Mayda et al., 2020). In the study of Zuluaga et al. (2015), the total phenolic content of
Columbian bee bread ranged from 2.5 to 13.7 mg GAE/g. Rzepecka-Stojko et al. (2012)
found that the phenolic content of bee pollen was 21.30 mg GAE/g. Čeksteryté et al. (2016)
determined 23.3 mg GAE/g for bee pollen and 21.2 mg GAE/g for bee bread. In general,
kaempferol, myricetin, luteolin, isorhamnetin, and quercetin were the most detected
phenolic compounds in bee bread (Vit et al., 2018). Other phenolic compounds, gallic
acid, caffeic acid, and p-coumaric acid, were also detected in bee bread. It is expected
that phenolic compounds in bee bread vary widely, affected by differences in bee pollen
418
FIGURE 16.5 Bee bread in the frame.
Source: Photographed by J. Ćirić.
⏎
FIGURE 16.6 Bee bread.
Source: Photographed by J. Ćirić.
⏎
419
(botanical origins), season catchment area, and geographical location (Campos et al., 2008).
In general, many studies used two different methods to determine the antioxidant capacity
of extracts: the DPPH and ABTS assays. Both assays have been successfully employed to
estimate the antioxidant activities of bee products.
TABLE 16.4 Polyphenolic Compounds in the Different Bee Pollen Samples
Compound Content (µg/g)
Gallic acid 21.30 3.68
Ellagic acid 2.20 ND
Neochlorogenic acid 0.90 ND
Chlorogenic acid 0.70 ND
Protocatechuic acid 0.10 ND
Sakuranetin dimer ND ND
Caffeic acid ND ND
Rutin 10.00 50.80
Sinapic acid 42.80 ND
Isorhamnetine 3-O-rutinoside
3,4-Di-O-caffeoylquinic acid
Quercetin 3-O-glucuronide
Orientin ND ND
Vitexin ND ND
Quercetin ND ND
Epicatechin 7.20 ND
Kaempferol ND 179.53
Protocatechuic acid-O-hexoside
Pinobanksin 0.70 ND
Apigenin ND ND
5.80 ND
ND ND
7.90 ND
0.20 ND
⏎
16.4 BEE POLLEN
Bee pollen contains essential nutrients. According to Campos et al. (2008), carbohydrates
(13–55%), proteins (10–40%), lipids (1–13%), and fibers (0.3–20%), all contribute to
the composition of bee pollen. In addition, bee pollens are rich in biologically active
compounds like minerals and polyphenols. According to Habryka et al. (2016), bee pollen
is used in apitherapy mainly for its antioxidant and anti-inflammatory effects. Bee pollen
improves blood supply to the nerve tissue, thereby increasing mental performance and
eliminating the state of fatigue. Some studies have also shown a positive effect of bee
pollen on some diseases of the liver, heart, and prostate. The main consumers of bee pollen
are the followers of the health- and environment-conscious lifestyle, as well as the elderly
(Végh et al., 2021) (Figure 16.7).
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FIGURE 16.7 Bee pollen.
Source: Photographed by J. Ćirić.
⏎
Bee pollen is a very popular bee product that is presently not dened in most national
regulations. In Europe, many studies are conducted, but little data are available from
other continents. According to different studies, bee pollen is characterized by heterogeneous food safety risks and could also be used as a potential environmental bioindicator
(Ćirić et al., 2020).
One of the major secondary metabolites of bee pollen is polyphenols. The total phenolic
content values have been reported to range from 10.8 to 17.64 mg GAE/g for walnut bee
pollen (Cosmulescu et al., 2015), 28.87 mg GAE/g dry weight for chestnut pollen, and
from 16 to 36 mg GAE/g for Turkish pollen. Findings have shown that bee pollen contains
approximately 0.30–3.0% polyphenols (Yıldız et al., 2013).
Rzepecka-Stojko et al. (2015) showed the presence of phenolic acids (gallic, caffeic,
ferulic, 4-hydroxycinnamic, 4-t-p-coumaric, and t-cinnamic acids) and some avonoids
(rutin, myrycithin, quercetin, kaempferol, and isorhamnetin) in bee pollen from Poland.
Also, this study shows that the bee pollen did not contain some compounds detected in the
samples examined in another study (Rzepecka-Stojko et al., 2015). The main compounds
in the bee pollen were sinapic acid (42.80%) followed by gallic acid (21.30%) which are
the indicators of antimicrobial and antioxidant activities.
Many studies presented results that popular bee products have a high antimicrobial
activity. The highest antimicrobial activity was exhibited by bee bread (perga), which
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inhibited the growth of all the tested microorganisms (Staphylococcus aureus G3, S.
aureus 629G, S. aureus ATCC29213, Listeria monocytogenes 67, L. monocytogenes 74,
L. monocytogenes ATCC1912, Escherichia coli 14169, E. coli 25922, E. coli ATCC8793,
Salmonella typhimurium, S. typhimurium 235, S. typhimurium 63) (Sawicki et al., 2022).
Stronger antimicrobial properties of bee bread could be related to a high contribution of
gallic acid.
16.5 BEE PROPOLIS
Propolis is defined as a mixture of natural substances produced by honey bees from
substances collected from parts of plants and honey bees use propolis to defend the hive
(Figure 16.8). As with other honey bee products, different studies show that propolis
possess very high antimicrobial effects, hence used in medicine. This effect correlated
with the higher contents of polyphenols and terpenoids in propolis. The flavonoid group
includes chrysin, pinocembrin, pinobenchin, apigenin, quercetin, tectochrysin, pinostrobin,
and chrysin (Przybyłek and Karpiński, 2019). Other biological compounds of propolis are
aromatic acids, among which the most often occur are ferulic, cinnamic, caffeic, benzoic,
salicylic, and p
-cumaric acids (Bankova et al., 2000; Kędzia, 2006; Kędzia and Hołderna-
Kędzia, 2017). In addition, propolis also includes phenolic compounds (artepillin C), and
FIGURE 16.8 Bee propolis.
Source: Photographed by J. Ćirić.
⏎
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terpenes (Bankova et al., 2000; Kędzia and Hołderna-Kędzia, 2017; Kędzia, 2006). Kędzia
(2008) and Toreti et al. (2013) reported micro and macroelements (manganese, iron,
silicium, manganese, zinc, selenium, calcium, potassium, kalium, natrium, and copper)
and vitamins (B1, B2, B6, C, and E) in bee propolis. The presence of these abovementioned
bioactive compounds in various proportions is responsible for antimicrobial properties of
bee propolis (Pamplona-Zomenhan et al., 2011).
16.6 CONCLUSION
The antiviral activities of honey bee products were investigated in many studies against
SARS-CoV-2 infection (COVID-19) during the pandemic. Polyphenols present in bee
pollen and bee bread has promising activity against SARS-CoV-2. Beside polyphenols,
flavonoids and isoflavones have high antiviral activity.
KEYWORDS
• honey
• bee pollen
• bee bread
• functional foods
• antimicrobial effects
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