JFS R: Concise Reviews and Hypotheses in Food Science
M. VIUDA-MARTOS, Y. RUIZ-NAVAJAS, J. FERN´ ANDEZ-L´ OPEZ, AND J.A. P´ EREZ-´ALVAREZ
ABSTRACT: Honey, propolis, and royal jelly, products originating in the beehive, are attractive ingredients for
healthy foods. Honey has been used since ancient times as part of traditional medicine. Several aspects of this
use indicate that it also has functions such as antibacterial, antioxidant, antitumor, anti-inflamatory, antibrown-
ing, and antiviral. Propolis is a resinous substance produced by honeybees. This substance has been used in folk
medicine since ancient times, due to its many biological properties to possess, such as antitumor, antioxidant, an-
timicrobial, anti-inflammatory, and immunomodulatory effects, among others. Royal jelly has been demonstrated
to possess numerous functional properties such as antibacterial activity, anti-inflammatory activity, vasodilative
and hypotensive activities, disinfectant action, antioxidant activity, antihypercholesterolemic activity, and antitu-
such as flavonoids. Flavonoids have been reported to exhibit a wide range of biological activities, including antibac-
terial, antiviral, anti-inflammatory, antiallergic, and vasodilatory actions. In addition, flavonoids inhibit lipid per-
oxidation, platelet aggregation, capillary permeability and fragility, and the activity of enzyme systems including
cyclo-oxygenase and lipoxygenase.
Keywords: antimicrobial, functional properties, honey, phenolic compounds antioxidant, propolis
ways in which it may help maintain human health. The important
role that diet plays in preventing and treating illness is widely ac-
cepted. The basic concepts of nutrition are undergoing significant
change. The classicalconcept of “adequate nutrition,” that is, a diet
is tending to be replaced by the concept of “optimal nutrition,”
which includes, besides the above, the potential of food to promote
health, improve general well-being, and reduce the risk of devel-
oping certain illnesses. This is where functional foods, also known
medicinal foods, play their part (Nagai and Inoue 2004).
The concept of functional food is complex since it covers many
of the components, whether or not a nutrient in itself, affects tar-
get functions of the organism, so that it positively and specifically
promotes a physiological or psychological effect over and above
its traditional nutritive value. This positive effect may arise from a
contribution to the maintenance of health and well-being, such as
The market for functional foods is increasing at an annual rate
of 15% to 20% (Hilliam 2000). A functional food may be natural or
ecent years have seen growing interest on the part of con-
sumers, the food industry, and researchers into food and the
MS 20080450 Submitted 6/14/2008, Accepted 9/3/2008. Authors are with
Grupo Industrializaci´ on de Productos de Origen Animal (IPOA), Grupo
1 UMH, Grupo REVIV, Generalitat Valenciana, Dept. de Tecnolog´ ıa
Agroalimentaria, Escuela Polit´ ecnica Superior de Orihuela, Univ. Miguel
Hern´ andez, Ctra, E-03312 Orihuela, Alicante. Direct inquiries to author
Fern´ andez-L´ opez (E-mail: email@example.com).
be obtained by eliminating or modifying one or more of its basic
components (Perez-Alvarez and others 2003). Many components,
too, may be added to food to make them “functional” among them
ω-3 fatty acids (Hjaltason and Haraldsson 2006; Jacobsen and Let
2006), vitamins (Baro and others 2003), probiotics (Chaila and oth-
Malcata and others 2005), symbiotics (D’Antoni and others 2004),
fibre(Fern´ andez-Ginesandothers2004;Fern´ andez-L´ opezandoth-
ers 2004, 2007), phytochemicals (Wolfs and others 2006), bioactive
peptides (Korhonen and Pihlanto 2006; Thoma-Worringer and oth-
ers 2006),and so on.
Among foods that possess the characteristic of functionality, we
may include all those originating in the beehive: honey, propolis,
and royal jelly.
Honey forms part of traditional medicine in many cultures
(G´ omez-Caravacaand others 2006), although itis most widely used
as sweetener. It is composed of at least 181 components and is
basically a solution supersaturated in sugars, the fructose (38%)
and glucose (31%) are the most important (Gheldof and others
2002); the moisture content is about 17.7%, total acidity 0.08%, and
ashes constitute 0.18% (Nagai and others 2006). In addition, there
is a great variety of minor components, including phenolic acids
and flavonoids, the enzymes glucose oxidase and catalase, ascor-
bic acid, carotenoids, organic acids, amino acids, proteins, and
α-tocopherol (Ferreres and others 1993). The actual composition of
climate, environmental conditions, and the processing it under-
goes (Gheldof and others 2002; Azeredo and others 2003).
Propolis is a resinous substance that bees collect from the ex-
udates of plants and which they use to seal holes in the bee-
hive (Marcucci and others 2001). Propolis, too, forms part of
traditional medicine, and chemical analysis has pointed to the
presence of at least 300 compounds in its composition (Castro
C ?2008 Institute of Food TechnologistsR ?
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Vol. 73, Nr. 9, 2008—JOURNAL OF FOOD SCIENCE
Properties of beehive products. ..
(10%), pollen (5%), and other organic compounds (5%) (G´ omez-
Caravaca and others 2006). Among these organic compounds,
we may find phenolic compounds and esters, flavonoids in all
their forms (flavonoles, flavones, flavonones, dihydroflavonoles,
and chalcones), terpenes, beta-steroids, aromatic aldehydes and
alcohols, sesquiterpenes, and stilbene terpenes (Aga and others
1994; Russo and others 2002). As with honey, its composition varies
with different factors, such as source of the exudates, climate, and
environmental conditions (Chen and Wong 1996; Nieva-Moreno
and others 1999). Caffeic acid phenethyl ester (CAPE) is a biolog-
ically active ingredient of propolis with several interesting biologi-
cal properties, including apoptosis (Draganova-Filipova and others
2008), metastasis (Liao and others 2003), and radiation sensitivity
(Chen and others 2005) of cancer cells.
Royal jelly is the exclusive food of the queen honeybee (Apis
millifera) larva. Chemically royal jelly comprises water (50% to
60%), proteins (18%), carbohydrates (15%), lipids (3% to 6%), min-
eral salts (1.5%), and vitamins (Nagai and Inoue 2004) together
with a large number of bioactive substances such as: 10-hydroxyl-
2-decenoic acid (Caparica-Santos and Marcucci 2007) with im-
munomodulating properties (Ferlat and others 1994), antibacte-
rial protein (Fujiwara and others 1990), fatty acids (Vucevic and
others 2007), and peptides (Tokunaga and others 2004). The royal
jelly also demonstrated significantly improved the recovery from 5-
fluorouracil-induced damage (Suemaru and others 2008).
On the other hand, honey, propolis, and royal jelly may have
undesirable effects on health. Some researchers (Choo and oth-
ers 2008; Gunduz and others 2008) reported intoxication events,
such as cardiac dysrtythmias, hypotension, respiratory depression,
and altered mental status caused by grayanotoxin present in some
The intrinsic properties of honey affect the growth and survival
of microorganisms, in particular, the low pH and high sugar con-
tent of undiluted honeys prevent the growth of many species of mi-
croorganisms (Iurlina and Fritz 2005). In consequence, honey can
be expected to contain a small number and a limited variety of
microorganisms. These microorganisms include certain yeasts and
spore-forming bacteria; coliforms or yeasts indicative of sanitary
tain conditions could cause illnesses in humans (Snowdon and
Cliver 1996; K¨ upl¨ ul¨ u and others 2006; Finola and others 2008).
Other researchers found in honey several heavy metals such as Sb,
As, Cd(II), and Pb(II), which could cause illness (Rashed and Sultan
2004; Ioannidou and others 2005; Mu˜ noz and Palmero 2006; Pisani
and others 2008).
The aim of the present study was to study some of the functional
properties of some compounds produced by bees.
many foods, such as antioxidant capacity (Kerem and others 2006;
Almaraz and others 2007), antibacterial capacity (Huang and oth-
ers 2006; Theodori and others 2006), antiviral capacity (Evers and
others 2005; Ozcelik and others 2006), anti-inflammatory capacity
(Harris and others 2006; Wu and others 2006), cardio-protective ef-
fects (Moon and others 2003; Celle and others 2004), and the pre-
vention of enzymatic browning (Chen and others 2000; Jeon and
Zhao 2005). Among these foods, we may include honey, propolis,
and royal jelly since they contain phenolic compounds collected by
the bees from the plants where they gather nectar (Marcucci and
others 2001; Fiorani and others 2006).
henolic compounds in their many forms are the main compo-
nents responsible for the functional properties associated with
Phenolic compounds are found mainly in fruits, to which in
many cases they contribute color and taste (Belitzand Grosh 1997).
Chemically, phenols can be defined as substances that possess an
aromatic ring bound with one or more hydrogenated subsituents,
including their functional derivates (Mar´ ın and others 2001). The
as natural antioxidant and antimicrobial substances.
The simplest phenols are liquids or solids with a low fusion
point; they have a high boiling point due to the hydrogen bridges
they form. Most other phenols are insoluble. They are colorless,
but possess a group capable of being colored, which is why they
are frequently found colored when oxidized (Mar´ ın and others
The main groups of phenolic compounds present in plants,
whether in free form or as glucosides, are derivatives of cinnamic
acid, cumarins, and flavonoids (Manthey and Grohmann 2001).
In honey, propolis, and royal jelly, most of the phenolic com-
pounds are in the form of flavonoids (Table 1 and Figure 1), whose
concentration depends on various factors, including plant species
and so on (K¨ uc ¸¨ uk and others 2007).
their health, which has spurred greater research effort into such
foods. One of their most important properties is their antioxidant
capacity, which contributes to the prevention of certain illnesses,
including cardiovascular diseases, cancer, and diabetes (Ames and
others 1993; Gutteridge and Halliwell 1994). The importance of
protecting cell defense systems against the damage caused by
oxygen is well known. Free radicals and other oxidative agents
are of great importance in the action mechanism of many toxins
(Nagaiand others 2001). These radicalsinduce oxidativedamagein
biomolecules, such as carbohydrates, proteins, lipids, and nucleic
acids, which may alter the cell and provoke its death (Diplock and
others 1994). The tissues of living organisms possess their own pro-
matic systems such as superoxide dismutase, catalase, peroxidase,
and low molecular weight molecules such as tocopherol, ascorbic
acid, and polyphenols (Nagai and others 2001). The undesirable ef-
fects of oxidation reactions in foods also have to be taken into ac-
and others 2005). These effects include unpleasant odors and fla-
vors (Antony and others 2006; Fern´ andez-L´ opez and others 2006),
color loss (Thanonkaew and others 2007), and the loss of nutri-
Honey and other bee products, such as royal jelly and propolis
may be used as functional foods because of their naturally high an-
tioxidant potential. Apart from sugars, honey contains many minor
components with antioxidant activity (Gheldof and others 2002),
among them amino acids and proteins, carotenes, phenolic com-
pounds and flavonoids, ascorbic acid, organic acids, and Maillard
uring recent years, functional foods have attracted growing
attention because of consumers’ increasing concerns about
Table 1---Principal flavonoids present in honey, propolis,
and royal jelly.
Quercetin, kaempherol, galangin, fisetin
Pinocembrin, naringin, hesperidin
Apigenin, acacetin, chrysin, luteolin
Source: Cushnie and Lamb (2005) and Fiorani and others (2006).
JOURNAL OF FOOD SCIENCE—Vol. 73, Nr. 9, 2008
Properties of beehive products. . .
reaction products (Al-Mamary and others 2002; Schramm and oth-
ers 2003; Aljadi and Kamaruddin 2004).
According to Aljadi and Kamaruddin (2004), the antioxidant ca-
pacity of honey and propolis is due mainly to the phenolic com-
pounds and flavonoids they contain, and there is a high degree of
correlation between these substances and the antioxidant capacity
of honey, although a synergic action between several compounds
cannot be discounted (Johnston and others 2005; K¨ uc ¸¨ uk and oth-
ers 2007). Propolis, which also shows antioxidant activity, contains
amino acids, phenolic acids, flavonoids, terpenes, steroids, aldehy-
des, and ketones (Borrelli and others 2002).
Several researchers (Cowan 1999; Chen and others 2000;
Al-Mamary and others 2002; Yao and others 2003) reported that the
composition of honey and so its antioxidant capacity depends on
several factors, such as the flower source of the nectar, season, and
Figure 1---Chemical structures of
the most important flavonoids
found in honey and propolis.
environmental factors, such as soil type and climate, genetic fac-
tors, and processing methods. In other words, the possible health-
related effects due to the antioxidant activity of honey and propolis
may well depend on the origin of both (Baltrusaityte and others
to the presence of phenolic compounds and flavonoids, although
the exact action mechanism is unknown. Among the mechanisms
proposed arefree radicalsequestration, hydrogen donation, metal-
lic ion chelation, or their acting as substrate for radicals such as su-
peroxide and hydroxyl (Van Acker and others 1996; Al-Mamary and
These biophenols may also interfere with propagation reactions
(Cotelle and others 1996; Russo and others 2000), or inhibit the en-
zymatic systems involved in initiation reactions (Hoult and others
Vol. 73, Nr. 9, 2008—JOURNAL OF FOOD SCIENCE
Properties of beehive products. ..
1994; You and others 1999). Note that the more hydroxyl groups
that flavonoids contain, the more easily they are oxidized (Mayer
and others 1998). Furthermore, studies made by Gazzani and oth-
antioxidants, may react more rapidly in the same conditions. It has
also been suggested that the organic acids present in honey, such
as gluconic, malic, and citric acids, contribute to antioxidant activ-
ity through metal chelation and increase the effect of flavonoids by
lase, also show antioxidant activity through their ability to elimi-
nate oxygen from foods (Rajalakshim and Narasimha 1999). During
processing heating may provoke changes in composition due to
caramelization of the carbohydrates, Maillard reactions, or fruc-
tose decomposition. All these reactions lead to the formation of
hydroxymethylfurfural aldehyde, other furfural compounds, and
Maillard reaction products that may act as antioxidants (Namiki
These antioxidant properties have already been assayed in meat
products such as minced turkey (McKibben and Engeseth 2002),
turkey breast (Antony and others 2006), ready-to-eat ground beef
patties (Jonhston and others 2005), and cured pork sausages (Han
and Park 2002).
he inflammatory process is triggered by several chemicals
and/or biologicals, including pro-inflammatory enzymes and
cytokines, low molecular weight compounds such as eicosanoids
or the enzymatic degradation of tissues (Dao and others 2004).
According to several studies (Griswold and Adams 1996; Cho and
others 2004), the enzyme most related with the inflammatory pro-
cess is cyclooxygenase-2 (COX-2), an isoform of cyclooxygenase
(COX), which catalyses the transformation of arachidonic acid
to prostaglandin. The other isoform is cyclooxygenase-1 (COX-1),
which regulates homeostasis processes (Dao and others 2004). In
the last 30 y, many studies have pointed out the anti-inflammatory
properties of honey and propolis (Ali and others 1991; Ali 1995),
properties due basically to the presence of flavonoids that inhibit
the development of inflammation provoked by a variety of agents
(Laslo and Marghitas 2004; Teixeira and others 2005; Mani and oth-
This compound is capable of inhibiting cyclooxygenase (COX) and
lipo-oxygenase activity, limiting the action of polygalacturonase,
and reducing the expression of the inducible isoform of COX-2
(Raso and others 2001; Rossi and others 2002a, 2002b). Another
compound, caffeic acid phenethyl ester (CAPE), also present in
propolis, shows anti-inflammatory activity through inhibiting the
release of arachidonic acid from the cell membrane, which leads
to the suppression of COX-1 and COX-2 activity and inhibits the
activation of the genic expression of COX-2 (Mirzoeva and Calder
1996). These data were confirmed by the studies of Lee and others
Chrysin, another flavonoid present in both honey and propo-
lis, also shows anti-inflammatory activity (Kim and others 2002; Ko
and others 2003). Its action mechanism is related with the suppres-
sion of the pro-inflammatory activities of COX-2 and inducible ni-
tric oxide synthase (iNOS) (Cho and others 2004), as first suggested
by Jiang and others (1998). Woo and others (2005) also described
and COX-2 synthesis, although for these researchers the cellular
and molecular mechanisms by means of which chrysin inhibited
COX-2 synthesis were not clear.
Inhibition of Enzymatic Browning
in Fruits and Vegetables
nzymatic browning seriously affects the quality of foods. The
action of polyphenol oxidase is responsible for this process in
fruits and vegetables, while in crustaceans it prevents melanosis
(Aubourg and others 2007), provoking the appearance of brown
colors, unpleasant smells, and generally unfavorable effects on the
nutritional value of foods (Chen and others 2000). The browning
reactions induced by this enzyme have traditionally been coun-
tered by using chemical substances such as citric acid, ascorbic
acid, and sulfites. However, the high cost, restricted action peri-
ods, and potential health hazards of some of these products limit
their use in food (Jeon and Zhao 2005). Sulfites are the most po-
tent substances in preventing browning but their use may induce
asthma attacks or anaphylactic reactions in susceptible subjects
(Taylor and others 1986; Sapers 1993). For this reason, there is a
search for natural substances that have the same effect, while not
inducing harmful reactions.
Honey has been used since ancient times as sweetener, while
more modern studies have suggested it may also be a food pro-
tector (Osztmianski and Lee 1990; Chen and others 2000). As men-
act in this way, including ascorbic acid, small peptides, flavonoids,
α-tocopherol, and enzymes such as glucose oxidase, catalase, and
peroxidase (Ferreas and others 1993; Jeon and Zhao 2005). There-
fore, honey may be a natural alternative to sulfites for control-
ling enzymatic browning during fruit and vegetable processing and
for obtaining juices and preserves (McLellan and others 1995; Lee
lis on the DNA and RNA of different viruses, among them Herpes
simplex type 1, Herpes simplex type 2, adenovirus type 2, vesicu-
lar estomatitis virus, and poliovirus type 2. The effects observed in-
volve a reduction in viral multiplication and even a virucidal action
(Amoros and others 1992a).
It has also been claimed that various propolis fractions affect
the replication of viruses such as vaccinia virus and the virus re-
stances isolated from propolis have also been seen to have antiviral
activity. For example, isopentyl ferulate inhibits the infectious ac-
tivity of Hong Kong virus A (Serkedjieva and others 1992). In stud-
ies by Critchfield and others (1996), it was seen that characteristic
honey flavonoids, like chrysin, acacetin, and apigenin, inhibit the
activation of HIV-1 in latent models of infection through a mech-
anism that probably includes inhibition of viral transcription. Two
of the flavonoids present in propolis (chrysin and campherol) have
also been studied and were seen to be very active in the inhibition
of replications of several herpes viruses, adenovirus, and rotavirus
(Cheng and Wong 1996), while other flavonoids, which are re-
sponsible for antioxidant activity (galangin and acacentin) had no
effect on these viruses (Debiaggi and others 1990; Amoros and oth-
ers 1992b). However, other studies have pointed to the antiviral ef-
fect of galangin on herpes simple virus (HSV) and Coxsackieb virus
(Meyer and others 1997). Flavonoids such as quercetin and rutin,
which are found in both honey and propolis (Yao and others 2004;
Orsolic and Basic 2005), show antiviral activity against HSV, syncy-
Chithan 1993). The action mechanisms proposed for these com-
pounds are related with the inhibition of viral polymerase and the
binding of viral nucleic acid or viral capsid proteins (Selway 1986).
JOURNAL OF FOOD SCIENCE—Vol. 73, Nr. 9, 2008
Properties of beehive products. . .
show antiviral activity. However, the individual components may
also act synergistically. Indeed, some studies have pointed to
such synergism. For example, Amor´ os and others (1992b) and
Cushine and Lamb (2005) mention the synergistic effect of api-
genin and campherol on HSV, which would explain why honey
and propolis present greater antiviral activity than their individual
nother of the functional properties of both honey and propo-
lis is their anti-ulcerous capacity. Several studies describe such
activity in honey (Gurbuz and others 2000; Bruschi and others
2003) and, once again, this ability has been attributed to the pres-
ence of phenolic compounds, particularly the flavonoids (Gracioso
and others 2002; Batista and others 2004; Hiruma-Lima and others
2006). The action mechanism of these compounds varies: accord-
ing to Speroni and Ferri (1993), flavonoids increase the mucosal
content of prostaglandins, which enhances the protective effect on
the gastric mucosa, thus preventing ulceration. Vilegas and others
(1999) also mention how the flavonoids increase the mucosal con-
tent of prostglandins and have an important inhibitory effect on
acid secretions, preventing the formaton of peptic ulcers. Other re-
searchers (for example, Martin and others 1998) argue that ulcers
are related with reactive oxygen species, flavonoids inhibiting lipid
peroxidation, which considerably increases glutathione peroxidase
activity (Martin and others 1998; Young and others 1999; Duarte
and others 2001).
Some studies demonstrate the anti-ulcerous activity of cam-
pherol and quercetin, both of which are found in honey (Leite and
others 2001; Yao and others 2004; Orsolic and Basic 2005; Fiorani
and others 2006). Similarly, Kanaze and others (2003) attribute this
activity to the flavonoids hesperitin and naringin, which are found
in honey made from orange blossom (Ferreres and others 1993;
Ferreres and others 1994).
One theory suggests that the anti-ulcerous capacity of honey
and propolis is due to flavonoids but acting jointly with other sub-
stances such as esterols, terpinens, saponins, gums, and mucilage.
This idea is supported by Borrelli and Izzo (2000), Zhu and oth-
ers (2002), Al-Howiriny and others (2003), and Osadebe and Okoye
(2003), among others. All these substances are found to a greater or
lesser extent in both honey and propolis (Echigo and others 1986;
Sahnler and Kaftanoglu 2005; Teixeira and others 2005).
rently being revised. Two main theories have been proposed to
explain this capacity: one is that it is due to the action of the hydro-
gen peroxide in honey that is produced by glucose oxidase in the
presence of light and heat (Dustmann 1979), and the other is that
it is the nonperoxide activity, which is independent of both light
and heat, that inhibits microbial growth (Bogdanov 1984; Roth and
others 1986). This nonperoxide activity, which remains unaltered
nectar used and so not all honeys possess this activity (Molan and
The major components of honey are sugars, which themselves
possess antibacterial activity due to the osmotic effect they have
(Molan 1992), although studies carried out to test this antimicro-
bial activity use concentrations at which the sugars are not osmot-
ically active. It is also well known that honey contains lysozyme, a
powerful antimicrobial agent (Bogdanov 1997).
Other researchers attribute the antimicrobial capacity of honey
to a combination of properties, such as its low pH and high os-
molarity (Yatsunami and Echigo 1984), or to the presence of cer-
tain volatile substances, although this has not been studied in great
depth (Obaeiseki-Ebor and others 1983; Toth and others 1987).
The antimicrobial activity of both honey and propolis is basi-
cally against Gram-positive bacteria (Marcucci and others 2001).
Burdock (1998) attributes this capacity to the presence of aro-
matic acids and esters, while Takaisi and Schilcher (1994) suggest
that it is due to the action of the flavonone pinocembrin and the
flavonol galangin, and caffeic acid phenethyl ester, whose action
Cushnie and Lamb (2005) reported that other flavonoids such as
galangin also presents antibacterial action. The action mechanism
leads to a loss of potassium ions and the damage caused provoking
cell autolysis. Quercetin, which is also found in honey, increases
membrane permeability, and dissipates its potential, leading the
bacteria to lose their capacity to synthesis ATP , their membrane
transport, and motility (Mirzoeva and others 1997).
While the antibacterial capacity of honey is clear, there seems to
be no one clear-cut cause, suggesting that there is a combined or
synergistic effect at work.
tional properties but also for their functional and biological prop-
erties. Antioxidant, anti-inflammatory, antibacterial, antiviral, and
anti-ulcerous activities and also the capacity for the inhibition of
enzymatic browning are some of these important properties. These
activities are mainly attributed to the phenolic compounds such as
propolis, and royal jelly presented on the body, these products
could be considered as potential ingredients for different foods. In
any case, some precautions must be taken for their use in foods to
avoid some problems in persons who suffer from allergy by bee-
oney, propolis, and royal jelly are food products obtained
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