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Bee World

ISSN: 0005-772X (Print) (Online) Journal homepage: http://www.tandfonline.com/loi/tbee20

Propolis: A Review

E. L. Ghisalberti

To cite this article: E. L. Ghisalberti (1979) Propolis: A Review, Bee World, 60:2, 59-84, DOI:
10.1080/0005772X.1979.11097738

To link to this article: http://dx.doi.org/10.1080/0005772X.1979.11097738

Published online: 31 Jul 2015.

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59

PROPOLIS : A REVIEW
by E. L. GHISALBERTI

Department of Organic Chemistry, University of Western Australia, Nedlands,


6009 Western Australia

Contents
PAGE
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Introduction 59
Origin of propolis 60
Collection of propolis by honeybees 60
Use of propolis by bees 61
Composition and constituents of propolis 62
Biological activity of the constituents of propolis 65
Pharmacological activity attributed to propolis:
Antibacterial and antifungal activity .. 68
Anaesthetic action of propolis 69
Use of propolis in dermatology 73
Other pharmacological activity 73
Toxicity of propolis 74
Phytoinhibitory properties 75
Commercial uses of propolis 75
Conclusion 76
References .. 76

Introduction
The last few years have seen a renewed interest in the properties of propolis, the
resinous hive product collected by bees. The use of propolis dates back at least to
300 BC58, when its resinous and glue-like qualities were made use of. Soon propolis
found its way into the remedies in folk medicine. However, apart from some studies
made at the beginning ofthis century, most of the work on the composition, pharma-
cological properties and commercial uses of preparations from propolis has been
carried out in the last thirty years. Many of the reports dealing with propolis are not
accessible to most readers except as abstracts, the majority being published by eastern
European journals.
The last detailed review in English seems to be that by Haydak in 195058 • With
the recent increased interest in the chemistry and pharmacology of propolis, an attempt
to collect together much of the information available seems timely.
This review is concerned with the origin and uses of propolis, the pharmacological
activity attributed to its extracts, and the compounds that have been isolated and
identified from them. Whether a chemical basis exists for the reported pharmaco-
logical effects of propolis is also discussed. It has not been possible to evaluate clearly
many of the results reported for propolis, since much of the information has been
available to the author only as short abstracts. Nevertheless, many of the publications
on propolis are cited, and it is hoped that this review and bibliography will provide
a starting point for those interested in the topic.
60

Origin of propolis
Propolis (bee glue) is the generic name for the resinous substance collected by honey-
bees from various plant sources. The word propolis is derived from the Greek pro-,
for or in defence, and polis-, the city, that is defence of the city (or the hive). Although
early observers of bee behaviour would have been aware of the plant origin ofpropolis,
some doubt clearly existed in the minds of workers who studied the composition of
propolis in the early 1900s. Helfenberg in 1908 mentioned 65 that bees obtained propolis
from the boughs, leaves and buds of the birch, ash, elm and balsam trees, hence the
composition of propolis varied with its origin. J aubert 70 in 1926 isolated from propolis
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chrysin, the compound responsible for the colour of beeswax, and he knew that propolis
was obtained from Populus nigra var. pyramidalis. The plant origin of propolis was
asserted by Rosch in 1927 135 and again by Vansell and Bisson in 1940 165 . Vansell and
Bisson examined propolis as a contaminant of beeswax, and concluded that the US
varieties originated from the buds of Populus nigra and the alder, Alnus viridis, in the
western states. Jungkunz 74 found pollen grains of Lupinus, Robinia and Onobrychis
sativa in the insoluble fraction of propolis, and stated that the wax in propolis was
apparently vegetable wax. Yet he wrote that the origin of propolis wax was unknown.
It is now generally accepted that bees collect propolis from various plant sources
in tlle north temperate zone, particularly species of poplar, birch, elm, alder, beech,
conifer and horse-chestnut trees. Rather little is known about these trees as sources
of propolis, and even less about sources of propolis in the tropics. There is some
evidence that in Western Australia bees may obtain some propolis from grasstrees
(Xanthorrhoea) which are unique to Australia.
Whether propolis is in any way altered by the bees remains a debatable point,
which will be touched upon under Composition and constituents. Here it is sufficient
to say that there is evidence that a number of compounds, present in the trees from
which bees forage for propolis, are found unchanged after the bees have apparently
used it.

Collection of propolis by honeybees


The mechanism of the worker bees' collection and delivery of propolis within the hive
has been described by various authors 3· 14 · 28 · 99 • 102 . One report 28 clearly describes
the collection of propolis from poplars; buds which developed on the branches in
early March attracted propolis foragers. The bees broke off pieces of the resinous
exudate from the buds, using their hind legs and mouthparts. The pieces were
moistened with the tongue and formed into pellets by the mandibles. With the help
of their legs, the bees brought the pellets from the mouth along the hair of the tibia
and into the corbiculae, the hairless indentation on the external side of the posterior
tibia. While packing one piece of propolis into the corbicula the bee would already be
groping for more propolis. The intricate leg movements involved in this procedure
have been illustrated by Meyer1° 2.
The collection of propolis could take a long time, and it might be interrupted by
visits to the hive for feeding. When the corbiculae had been filled, the bees finally
delivered the propolis to the hive. They might have to wait on the wall of the hive-
records ranged from one hour to two days-before the propolis load was removed by
other bees, which immediately utilized it. It appears that the bees that normally
forage propolis also use it in the hive. These bees were older than those that built
comb and capped honey cells, and the wax glands of most were atrophied.
61

The factor(s) which trigger propolis collection by the bees are not completely
understood. Some observers have suggested that seasonal factors may be responsible
rather than the availability of propolis. In northern Europe bees collect from late
June until the end of the flying season, but in Italy bees collect as early as March, at
the first signs of spring. Another suggestion is that the collection of propolis is initiated
by some inherent change in the behaviour of the foragers in late summer, not by
climatic conditions53 . It is conceivable that these factors may be interrelated with
those which are involved in the use of propolis by bees.
Use of propolis by bees
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Bees use propolis in a thin layer on the internal walls of their hive or other cavity they
inhabit. It is used to block holes and cracks, to repair combs, to strengthen the thin
borders of the comb, and for making the entrance of the hive weathertight or easier
to defend. Propolis is also used as an 'embalming' substance to cover the carcass of a
hive invader which the bees have killed but cannot transport out of the hive 108, e.g.
the wax moths Galleria mellonella and Achroia grisella, Acherontia atropos, Vespa
vulgaris, V. crabro, and small snails (Limacida, Arionida). The bees cover the invader
with propolis and wax, and the remains are left at the bottom or on one of the walls of
the hive.
The instinct causing the above behaviour patterns is interesting, and should be
considered with that which triggers off propolis collection. A number of rationaliza-
tions have been advanced. One suggests that propolis is used to provide an impervious
lining to the hive or nest cavity which limits the escape of water vapour needed by the
developing brood 10 , 104. Another interpretation is that bees use propolis during the
'completion' phase of a certain part of the nest, after which the bees leave that area17 2 ,
In this sense the 'embalming' process of intruders would simply be a continuation of
the bees' activity in 'completing' the nest. This appears to find support in some
observations that propolis is collected during the period of declining brood rearing,
before the onset of winter. In view of the uses to which bees put propolis, it seems
reasonable to suggest that its collection may occur also in response to adverse environ-
mental conditions in the colony, e.g. poor maintenance, presence of intruders.
It is noteworthy that some races of honeybees collect propolis more actively than
others. Grey mountain Caucasian bees collect rather more than dark forest bees,
whereas Italian, Ukrainian and Far East bees collect very little 150 . Tropical honeybees
A pis cerana, A. fiorea, A. dorsata and tropical Mrican A. mellifera are said to make no
use of propolis14 9; Carniolan bees are reported to use wax in place of propolis1°4 •
Apart from the purely mechanical use of the glue-like and cementing properties of
propolis, its use may have a chemical basis. The 'embalming' of intruders may serve
to contain putrefaction, and thus the spread of infections and disease. The presence
of propolis within the hive may also provide an environment not conducive to the
growth of bacteria and other micro-organisms. It has been suggested 39 that propolis
is in fact responsible for the lower incidence of bacteria and moulds within the hive
than in the atmosphere outside. The volatile constituents of propolis reduce the
aeroftora within the apiary 38 . It is likely that many factors are involved, and more work
will have to be done to gain a proper insight into this interesting aspect of bee behav-
iour. It seems valid, however, to ask if the chemical properties of propolis may not
only be beneficial to bees but may prove to have general pharmacological value. Most
of the work discussed below was done in seeking to answer this question, and the
sections that follow attempt to evaluate the evidence available.
62

Composition and constituents of propolis


Propolis is a resinous, sticky gum, whose colour varies from yellow-green to dark
brown depending on its source and age. It can be likened to an aromatic glue. It is
difficult to remove from the human skin, since it seems to interact fairly strongly with
the oils and proteins in the skin. It is hard and brittle when cold, but becomes soft and
very sticky when warm.
As a mixture, propolis does not lend itself easily to extraction or fractionation, so
it is not surprising that most of the early attempts to determine the composition of
propolis were concerned with simple fractionation of the mixture. The usual method
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was to extract the fraction soluble in alcohol, called the resin fraction, leaving the
alcohol-insoluble or wax fraction. Propolis 'balsam' referred to that fraction which
could be extracted with 70% alcohol. In the early 1900s estimations of the gross
composition ofpropolis (Table 1), presumably based on samples from various sources,
were qualitatively similar. Few attempts were made to purify further and investigate
the individual fractions. Notable exceptions are found in the work of Kustenmacher 87 ,
who identified cinnamyl alcohol (1)* and cinnamic acid (2) as constituents of propolis,
and of Dietrich who detected traces of vanillin (3) 44 • Some sixteen years later, in 1927,
Jaubert found that the colour of beeswax was due to the presence of the flavonoid
pigment chrysin (7) which could also be isolated from propolis 70 •
No report of the identification of other compounds in propolis appeared until 1969.
The lack of interest and activity was probably due to the intractable nature of propolis
and the lack of appropriate techniques for separation and analysis.
In 1969 Popravko et al. 122 • 123 applied modern separation and identification tech-
niques in an investigation of the components of propolis. Six flavonoid pigments were

TABLE 1. Percentage gross composition of propolis as determined between 1900 and 1950.

Volatile Soluble in
Author Resin and Wax Balsam (oils) alcohol Insoluble

Helfenberg, 1908 65 80·3 0 6·7 12·9


Bohrisch, 1908 21 8·7 27·9 6·9 12·9
Dieterich, 19084 2 64·6 16·1 6·0 12·9 some
Dieterich, 1911 43 78·6-72·6 3-8 5-6* 13·4
Dieterich, 1911 44 60·0 11·0 6 22·0
Heiduschka &
Vogel1913 63 70·7 14·8 5·0 4·2 5·3
Caillas, 1923 25 70·0 30·0
}ungkunz, 1932 74 68·9 19·3 4·0 0·5 4·3
Nicolas, 1947 108a 50 40 10

* soluble in water

* Compounds numbered (1), (2) ... are listed in Table 2.


63

TABLE 2. Constituents of propolis discussed in the text.

No. Common name Chemical name or formula

1 cinnamyl alcohol C 6H 5 CH = CHCH 20H


2 cinnamic acid C 6H 5CH = CHC0 2H
3 vanillin 4-hydroxy-3-methoxybenzaldehyde
4 isovanillin 3-hydroxy-4-methoxybenzaldehyde
5 caffeic acid 3,4-dihydroxycinnamic acid
6 ferulic acid 4-hydroxy-3-methoxycinnamic acid
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7 chrysin 5,7-dihydroxyflavone
8 tectochrysin 5-hydroxy-7-methoxyflavone
9 acacetin 5,7-dihydroxy-4' -methoxyflavone
10 5-hydroxy-4',7-dimethoxyflavone
11 quercetin 3,3',4',5,7-pentahydroxyflavone
12 kaempferide 3,5, 7-trihydroxy-4' -methoxyflavone
13 rhamnocitrin 3,4',5-trihydroxy-7-methoxyflavone
14 3,5-dihydroxy-4', 7-dimethoxyflavone
15 galangin 3,5,7-trihydroxyflavone
16 isalpinin 3,5-dihydroxy-7-methoxyflavone
17 5,7-dihydroxy-3,4 '-dimethoxyflavone
18 pectolinarigenin 5,7-dihydroxy-4',6-dimethoxyflavone
19 pinostrobin 5-hydroxy-7-methoxyflavanone
20 5-hydroxy-4',7-dimethoxyflavanone
21 pinocembrin 5,7-dihydroxyflavanone
22 sakuranetin 4',5-dihydroxy-7-methoxyflavanone
23 isosakuranetin 5,7-dihydroxy-4' -methoxyflavanone
24 quercetin-3,3' -dimethyl ether 4',5, 7-trihydroxy-3,3 '-dimethoxyflavone
25 pinobanksin 3,5,7-trihydroxyflavanone
26 3-acetyl pinobanksin 5,7-dihydroxy-3-acetylflavanone
27 pterostilbene (CH 3 0) 2C 6 H 3 .CH = CH.C 6H 40H
28 xanthorrhoeol
29 3,5-dimethoxybenzyl alcohol
30 myristic acid tetradecanoic acid
31 benzoic acid benzoic acid
32 benzyl alcohol benzyl alcohol
33 sorbic acid hexa-2,4-dienoic acid
34 eugenol 4-allyl-2-methoxyphenol

isolated and shown to be 5,7-dihydroxy-4'-methoxyflavone (acacetin) (9), 5-hydroxy-


4', 7-dimethoxyflavone (10), 3,5,7-trihydroxy-4'-methoxyflavone (kaempferide) (12),
3,4',5-trihydroxy-7-methoxyflavone (rhamnocitrin) (13), 5,7-dihydroxy-3,4'- dimeth-
oxyflavone (17) and 3,5-dihydroxy-4',7-dimethoxyflavone (14). Two flavanones
(-)-5-hydroxy-7 -methoxyflavanone (-(-)-pinostrobin) (19) and (-)-5-hydroxy-4',7-
dimethoxyflavanone (20) and the simple aromatic 3-hydroxy-4-methoxybenzal-
dehyde (isovanillin) (4) were also isolated. The amount of each of these compounds
ranged from 1 to 4% of the original sample of propolis. Evidence was obtained for
the presence of derivatives of another flavone, quercetin (11), but the compounds
64

were not further characterized. The compounds isolated were consistently found in
samples of propolis collected from different regions and by various races of bees.
The flavone and flavanone compositions of these extracts corresponded to those found
in dormant buds of Betula verrucosa 121 •
Following the observation of Lavie90 , that propolis showed significant antibacterial
activity towards Bacillus subtilis, B. alvei and Proteus vulgaris, French workers were
successful in isolating the flavone galangin (15) from extracts of propolis, and in
showing that the bacteriostatic activity attributed to their sample of propolis was due
partly to this compound 169 • Later work by the same group resulted170 in the isolation
of a flavanone, pinocembrin (21), which also showed similar activity to galangin. In
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addition, the flavones chrysin (7), tectochrysin (8) and isalpinin (16) were isolated and
identified. It is of some interest that these compounds had previously been isolated
from the young buds of poplar trees, from which bees are known to collect propolis;
the results indicate that these flavones are found in propolis unchanged. More recent
work has resulted in the isolation of caffeic acid (5) 33 and ferulic acid (6) 34 from samples
of propolis in eastern Europe. Both of these compounds are known to have anti-
bacterial activity on some gram-positive and gram-negative micr0-organisms 33 • 34 •
An investigation141 of the antimicrobial components in propolis led to the isolation
and identification of 17 constituents, including 9 previously isolated from other
samples of propolis; these were ( 7), (8), (1 0), (13), (15), (16), (19)-(21 ). The compounds
isolated for the first time were the two flavones pectolinarigenin (18), quercetin-3,3'-
dimethyl ether (24), three flavanones, sakuranetin (22), pinobanksin (25) and its
3-acetate derivative (26), p-coumaric benzyl ester, and an ester of caffeic acid with
an aromatic alcohol.
A preliminary investigation of the components in propolis collected by bees in the
south-west region of Western Australia has shown that the following compounds are
present48 : four flavanones, pinostrobin (19), sakuranetin (22), isosakuranetin (23)
and (20), pterostilbene (27) and the naphthalene derivative xanthorrhoeol (28). Trace
quantities of chrysin (7) and 3,5-dimethoxybenzyl alcohol (29) were also detected.
The possibility cannot be excluded 19 that (18) is an artefact arising from base-catalysed
cyclization of the corresponding chalcone during extraction.
Myristic acid (30) has been isolated from one sample of propolis, together with
quantities of other fatty acids ranging from C 7 to C 18 • The fatty acid constituents
represented about 5% of the sample 64 •
The presence of small amounts of vitamins has been reported for propolis obtained
in the USA. Vitamin B 10 B 2 , B 6 , C and E, and nicotinic acid and pantothenic acid
were detected in variable amounts 59 • 62 • Vitamin B 1 levels were estimated 60 as 4 · 5f.Lg/g
offresh matter (6·4 f.Lg/g of dry matter), vitamin A as 6 ·1 and 8 ·1 IUjg, riboflavin as
20 and 28 f.Lgfg 61 , and vitamin B 6 as 5 f.Lg/g of fresh matter.
Copper and manganese have been detected in propolis at levels of 26 · 8 mg and
40 mgjkg respectively 110• The ash residue of propolis has been shown to contain iron,
calcium, aluminium, vanadium, strontium, manganese and silicon66 •
Helfenberg 65 reported that there were no alkaloids or volatile oils in the sample of
propolis investigated. However, a recent report 69 describes the composition of the
steam-volatile fractions of a propolis sample. The compounds identified in the fraction
were benzoic acid (31), benzyl alcohol (32), sorbic acid (33), vanillin (3) and probably
eugenol (34). In addition it was reported 69 that phenyl vinyl ether, anisyl vinyl ether
and cyclohexylbenzoate were identified in the steam distillate. Whether these last
three compounds actually occur in propolis is debatable since they are sometimes
65

present in synthetic polymers. Cyclohexylbenzoate is sometimes used as a plasticizer,


and it is likely that the compounds were artefacts of the handling and separation
procedures.
Some interesting points emerge from the limited work that has been carried out
on the constituents of propolis. By far the largest group of compounds isolated are
flavonoid pigments, which are ubiquitous in the plant kingdom. It is not surprising
therefore that the same flavones have been isolated from different samples of propolis,
particularly since most represent the simplest flavone, flavanone or flavonol structures.
The series of flavonoids isolated from propolis correlates reasonably well with those
present in the plants from which honeybees collect propolis, but relatively few of the
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many flavonoids in buds of plants are detectable in propolis; for instance Betula
nigra contains 19 flavonoids in reasonable amounts and 10 in trace quantities 174 • It
has been suggested123 that some of the flavones are modified by an enzyme in the
honeybee. If so, it seems likely that any transformation must occur in the presence of
enzymes in the saliva of the bees during collection. The simple aromatic compounds
found in propolis, (1)-(6), also occur commonly in plants, and their presence in
propolis is not unexpected.
Rather more interesting is the presence of xanthorrhoeol (28), pterostilbene (27)
and 3,5-dimethoxybenzyl alcohol (29) in the sample of Western Australian propolis
investigated48 • Xanthorrhoeol (28) has been found previously in the grasstree
Xanthorrhoea pressii. Sakuranetin (22) has also been isolated from this plant, and
isosakuranetin from the related species X. australis 17 • It seems likely that these com-
pounds are obtained by the bees from the plants.
Although Eucalyptus species are known56 , 57 , 67 to contain a number of hydroxy-
and methoxy-stilbenes, pterostilbene (27) has not been reported as a constituent of
them. One explanation may be that bees transform naturally occurring stilbenes by
methylation or demethylation to pterostilbene. The presence of the benzyl alcohol
is also intriguing. Although alkyl resorcinols are found in Australian Grevillea species 27 ,
the substitution pattern may be taken as an indication that it is a degradation product
of pterostilbene.
It must be emphasized that the many compounds already isolated from propolis
represent only a small proportion of the total. Most came from the fraction of propolis
soluble in organic solvents, a few percent of the total. The large part of propolis not
readily soluble in water or organic solvents is likely to consist of natural polymeric
material. A proper delineation of the constituents will require much more investigation,
and they will doubtless vary with the plant source.
This raises the question of the value of simply determining the 'composition' of
propolis. If any credibility is to be given to even a small range of the pharmacological
activity attributed to propolis, satisfactory evidence of the presence of the compounds
responsible must be provided. So far a great deal of 'research' carried out must be
classed as pseudo-scientific investigation. More rigorous attempts must be made to
isolate the compounds involved, using appropriate bioassays to guide the separation
and purification processes. This assumes extra importance when considering pharma-
cologically active compounds present only in trace quantities.

Biological activity of the constituents of propolis


Although much work has been done to determine the spectrum of pharmacological
activity and the constituents of propolis, few attempts have yet been made to determine
66

if the compounds present in a particular sample are responsible, entirely or in part,


for its reported activity.
In 1960 Lavie 89 found that propolis showed bacteriostatic activity towards Bacillus
subtilis, Proteus vulgaris and B. alvei. The effect was less marked towards Salmonella
gallinarum, S. pullorum and S. dublin, and negligible towards different strains of E. coli.
Following fractionation of the propolis sample, galangin (15) and pinocembrin (21)
were isolated and found to be partly responsible for the activity 169 · 170 . In fact,
galangin at concentrations of 0 · 065 mg/ml inhibited B. subtilis for 12 h 169 . Higher
levels (0·080 mg/ml) inhibited B. alvei growth for 24 h and P. vulgaris for 12 h.
Twice this concentration was needed to inhibit S. gallinarum for 24 h. Although the
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concentration of galangin in the propolis sample could not be estimated, it appeared


that other compounds present may also contribute to the activity observed. Further
work 170 showed that another constituent, pinocembrin (21), inhibited B. subtilis for
24 h at 0 ·03 mg/ml. None of the other constituents identified (chrysin (7), tectro-
chrysin (8), isalpinin (16)) was active towards this micro-organism.
Recently in a detailed study of the constituents of propolis, Metzner et al. 100
employed bioautographic methods to detect compounds active against B. subtilis,
Staphylococcus aureus, E. coli and Candida albicans. The authors concluded that, of
the 26 or more compounds detectable in the extract of propolis, only pinobanksin-3-
acetate (26), pinocembrin (21), p-coumaric acid benzyl ester, and a caffeic acid ester,
showed significant antimycotic activity.
Of all the other constituents isolated from different propolis samples, only a few
have been tested for biological activity. Caffeic acid (5) shows the following: anti-
bacterial activity towards S. aureus, C. diphteriae, P. vulgaris; in vitro tuberculostatic
activity towards Mycobacterium tuberculosis; fungistatic activity against Helmintho-
sporium carbonum; inhibition of growth in Streptomyces scabies 33 •. This fits in with
the activity of propolis extract towards most of these organisms, as found by Linden-
felser92 and other workers 125.
Ferulic acid (6) shows antibacterial activity towards some gram-positive and gram-
negative bacteria, and it possibly also contributes to the bactericidal and bacteriostatic
activity of propolis 34 . Ferulic acid also has a marked astringent effect 142 and, in
common with organic acids which contain a benzylic double bond and aromatic
methoxyl group (e.g. 3,4-dimethoxycinnamic acid), a significant choleretic activity
(increasing secretion of bile by the liver) similar to that of sodium deoxycholate 146 .
Pinocembrin (21) has considerable antimicrobial activity towards Alternalia
fungi 103 . Sakuranetin (22) is active against wood-rotting fungi 8.
A number offiavones isolated from propolis have been shown148 to have papaverine-
like spasmolytic activity, in tests carried out on the small intestine of mice in vitro,
using acetylcholine to bring about contraction. Compared to papaverine hydro-
chloride (100 %), the activities of the fiavones were as follows: pectolinarigenin (18),
28; quercetin (11), 262; kaempferide (12), 246. The fiavanones sakuranetin and
isosakuranetin were found to have negligible activity at the concentrations used in
the tests, which were limited by the insolubility of the compounds.
Stilbenes are known to possess fungicidal and fungistatic properties towards wood-
rotting fungi 83 • 94 • 137 , and it is believed that the presence of these compounds in
certain hardwoods provides some protection. The antifungal activity of pterostilbene
(27) has been noted 1. It has been reported 144 that pterostilbene has been used in the
treatment of diabetes (probably in folk medicine) but no confirmation of this has
been found.
67

The major constituents of propolis from most sources are flavones, flavonols and
flavanones. This is particularly so for propolis collected in eastern Europe, where most
of the work on the pharmacological activity of propolis has been carried out. Whether
these compounds are directly or indirectly responsible for some of the observed
effects remains an open question. However, since propolis appears to be widely used
in certain countries, it is useful to consider the known pharmacological properties of
these ubiquitous compounds.
Over the last thirty years much effort has been expended in determining the
physiological and therapeutic effects of the flavonoid pigments. Several early contra-
dictory results led to a great deal of discussion and lack of interest, but in the last few
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years a number of workers have made some effort to re-examine the therapeutic
properties of flavonoid compounds. Some of the more recent results are summarized
here. Comprehensive reviews are available 20 ' 47 on the research into the physiological
action, pharmacodynamics and therapeutic uses of flavonoids up to 1967.
It is now generally accepted that the vast majority of flavonoids are innocuous in
the human diet 152 • Powers 124 studied the antibiotic effect of more than 20 flavonoids
on strains of Salmonella, Staphylococcus aureus, Proteus vulgaris, E. coli and other
organisms. No compound was devoid of inhibitory activity towards one or more
of the ten types of bacteria studied. Luteolin (5,7,3',4'-tetrahydroxyflavone) and
apigenin (5,7,4'-trihydroxyflavone) 32 had a marked protective effect on induced
gastric ulcers in guinea-pig and rat. The 3'-methyl ether of apigenin (acacetin) was
ineffective, suggesting that there is a requirement for free hydroxyl(s) group(s) in
the B-ring. Acacetin on the other hand is reported to decrease formalin-induced
inflammation, and to reduce capillary fragility, when given orally (25-100 mgfkg) to
mice 78 • The 3',4'-dimethyl ether of luteolin is reported to have hypocholeretic and
spasmolytic properties 88 •
Quercetin (11) has been shown to enhance in vitro the histamine-fixing capacity of
several protein fractions (particularly y-globulins) 45 •
A number of flavonoid compounds exert an anti-inflammatory effect on joints, skin
and mucous membranes. It has been suggested that some flavonoids stabilize con-
nective tissue and vessels, protect vitamin C against oxidation, and decrease the
activity of mucopolysaccharide-destroying enzymes 109 •
Eriodictyol (5,7 ,3',4'-tetrahydroxyfiavanone) administered orally or parenterally
to rats prevented the appearance of acute pulmonary insufficiency, which was induced
by several procedures and which normally results from respiratory burns, thoracic
and non-thoracic trauma and shock9 •
In general flavonoids with 3'4'-dihydroxylation exert a beneficial effect on the
capillaries by (a) chelating metals thus sparing ascorbic acid from oxidation, (b) pro-
longing adrenaline action by inhibiting 0-methyl transferase, (c) inhibiting hyaluroni-
dase and histamine, and (d) counteracting the effect of anticoagulants. If these hydroxyl
groups are lacking, or are partially or totally methylated, the effect is lessened. Al-
though most flavonoids isolated from propolis lack the 3',4'-dihydroxylation pattern,
it is interesting to note that one of the major pathways of metabolism of flavonoids
involves hydroxylation at position 3' as well as demethylation of the methyl ether
group at position 4'.
Recent evidence 129 , 130 shows that polymethoxylated flavonoid compounds may
significantly inhibit erythrocyte aggregation in vitro and in vivo. This is of some
significance, since diseases and injuries are accompanied by block cell aggregation.
If this is severe and prolonged, organ damage and enlargement can result.
68
Results obtained with certain ftavones suggest that these compounds may be used
clinically131 • The beneficial effects of ftavonoids against abnormal capillary permea-
bility and fragility may also be explained if they act by reducing blood cell aggregation
and improving microcirculation.
It has been suggested that apart from acting as antipathogenic agents, ftavonoids
may potentiate enzymes which detoxify hydrocarbons, exhibit anti-inflammatory
activity, exert an anti-adhesive action on blood cells, and show antithrombogenic
activity 129 • 133 • Some ftavonoids appear to have antiviral effects in animals. Cells
treated with quercetin exhibit decreased sensitivity to Herpevirus hominis 11 • Despite
these and other reports, inconsistencies are still apparent regarding the beneficial
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action of flavonoids. Particularly doubtful is their clinical effect when administered


orally49 • It has been argued, however, that the beneficial effects are often only apparent
after prolonged treatment.
No specific studies have been carried out to determine the activity of other flavonoid
constituents of propolis.

Pharmacological activity attributed to propolis


Reports on the pharmacological use of propolis appeared in the early 1900s. A pre-
paration of propolis and vaseline, 'propolisin vasogen', was known to have antibacterial
properties 101 and was used as a medication during the Boer war 169 • It aids the healing
of wounds and tissue regeneration 26 , and its use in surgery has been reported 134 •
Other reports refer to the use of propolis for inhalations, treatment of rheumatism,
gout, and as a non-irritant dressing for wounds 154 • 155 • Recent compilations on
medications (e.g. reference 98) list yellow beeswax as an additive for the preparations
of styptic creams and ointments. The yellow colour imparted to beeswax is known to
be due to the presence of some constituents of propolis 12 · 70 • An aseptic surgical wax,
used to prevent haemorrhage during cranial surgery, requires the addition of 7 parts
of yellow beeswax9 B.
Recently a commercial propolis preparation Mylit has been developed 13 and used
in clinical treatment of mycotic infections and eczema. Addition of 2% of propolis
is claimed to increase and prolong the antibacterial activity of ointments 82 • Other
reports refer to the use of propolis as a drug 86 , and in folk medicine 118 • The clinical
usefulness of propolis preparations has been evaluated 30 • 68 , and another report gives
the results of therapy with propolis ointments 156 •
In the following sections the results of recent investigations of the pharmacological
activity attributed to propolis are summarized. A number of reports cited have not
been available to the author.

Antibacterial and antifungal activity


The first systematic investigation of the antibacterial activity of propolis on a range
of bacteria appears to be that of Kivalkina79 , who found that fused propolis showed
bacteriostatic activity against Streptococcus aureus, the typhoid bacillus and other
bacteria. Several other reports followed (Table 3), from studies of only crude extracts
of propolis, from various sources, obtained by different extraction procedures. This
perhaps accounts for some of the apparently contradictory entries, e.g. Streptococcus
and Escherichia. In general the results should be viewed with some caution, and
considered as at best indicative; the lack of comparative studies with accepted efficient
antibiotics also detracts from their value.
69

In a detailed study of the antimicrobial activity of propolis, Lindenfelser92 tested


15 samples collected from different parts of the USA at various seasons. Extracts
showed strong inhibitory activity in vitro in 25 of the 39 bacterial species tested.
Bacillus larvae was most strongly inhibited, and 24 others were sensitive including
gram-positive cocci and acid-fast rods; 7 gram-negative rods were resistant. Of 39
fungus species, 20 were inhibited. Resistance was shown by 2 yeasts. The in vitro
sensitivity of Trichophyton rubrum to propolis provides some support for the claim of
the effectiveness of propolis ointment in the treatment of a skin infection by this
organism 22 . Further, the activity against acid-fast bacteria is of interest in view of the
claim that propolis can be used for the treatment of tuberculosis patients 75 • 76 .
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In another experiment, Lindenfelser93 found that an alcohol extract of propolis


controlled American foul brood disease in honeybees. The extract was fed directly,
or mixed in dilute honey, or it was sprayed as an aqueous or saline solution on to the
combs. At 500 1-'g/ml the disease was controlled only during treatment, but higher
concentrations destroyed healthy larvae and caused deformities. Sulphathiazole at
132 1-'g/ml eliminated the infection. Propolis at 1 · 25-5 mgjml showed bactericidal
effect towards 20 Staphylococcus, 10 Streptococcus and 10 E. coli cultures isolated from
the sputum of children with chronic pneumonia 29 .
Extracts of propolis have been shown to potentiate the effect of certain anti-
biotics29· 81 • 82 · 175 . The action of biomycin, tetracycline, neomycin, polymyxin,
penicillin and streptomycin towards S. aureus and E. coli was increased by the addition
of propolis to the nutrient medium 81 . In some cases the bacteriostatic effect was
increased 10-100 fold. Similar synergistic effects of a combination of propolis with
penicillin, streptomycin or furagin were also observed toward Staphylococcus strains 29 .
The most effective combination against E. coli was a mixture of propolis and furagin 29 •
Propolis did not affect the antistaphylococcal activity of oleandomycin 81 .
A water-soluble preparation obtained from propolis showed significant bacterio-
static effect on acid-resistant saprophyte B 5 (organism living on dead matter) at
0 · 001% levels 158 . The treatment of candidiasis in the infant with propolis in an
alcohol-water mixture has been reported 160 . Other papers dealing with aspects of the
antibiotic activity of propolis have appeared22, 31, 46, ss, 89, 91, 117, 168.
Still others deal with the use of propolis in the treatment of vaginitis and cervicitis 176,
of suppuration skin diseases caused by antibiotic resistant strains of Staphylococcus 112 ,
and of the alteration of microfiora following ear surgery 145. One report points out
that storage for 3-4 years at 0-4° or room temperature does not reduce the antibacterial
activity of the propolis extract16 2.
Despite the somewhat arbitrary nature of most of these experiments, the results
indicate that propolis possesses antibacterial activity. It is unfortunate that even now
some experiments are carried out on crude extracts.

Anaesthetic action of propolis


A 4% alcohol extract of propolis, diluted with water to a concentration of 0 · 25 %,
was reported to produce complete anaesthesia of the rabbit cornea 126 • 127 . The effect
lasted for an hour, being 3 times that observed for cocaine and 52 times that of
procaine. A synergistic effect of propolis and procaine was also observed. A 0 · 03%
solution (water and alcohol) added to a 0 · 25% solution of procaine was 14 times more
effective than procaine alone. In an experiment on conduction anaesthesia in frogs,
a 1% solution of propolis was found to be 4 times as effective as procaine 126. From
this it was concluded that the propolis extract was essentially a surface anaesthetic
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-..1
TABLE 3. Antibacterial and antifungal activity of propolis extracts. 0

Organism Origin of propolis Type of extract Activity Remarks Ref.


--
Staphylococcus
aureus USSR alcohol - enhances effect of some antibiotics
towards this organism 175
Oxford strain USSR 1:10 alcohol - 38
Oxford strain Romania - 38
--
Streptococcus
faecalis USSR 1 :10 alcohol + 38
faecal is Romania + 38
faecalis Poland alcohol - propolis tested came from various
sources 139

Staphylococcal and USSR + various strains (c. 40) isolated 29,


Streptococcal species from sputum of children with also
chronic pneumonia 37
Corynebacterium Poland alcohol + partly sensitive; only 1 sample 139
in 4 active

Escherichia
coli 026 USSR 1 :10 alcohol + 38
coli 0111 USSR 1:10 alcohol + 38
coli USSR 1 :10 alcohol + 38
coli USSR alcohol - enhances effect of some anti- 175
biotics against this organism
coli France alcohol - 89,90
coli USSR + 29
-
Klebsiella
ozaenae alcohol + very sensitive 139
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TABLE 3 continued
Organism Origin of propolis Type of extract Activity Remarks Ref.
Salmonella
choleraesuis USSR 1:10 alcohol + 38
enteritidis USSR 1 :10 alcohol + 38
typhosa USSR 1 :10 alcohol + 38
dublin France + 89,90
gallinarum France + 89,90
pullorum France + 89,90
Shigella
dysenteriae USSR 1 :10 alcohol + 38
dysenteriae Romania 1 :10 alcohol + 38
sonnei USSR 1 :10 alcohol + 38
Proteus
vulgaris France + 89,90
Mycobacterium Poland alcohol + saline extract of propolis not 139
active
Bacillus
alvei France + 89,90
larvae USA 1 :20 alcohol + 15 samples from different areas 92
mesentericus USSR 1:10 alcohol - 38
subtilis (Caron) France + activity partly due to galangin 89,90
and pinocembrin
Microsporum
audoinii Czechoslovakia + 36
canis 70% alcohol + 120
cookei Czechoslovakia + 36
distortum Czechoslovakia + 36
ferrugineum 70% alcohol + used as a tincture 23
gypseum Czechoslovakia + 36
....-.J
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~
TABLE 3 continued N

Organism Origin of propolis Type of extract Activity Remarks Ref.


---
Trichophyton
ferrugineum 70% alcohol + used as a tincture 23
schoenleini Czechoslovakia + 36
schoenleini 70% alcohol + 120
tonsurans 70% alcohol + 120
tonsurans Czechoslovakia + 36
verrucosum Czechoslovakia + 36
verrucosum 70% alcohol -:- used as a tincture 23
6 other strains Czechoslovakia + 36

Candida Poland alcohol + partially sensitive 139


9 strains Czechoslovakia + 35
--
Torulopsis
4 strains Czechoslovakia + 35
--
Trichosporon
infestans Czechoslovakia + 35
73

with negligible penetrating power, and could ber ecommended for use in stomatological
practice 126 • It was suggested that the active principle(s) came from its essential oil 127
and was soluble in ether and alcohol.
From another study159 it was concluded that an aqueous extract of propolis is a
good local anaesthetic, with a peripheral action on the mucous membrane of the eye
greater than that of cocaine, and an infiltrative action equal to that of procaine. These
results suggest that, in these preparations at least, the active principle(s) must be
partly water-soluble. A preparation made from the 70% alcoholic extract of propolis
(40 g in 100 ml of 70% alcohol) was reported to be 3 · 5 times as strong as cocaine as
an anaesthetic 106 • This was introduced in dental practice in the USSR in 1953.
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Bulgarian workers found 161 that although an aqueous (1 :1) and an aqueous alcoholic
(30 %) extract of propolis showed some anaesthetic action, the effect was slower and
weaker than that of a 5% procaine solution. Nevertheless, this extract was recom-
mended as suitable for cutaneous infiltration. A 50% alcoholic extract of propolis
has been used in the treatment of chronic otitis and was found to exert a feeble
anaesthetic action lasting approximately 10 min4 •
The discrepancies between the observations described above may be rationalized
best by considering that the propolis used came from different sources and that
slightly different extraction procedures were used. In the absence of more detailed
information on the criteria chosen to establish the anaesthetic action of these extracts,
no definite conclusions can be drawn on these reported actions.

Use of propolis in dermatology


The effect of propolis preparations on wound healing and tissue regeneration have
long been recognized. This is consistent with the known antibiotic, styptic and
astringent effects attributed to propolis. A number of reports on the use of propolis
in treating various dermatological problems have appeared in recent years. Application
of an alcoholic solution of propolis and sulphopen (potassium penicillin G; benzene-
sulphonamide hydrochloride; sulphonilamide) and framykoin (neomycin plus zinc
bacitracin) is reported to promote the tissue regeneration process 151 • The effect of
propolis extract on 38 skin fungi has already been listed (Table 3). Other reports
comment on the efficacy of propolis treatment for second degree burns 77 , neuro-
dermatitis, microbial eczemas and other dermatological problems 40 • 105 • 113• Propolis
can be applied as a pomade (30 %) 77 or as an alcoholic solution105 • For the treatment of
dermatological diseases (particularly ulcus cruris) a preparation consisting of Peru
balsam, boric acid, arnica extract, acriflavine hydrochloride and propolis has been
used167 •

Other pharmacological activity


Injection of a propolis extract (1 · 5 parts of pro polis to 10 of 95% alcohol) diluted with
water (1 :10) raised the liver temperature of rabbits by 0·2 to 0·5°C. Comparative
studies with atropine and adrenaline showed that propolis stimulates the receptors
of mucous membranes, raising the local temperatures in stomach and liver 119, although
to a lesser extent than observed for the other two drugs.
Propolis extracts (30% alcoholic solution) have been used in the treatment of
ulcers 54• 95 • Some evidence of their beneficial effect on experimentally induced ulcers
in laboratory animals has been reported7 • Rats which had ulcers induced by arsenic
pentoxide and caffeine treatment were divided into 4 groups. Seven days after ulcer
74

development the 3 experimental groups were fed 1 ml of propolis extract, 75 mg of


methyl uracil and 1 ml of ethanol per kg body weight, respectively. The control
group received 2 ml water/kg. The animals treated with propolis and methyl uracil
gained weight as intoxication diminished, whereas the control group showed subacute
arsenic poisoning. The average areas of stomach ulceration for the rats treated with
propolis and methyl uracil were similar and were considerably less than that observed
for the control group.
Aqueous extracts of propolis are reported to have a strong effect on the autonomic
nervous system, with peripheral action on nervous transmission. The normal tension
and peristaltic action of isolated intestine are altered by this extract, which also
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produces vasodilation of the blood vessels 159 .


The use of propolis in the treatment of ear and respiratory tract infections and
general disorders has been reported4 • 84 · ns. An alcoholic extract of propolis (50%)
was used in the treatment of patients with chronic suppurative otitis 4 •
The effect of propolis solutions on the growth of specific tumour cells has also been
reported41 • 164 . A 5% alcoholic solution of propolis has been shown to inhibit the
proliferation of an influenza virus, when administered intranasally or as an aerosol
to dogs 2 h prior to infection with the virus. This solution had no effect if administered
after injection 147 .
It has been claimed that propolis can act as an unspecific agent which stimulates
immunogenesis. Propolis enhanced the agglutinating and precipitating titre of
guinea-pigs immunized with full antigen 80 . The adjuvant effect of propolis on the
formation of serum agglutinins has been studied in calves immunized against para-
typhoid. Addition of propolis to the vaccine stimulates the synthesis both of N-
agglutinins and 0-agglutinins 153 . The preparation of solutions of propolis for injections
and for ophthalmic use 1n, and the result of treatment of chronic pharyngitis with
propolis, have been reported 85 .
An alcoholic extract of propolis resin mixed with toothpaste and with a mouth-wash
preparation has been claimed to improve their antiseptic properties 72 ; in another
patent 1-2% of a 10% alcoholic solution of propolis is added to toothpaste97 . In a
patent for a styptic, propolis resin (1-3 parts) is dissolved in ethanol (96% : 10-30
parts), and the solution cooled to 0° and filtered. The waxy filtrate diluted with alcohol
is reported to have strong antiseptic, astringent and styptic properties 71 •
A preparation for treating tooth and gingival diseases is prepared by mixing propolis
tincture with arnica tincture, chamomile extract and o-cresyl salicylate 166 . Propolis
has been added to glycerol and Freons for a preparation used in treating diseases of
the mucosa of the mouth 107 . A biologically active polyphenol preparation from propolis
can be obtained by extraction with organic solvents 157 . Several pharmaceutical pre-
parations have been described in eastern European countries. Mylit is a propolis
containing medicament which has apparently been tested clinically13, 100.

Toxicity of propolis
Relatively few studies have been carried out to determine whether propolis and
extracts from it are toxic, although it is generally regarded as being harmless 71 •77, 12 6,159.
An ether solution of propolis was not toxic to white mice at doses of 0 · 35 mgjg
body weight 126 . The LD 50 after 19 hours for both ether and alcohol extract was
0 · 7 mgjg body weight. The cause of death was apparently paralysis of the respiratory
centre. In comparison, procaine in similar doses killed 60% of the experimental
75

animals over the same period. Cats tolerated 0 ·I mgjg body weight of the extract
administered subcutaneously1 26.
Aqueous and alcoholic extracts of propolis did not show irritation of tissues 71 • 159
and did not appear to be toxic 159. Cases of hypersensitivity towards propolis have been
reported24, 73, 98, 136 • 173. Cases of dermatitis are few, however, and recent surveys
indicate that perhaps only 1 in 2000 beekeepers may be sensitive 24 . This is not in-
consistent with the general tendency to use propolis preparations to treat dermatitis
and superficial wounds. The allergens in propolis studied have been derived mainly
from poplars 24 • 98 • 136, but the allergic reaction does not seem to be caused by any of
the cinnamic acid derivatives 24 (see Constituents). In cases of allergy to propolis,
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application of silicone barrier creams prior to exposure is recommended 24 • 140 .


A recent report describes a secondary effect of propolis (probably when preparations
are used in dentistry or to treat mouth infections), which involved a softening of the
gums and a slight loosening of the teeth96 .
In view of the recommended topical use of propolis in creams, ointments and
solutions intended to have an anti-inflammatory, bactericidal or anaesthetic effect,
the sensitivity of some people towards propolis or its constituents should be kept in
mind 173.
More important are the possible effects on people who use propolis extract (normally
a 70% alcohol preparation) over a long period, to alleviate ulcer or respiratory prob-
lems. The known constituents of this fraction, for a number of propolis samples
examined, are flavone substances (see Constituents) which are regarded as nontoxic.
However, the presence of small quantities of toxic compounds, or compounds not
readily metabolized, could lead to problems in the long term.
Since the chemical composition of propolis is largely unknown, and variable, the
oral intake of propolis extracts is not to be recommended in the absence of more
detailed toxicity studies.

Phytoinhibitory properties
Several reports have referred to the phytoinhibitory and phytotoxic actiVIty of
propolis extracts. Potato tubers kept in a hive did not sprout50, and after storage in the
hive for an extended period they suffered permanent inhibition51 . An aqueous extract
of propolis was shown to be responsible for inhibiting germination, but the active
agent was not galangin, a known component of the propolis used, which shows anti-
bacterial activity. Growth of lettuce seedling and rice grains was also inhibited50• 52 .
Alcoholic extracts of Russian propolis were found to inhibit the germination of
Cannabis sativa seeds 38 · 39 .

Commercial uses of propolis


This section includes known commercial uses and patents for the use of propolis or
its preparations. Recently there has been an increased demand for propolis, and this
appears to be correlated with an increasing number of patent applications. A colony
of bees collects 150-200 g propolis in a year, and some races collect much less. Rather
little propolis is available, and the collection of propolis presents problems to the
beekeeper. There are few descriptions of suitable methods for harvesting it from
hives, and for obtaining a product free from beeswax. A bibliography of the methods
developed is available 171 .
76

Problems of standardizing propolis samples have been discussed 121 . It may be


significant that a Russian patent has been taken on a method to detect adulteration of
propolis 163 . This is based on the discoloration time ofO ·I-N potassium permanganate
by propolis, and is likely to be nonspecific. A possible use of propolis is suggested by
the observation that a 0 · 05% aqueous-alcoholic emulsion of propolis as a supplement
to the basal diet of chickens led to weight gains increased by up to 20% 6. Propolis
has been reported to be an effective antioxidant 16 , 138, and its use as a preservative
for stored horse fat has been noted5.
Solutions containing 0 · 3-2 · 5% of propolis have been used as toilet lotions 116 .
A 10% oil solution of propolis has been added to skin cream preparations 114 .
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Propolis has been used for a long time in polishes and varnishes, and may have
been used by the ancient Egyptians for embalming purposes 18 . References to the
use of propolis in the preparation of varnishes are available 171 , and it also has been
especially used in violin varnish73•. The suggestion 15 that the special qualities of
Stradivarius violins may be partly due to the type of propolis used now seems un-
likely73".
Propolis is reported to improve the adhesion to vegetable fibres of a composition
containing resin, beeswax, castor oil, polyethylene-phenylsiloxane lacquer, non-
drying resin and organic solvents 2.

Conclusion
An attempt has been made in this review to collect most of the information about
propolis which has been published over the last seventy years. Many of the claims
made about the pharmacological action of propolis have not been well confirmed,
but it nevertheless seems likely that propolis will be used increasingly for commercial
purposes. It is abundantly clear that it will have to be studied much more before it
can properly be considered for therapeutic purposes; because its constitution is
largely unknown, propolis should not be recommended in medicines. As with any
other pharmaceutical preparation, those who make claims about its beneficial effect
must provide sound supporting evidence. A preparation must also be examined for
side effects. Since a considerable number of people seem to be using propolis and
preparations of it, further research into its pharmacological properties is justified, and
it is hoped that this review will provide some basis for such investigations.
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51. GoNNET, M. (1968a) Proprietes phytoinhibitrices de la colonie d'abeilles (Apis mellifica


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80

76. KARIMOVA, Z. KH.; RODIONOVA, E. I. (1963) [Lung tuberculosis and propo!is.)


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Beekeep. Congr. Summ. : 136 In Russian B, AA666/70


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81

100. METZNER, J.; BEKEMEIER, H.; SCHNEIDEWIND, E.; SCHWAIBERGER, R. (1975) Bio-
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