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72: 5–10 (2015) 16–22 | www.jurnalteknologi.utm.my | eISSN 2180–3722 |
Jurnal
Teknologi
Full Paper
SKIN TEST REACTIVITY TO BEE HIVE
PRODUCTS (HONEY BEES, HONEY, ROYAL
JELLY AND POLLEN)
Mai Shihah Abdullaha*, Nasuruddin Abdullahb
aDepartment of Agricultural Science, Faculty of Technical
and Vocational Education, Sultan Idris Education
University, 35900 Tanjong Malim, Perak, Malaysia
bKulliyah of Medicine, International Islamic University
Malaysia, Kuantan Campus, Jalan Sultan Ahmad Shah,
Bandar Indera Mahkota, 25200 Kuantan, Pahang, Malaysia
Article history
Received
2 December 2015
Received in revised form
2 January 2016
Accepted
15 April 2016
*Corresponding author
mai.shihah@fptv.upsi.edu.my
Abstract
Bee hive products such as honey bees, honey, royal jelly and pollen are widely consumed as a health supplement. There
has been several cases of allergic reactions to bee hive products reported worldwide. Consumption of bee hive products
is common among Malaysians, but the degree of its sensitization is not known. The aim of this study is to determine the
prevalence of skin test reactivity to Apis mellifera, domesticated locally and the bee hive products such as honey bees,
honey, royal jelly and pollen among a group of volunteers. Four types of honey collected from different locations with
different plant sources; one sample of imported honey from Australia, one sample of royal jelly, four different sources of
bee pollen, and honey bee derivatives were used to prepare allergen extracts for skin testing. 2522 volunteers were skin
tested to these allergen extracts. 271 (10.75%) of the subjects had a positive skin prick test result to at least one honey bee
derivative or bee hive product allergen. Individuals with skin test positivity to honey bee are most likely to be sensitized to
bee pollen followed by honey and royal jelly. Skin test reactivity to honey bee and bee hive products is prevailed to be
high in Malaysia. This study has proven that bee hive products sensitization individuals are mostly to be also sensitized to
honey bees. Therefore, is recommended these allergens to be included in the skin prick panel.
Keywords: Allergen; bee hive products; honey bee derivatives; prevalence
Abstrak
Produk haif lebah seperti lebah, madu, jeli raja dan debunga digunakan secara meluas sebagai makanan tambahan
kesihatan. Terdapat beberapa kes reaksi alahan terhadap produk haif lebah dilaporkan di seluruh dunia. Pengambilan
produk haif lebah adalah suatu kelaziman dalam kalangan rakyat Malaysia, tetapi tahap kesensitifannya tidak diketahui.
Tujuan kajian ini adalah untuk menentukan prevalens kereaktifan ujian kulit terhadap Apis mellifera, yang diternak dalam
persekitaran tempatan dan produk haif lebah seperti lebah, madu, jeli raja dan debunga dalam kalangan sekumpulan
sukarelawan. Empat jenis madu yang dikumpul daripada lokasi yang berbeza dengan sumber tumbuh-tumbuhan yang
berbeza; satu sampel madu yang diimport dari Australia, satu sampel jeli raja, empat sumber debunga lebah, dan
derivatif lebah madu telah digunakan untuk menyediakan ekstrak alergen bagi ujian kulit. 2522 sukarelawan kulit diuji
dengan ekstrak alergen tersebut. 271 (10.75%) daripada subjek menunjukkan keputusan ujian cucuk kulit yang positif
terhadap sekurang-kurangnya satu alergen derivatif atau produk haif lebah. Individu yang mempunyai ujian kulit yang
positif kepada lebah madu adalah paling berkemungkinan menunjukkan sensitiviti kepada debunga diikuti oleh madu
dan jeli raja. Kereaktifan ujian kulit kepada lebah madu dan produk haif lebah menunjukkan prevalens yang tinggi di
Malaysia. Kajian ini telah membuktikan bahawa kesensitifan individu terhadap produk haif lebah berkemungkinannya
turut sensitif kepada lebah madu. Justeru, adalah disyorkan alergen-alergen ini dimasukkan ke dalam panel cucuk kulit.
Kata kunci: Alergen; produk haif lebah; derivatif lebah madu; prevalen
© 2016 Penerbit UTM Press. All rights reserved
1.0 INTRODUCTION
Through the ages, various medicinal properties have
been attributed to honey, royal jelly, bee pollen and
honey bee venom. These bee hive products; i.e.
honey [1-6], pollen [7-8], royal jelly [9-10], propolis [11]
and honey bee venom [12-14] are widely consumed
either as dietary supplements or skin applications. The
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prevalence of allergy to these products among
Malaysian is not known. However, there are a number
of reports of allergic reactions ranging from mild
symptoms to anaphylaxis from bee hive products, i.e.
honey [15-17], royal jelly [18-21], bee pollen [22-23],
propolis [23-5], honey bee[26-28], and honey bee
venom[29-31] as described in the literatures.
Honey is a mixture of flower nectar, pollens and
components from honey bees, the latter including
enzyme-containing secretions from the salivary and
pharyngeal glands. Recent researchers [32-34]
postulated that allergic sensitization to honey is
related to proteins either from pollen or honey bee
origin.
Royal jelly is a secretion of the hypopharyngeal
gland or worker honey bees. About 50% of its dry
weight consists of proteins; other components are free
amino acids, fatty acids, sugars, vitamins and some
minerals. Bee pollen is flower pollen that honey bees
collect for food. It is a popular health supplement that
apparently boosts the immune system. Amongst the
many therapeutic claims include its use in the
treatment of allergies, although pollen itself is a
common aeroallergen.
Ultimately, bee hive products were well
documented with large number of allergens that
come from the bee derivatives (saliva, body, venom),
pollen (freshly foraged and comb), honey (comb and
bottled), royal jelly, propolis and wax. Both positive
and negative impacts, between health boosters and
allergy sensitization; the consumption of bee hive
products could be determined by allergy
management [35].
1.1 Objectives
Consumption of honey bee by products such as
honey, royal jelly and bee pollen among Malaysians is
high, but the degree of sensitization is not known. The
aim of this study is to determine the prevalence and
pattern of skin test reactivity to these products
amongst a group of volunteers.
2.0 MATERIALS AND METHODS
2.1 Source and Allergen Extracts Preparations
Four types of local honey were collected from various
local apiaries. Three of these were unifloral honey
(Hevea brasiliensis, Cocos nucifera and Melalueca
leucadendron) and one sample was collected
directly from the comb. One source of imported
honey from Australia and royal jelly were also included
in the study. Four different sources of bee pollen
(collected at the entrance of the hive, comb pollen,
and coconut pollen) were also collected from the
local apiaries. Dried, commercial and imported pollen
was also included. Apis mellifera honey bees were
collected from an apiary in Tanjong Piai. Whole honey
bee heads and nectar crops were used for allergen
preparation.
Ten of honey was dissolved in 10 ml of distill water
and centrifuged. The supernatant was dialyzed over
two days against distill water. One gram of royal jelly
was dissolved in 10 ml of distilled water. Five grams of
pollen were added to 10 ml of distilled water. 30
honey bee heads and nectar crop from 30 honey
bees were homogenized in 10 ml of distilled water. All
the above were subjected to an overnight extraction
at 4oC. The extracts were filtered and lyophilized.
Extracts were reconstituted with Coca‟s solution
before use.
2.2 Subjects
2523 volunteers from Universiti Pendidikan Sultan Idris,
Perak were involved in this study. The subjects were
advised not to take antihistamine two weeks prior to
testing. A detailed history of allergen was obtained
from each subject. Subjects were grouped into
symptomatic atopic (with allergy symptoms) and
familial atopic (with family members positive to allergy
based on skin prick testing) allergies.
2.3 Skin Prick Test
The epicutaneous test was conducted on the volar
surface of the forearm using sterile lancets. The
subjects were skin tested with all the above extracts
and to a range of food and inhalational allergens.
Histamine (5mg/ml) and Coca‟s solution were used as
positive and negative control respectively. Wheal size
was read and recorded 15 minutes after testing. A
wheal size of 3 mm or more than the negative control
is regarded as positive.
2.4 Statistical Analysis
Data entry and statistical analysis were conducted
using the software SPSS version 17. The risk was
calculated by using Odd Ratio (OD) with Confidence
Internal (CI) at 95%. The subjects‟ skin prick test
positivity to bee hive products were grouped into
honey, pollen, royal jelly and honey bees sensitizations.
Other groups were food and aeroallergens.
3.0 RESULTS
Out of the 2523 subjects in the general population,
1384 (54.86%) of the subjects had a familial atopic
history of allergy and 1139 (45.14%) with symptomatic
atopic history. Skin prick test showed that the
sensitization prevalence in the population was 37.9%.
271 (10.75%) had a positive skin test to at least one of
the prepared bee hive allergens. Prevalence among
the general population showed that sensitization to
honey bee derivatives were the highest (8.48%),
followed by bee pollen (3.17%), royal jelly (2.38%), and
honey (2.10%).
This study also prevailed high prevalence of bee
hive products sensitization associated to inhalant
sensitization that amounted to 72.3% (196 subjects),
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and to food sensitization of 61.3% (166 subjects).
Among the individuals with bee hive sensitizations, 64
(23.62%) were also honey bee by products consumers.
The risk for them to be also associated with food
sensitization was the lowest (OR=1.75, CI 95%: 1.474 –
2.082), followed by inhalant sensitization (OR = 1.831,
CI 95%: 1.600 – 2.094). They were of a higher risk to be
associated to the rest of bee hive sensitizations by OR
= 2.719 (CI 95%: 2.082 – 3.550).
The prevalence of 271 subjects with at least one bee
hive products sensitization is as shown in Table 1. Of
the subjects with positive SPT to bee hive products, 35
(12.4%) were also sensitized to at least one of the food
allergens, 69 (24.5%) to any one of the inhalant
allergens and 137 (48.6%) to all the three groups of
allergens. It was also revealed that 10 (3.69%) were
sensitized to all bee hive products. Interestingly, 57
(21.03%) of those whom were sensitized to other bee
hive products, but not to the honey bees. 23 (8.49%)
were sensitized to any three of bee hive products,
while 60 (22.14%) to any two and 178 (65.68%) were
only sensitized to one of the honey bees by products.
Table 1 Skin test reactivity prevalence to bee hive products among the 271 subjects
Allergen
No. of Subjects with Positive Skin Prick Test
Percentage
Royal jelly (N=60)
60
22.14
Honey (N=53)
19.56
H. brasiliensis
13
4.8
C. nucifera
16
5.9
M. leucadendron
16
5.9
Comb honey
32
11.8
Imported honey (Australia)
8
3.0
Bee pollen (N=80)
29.52
Pollen collected at the bee hive entrance
28
10.3
Comb Pollen
20
7.4
Commercial, dried pollen
48
17.7
Coconut pollen
5
1.8
Honey bee derivatives (N=214)
78.97
Bee head
179
66.1
Nectar crop
107
39.5
3.1 Skin Test Reactivity Pattern to 214 Subjects
with Positive Skin Prick Test to Honey Bee
Individuals with skin test positivity to honey bee
derivatives were most likely to be sensitized to bee
pollen (23.83%), followed by honey (20.09%) and
the least to royal jelly (15.42%). 129 (60.28%)
individuals were sensitized to honey bee
derivatives only. The positive reactivity among the
honey bee towards other bee hive products is as
shown in Figure 1. Positive associations were not
found between positive honey bee derivatives
sensitization and symptomatic atopic (OR = 1.12,
95% CI .92 to 1.35) or to familial atopic (OR = 1.02,
95% CI .87 to 1.19).
Honey
group
Pollen
group
Royal jelly
group
Individuals positive to
honey bee
derivatives
(N= 214)
Honey bee
derivatives only
129 (60.28%)
16 (7.48%)
14
(6.54%)
23
(9.54%)
5
(2.33%)
11
(4.56%)
10
(4.67%)
7
(3.27%)
Figure1 Prevalence of subjects with honey bee sensitization
associated to other bee hive products sensitizations
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3.2 Skin Test Reactivity Pattern to 53 Subjects with
Positive Skin Prick Test to Honey
As for those with honey sensitization, they were of the
highest risk to honey bee derivatives (79.24%), bee
pollen (45.28%) and royal jelly (37.74%). 4 (7.55%)
were only sensitized to honey. The reactivity among
the honey positivity towards honey bee and other
bee hive products is as shown in Figure 2. The risk for
subjects sensitized to honey to be also sensitized to
honey bee derivatives was insignificant, OR=1.021
(.488 – 2.139), 95% CI). Among those who were and
without the honey sensitization, the risk is insignificant
with OR = 1.004 (.870 – 1.159, 95% CI) and OR = .983
(.542 - 1.785, 95% CI) respectively. Positive
associations were not found between positive honey
sensitization and familial atopic (OR = 1.08, 95% CI .86
to 1.35) but to symptomatic atopic (OR = 4.62, 95% CI
1.51 to 14.18).
3.3 Skin Test Reactivity Pattern to 60 Subjects with
Positive Skin Prick Test to Royal Jelly
Those with royal jelly sensitization, they have the
highest risk to honey bee derivatives (58.33%), to
honey (33.33%) and pollen (16.33%). A high
prevalence of subjects (19, 31.67%) were sensitized to
royal jelly only. The reactivities among the royal jelly
positivity towards other bee hive products were as
shown in Figure 3.
The calculated risk for subjects sensitized to
royal jelly to also be sensitized to honey bee
derivatives was at OR= .250 (.132 – .473), 95% CI).
Among those who were royal jelly sensitized
individuals, the risk was greater with OR = 2.682 (1.759
– 4.090, 95% CI). For those without royal jelly
sensitization, they have the risk of OR = .671 (.530 -
.851, 95% CI). A positive association was found
between positive royal jelly skin test and non
symptomatic atopic (OR = 3.13, 95% CI 1.31 to 7.46)
but not to non familial atopic (OR = 1.46, 95% CI .91
to 2.34).
3.4 Skin Test Reactivity Pattern to 80 Subjects with
Positive Skin Prick Test to Bee Pollen
Bee pollen sensitization individuals were found to be
risky to honey bee derivatives (62.50%), followed by
honey (30.00%) and royal jelly (22.50%). 26 (32.50%)
were found to be sensitized to only bee pollen. The
reactivities among the bee pollen positivity towards
honey bee and other bee hive products were as
shown in Figure 4.
The calculated risk for subjects sensitized to bee
pollen to also be sensitized to honey bee derivatives
was at OR =.274 (.149 – .504, 95% CI). Among those
who were bee pollen sensitized individuals, the risk is
greater with OR = 2.253 (1.594 – 3.183, 95% CI). For
those without bee pollen sensitization, they have the
risk of OR =.618 (.466 - .821, 95% CI).No positive
association was found between positive bee pollen
sensitization and both the symptomatic atopic (OR =
1.08, 95% CI .93 to 1.25) or to familial atopic (OR = .92,
95% CI .77 to 1.10).
Pollen
group
Honey group
Honey bee
derivatives
group
1
(1.67%)
14
(23.33%)
4
(6.67%)
6
(10.0%)
1
(1.67%)
10
(16.67%
)
5
(8.33%)
Figure 3 Prevalence of subjects with royal jelly
sensitization associated to honey bee and other bee
hive products sensitizations
Individuals
positive to
bee pollen
(N= 80)
Bee pollen
only
26 (32.5%)
Royal jelly
group
Pollen
group
Honey bee
derivatives
group
Individuals
positive to
honey
(N= 53)
Honey only
4 (7.55%)
4
(7.55%)
16
(30.19%)
2
(3.77%)
5
(9.30%)
1
(1.89%)
10
(18.87%)
11
(20.75%)
Figure 2 Prevalence of subjects with honey sensitization
associated to honey bee and other bee hive products
sensitizations
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4.0 DISCUSSION
A large percentage (54.86%) of the volunteers‟ skin
tested to these allergen extracts had a history of
allergy. 10.75% of the subjects had a positive skin
prick test (SPT) to at least bee hive products allergen.
In this study, bee hive product consumption among
subjects with its sensitization was slightly lower
(23.93%) compared to a study done by Leung et al.
[20] which was at 31.3%. Paradoxically, the
prevalence of royal jelly sensitization among the
atopic subjects in their study was 7.3%, while in this
study it was found that among the bee hive products
sensitized subjects, the prevalence of royal jelly
sensitization was 22.14%. This is three folds higher than
their findings.
Hence, an assumption can be derived that the
sensitization among our subjects with bee hive
product sensitization is three folds more risky
compared to those the atopic patients in Hong Kong
general population. Therefore, caution must be
taken to ensure individuals with any of the bee hive
sensitization should not to be exposed or consumed
these products and vice versa as they are of a more
risky subject.
Although Leung et al. [20] found a positive
association between positive royal jelly skin test and
symptomatic atopic (OR = 33.73, 95% CI 4.51 to
252.11) but in this study, it showed a negative
association for all the bee hive products to royal jelly.
It was only honey (OR = 4.62, 95% CI 1.51 to 14.18)
found to be positively associated to royal jelly
sensitization.
Risks of sensitization associations between the bee
hive products were described in this study. We found
that royal jelly sensitization was of the highest risk to
be associated to honey bee derivatives sensitization
(OR = 2.682), followed by bee pollen sensitization (OR
= 2.253) and the honey sensitization. Our results do
not only support finding by Leung et al. [18-21], but
also append to honey bee pollen sensitization [22-23,
34] and honey sensitizations [21, 31-32, 34].
Skin test reactivity varies among honey allergens.
Comb honey (11.8%) was more “allergenic”
compared to other honeys. Comb honey is an
“immature” honey and at this stage, honey bee
derivatives allergenic proteins such as the hyaluronic
enzymes from the honey bee saliva could probably
add to the allergenicity. Thus, this also explains the
least skin test reactivity was with imported honey.
Imported honey is prepared and comply to food
standard procedures prior to exporting. One of the
criteria is that the honey should comprise less than
17% moisture to prevent fermentation. This is also an
indicator the honey is fully matured. Hence all
allergenic proteins are digested.
Honey contains twenty to a hundred thousand
pollen grains which retain their allergenic properties
during the honey making process reported by
Helbling et al. [32]. As the local bottled (rubber,
Melalueca and coconut) honeys contain pollen
grains, which subjects are exposed, it is not surprising
that 4.8 – 5.9% of them are sensitized to them. When
compared to imported honey, it contains pollen that
the local population is not sensitized to. Thus, it is not
surprising that it gives the least subjects (3.0%)
sensitized to it.
29.5% of the bee hive products sensitized subjects
also had skin test reactivity to at least one type of
bee pollen. The preparation of commercial bee
pollen starts with collecting the pollen trapped at the
entrance of the bee hive, followed by the drying
process. The commercial bee pollen used in this
study is not a local product, but it is widely
consumed. The entrance bee pollen allergen was
prepared from fresh bee pollen collected at the bee
hive entrance. Comb pollen is different from
entrance pollen. Once the forager honey bee enters
the hive, worker honey bees then „process‟ the
pollen by mixing it with honey bee saliva and plant
nectar. The process could enhance allergenicity to it.
Ironically, this study showed more individuals were
skin test positive to the commercial bee pollen. The
entrance pollen was second, followed by comb
pollen and the coconut pollen. Although the comb
pollen is with the most contact with the honey bee
derivatives allergenic proteins, but the “fanning”
process of converting plant nectar into honey may
bring the same effect on comb pollen by denaturing
the allergenic proteins. Therefore, the comb pollen
has less sensitized subjects compared to the
entrance honey. The highest prevalence of
sensitization to the commercial bee pollen could be
explained that it has been observed as the most
widely consumed. Subsequently, the subjects are
well exposed to it and due to this, it gives rise to the
higher prevalence.
Bee products are promoted as a health tonic to
boost the immune system and as treatment for
allergies. Interestingly, we found that there was a
Royal
jelly
group
Honey
group
Honey bee
derivatives
Individuals
positive to
bee pollen
(N= 80)
Bee pollen
only
26 (32.5%)
1
(1.25%)
23
(28.75%)
2
(2.50%)
6
(7.50%)
1
(1.25%)
10
(12.50%)
11
(13.75%)
Figure 4 Prevalence of subjects with bee pollen sensitization
associated to honey bee and other bee hive products
sensitizations
Individuals
positive to
royal jelly
(N= 60)
Royal Jelly
only
19 (31.67%)
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positive association between the skin test reactivity to
house dust mites and bee hive products (OR = 1.831,
CI 95%: 1.60 – 2.09). This was also reported by Thien
et al. [19] and they suggested that cross-reactivity
between house dust mite and the honey bee
component might account for the high prevalence
of skin test reactivity to royal jelly in their population.
They assumed this could probably due to the
presence of honey bee component in royal jelly. In
our study population symptomatic atopic individuals
were more likely to be sensitized to these bee hive
products. Other investigators to list a few, Mansfield
and Goldstein [23], Helbling et al. [31] and Florida-
Lopez et al. [15] have expressed their concern with
regards to this issue.
From the pattern of skin test reactivity to bee hive
products, it can be assumed that allergic sensitization
to honey is related to proteins from either honey bee
derivatives or the nectar or pollen those in contact
with the honey bee. Studies by Dutau [31] suggested
differently, that if serums IgE from individuals with
honey bees sensitization are able to bind to a large
number of honey proteins and the prevalence of
honey allergies could be alleviated in those
allergenic to hymenopterans or among the
beekeepers. At present we are conducting further
studies to identify and characterize all the possible
allergenic proteins that are involved in the bee hive
products sensitization. Avoidance is always the
recommendation to allergy management. Therefore,
removing the allergenic proteins is the option to
lighten the problem, but it would be tough as bee
hive products are often used as the ingredients and
hidden in food, food supplements and energy
products.
5.0 CONCLUSION
Skin test reactivity to bee hive products is prevailed
to be high in Malaysia. As this study has proven that
bee hive products sensitized individuals are mostly to
be also sensitized to honey bees. Therefore, it is highly
recommended that honey bee by product allergens
to be included in the skin prick panel.
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