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ARTICLE IN PRESS

Journal of
Trace Elements
in Medicine and Biology
Journal of Trace Elements in Medicine and Biology 19 (2005) 183–189
www.elsevier.de/jtemb

FOOD CHAIN
Trace and mineral elements in royal jelly and homeostatic effects
Andreas Stockera,b,c, Peter Schramela, Antonius Kettrupa, Eberhard Bengscha,b,,1
a
GSF – National Research Center for Environment and Health, Institute of Ecological Chemistry, D-85758 Neuherberg, Germany
b
Centre de Biophysique Moléculaire, CNRS UPR 4301, University of Orléans, INSERM, F-45071 Orléans cedex 2, France
c
Lehrstuhl für Biologische Chemie, Fachgebiet Physikalische Biochemie, TU München-Weihenstephan, D-85350 Freising, Germany

Received 11 July 2005; accepted 24 August 2005

Abstract

Royal jelly from Apis mellifera is a highly active natural biological substance and is probably one of the most
interesting raw substances in natural product chemistry. Trace elements play a key role in the biomedical activities
associated with royal jelly, as these elements have a multitude of known and unknown biological functions. For this
reason concentrations of 28 trace (Al, Ba, Sr, Bi, Cd, Hg, Pb, Sn, Te, Tl, W, Sb, Cr, Ni, Ti, V, Co, Mo) and mineral
(P, S, Ca, Mg, K, Na, Zn, Fe, Cu, Mn) elements were systematically investigated in botanically and geologically
defined royal jelly samples. In addition, concentrations of 14 trace elements were measured in the associated honey
samples – honey being the precursor of royal jelly. Concentrations of K, Na, Mg, Ca, P, S, Cu, Fe, Zn, Al, Ba and Sr in
royal jelly were determined by inductively coupled plasma optical emission spectroscopy (ICP-OES), while
concentrations of Bi, Cd, Hg, Pb, Sn, Te, Tl, W, Sb, Cr, Mn, Ni, Ti, V, Co and Mo in royal jelly were determined
by double focusing magnetic sector field inductively coupled plasma mass spectrometry (SF-ICP-MS).
In the honey samples, trace and mineral element concentrations strongly depended on botanical and geological
origin, and substantial variation was found. In contrast, the concentrations of trace and mineral elements were highly
constant in the associated royal jelly samples. The most important results were the homeostatic adjustments of trace
and mineral element concentrations in royal jelly. This effect was evidently produced in the endocrine glands of nurse
bees, which are adapted for needs of bee larvae. In conclusion, this research yielded a surprising and completely new
finding – that royal jelly, as a form of lactation on the insect level, shows the same homeostatic adjustment as
mammalian and human breast milk.
r 2005 Elsevier GmbH. All rights reserved.

Keywords: Royal jelly; Honey; Trace elements; Minerals; Homeostatic effects

Introduction mately 66% water, 15% sugars, 5% lipids and 13%


proteins with a high content of essential amino acids and
Royal jelly is a bee product from the hypopharyngeal, vitamins [1,2], as well as minerals in the concentration
mandibular- and postcerebral glands of nurse bees (Apis range of 0.7–1.2% [3]. Royal jelly is of particular interest
mellifera). It is produced by the partial digestion of because, as a natural material, it offers probably the
essentially honey and pollen and consists of approxi- greatest potential to find new substances with pharma-
ceutical potential [4]. Biological activities of royal jellies
Corresponding author. are variable and have been correlated to their content of
1
In cooperation with J.M. Bonmatin. trace elements.

0946-672X/$ - see front matter r 2005 Elsevier GmbH. All rights reserved.
doi:10.1016/j.jtemb.2005.08.004
ARTICLE IN PRESS
184 A. Stocker et al. / Journal of Trace Elements in Medicine and Biology 19 (2005) 183–189

In preliminary descriptive studies elemental concen- The four royal jellies from Vendée-Maine (samples
trations of some trace and mineral elements were 1–4) were collected at four different sampling dates from
measured in pollen, nectar and royal jelly of the honey the same honeybee colonies in order to investigate
bee [5–7]. In total, nine elements were investigated to seasonal (i.e. botanical) variation of trace elements.
find correlations between alimentation, regional origin Pollen morphological analysis of main pollen in royal
and level of elements in royal jelly [8,9]. Several trace jelly samples from Vendée-Maine harvested on different
and mineral elements were used for the investigation of sampling dates showed following botanical origins:
authenticity of several samples [10]. Pyrus species and Brassica species in sample 1 (4 May
For honey and pollen, the precursors of royal jelly, 2001), Brassica species and Pyrus species in sample 2
trace and mineral elements were described as qualified (17 May 2001), Castanea sativa, Trifolium repens, Rubus
parameters of geographical, seasonal and botanical species in sample 3 (22 June 2001) and C. sativa in
origin. Analysis of honeys from defined botanical and sample 4 (2 July 2001). Royal jellies were kept at
geographical origins in France showed highly varying refrigeration temperature (41C) until analysis.
element concentrations depending on the plant material A total of 94 honey samples derived from various
[11,12]. Multi-floral honeys from Northern Italy [13] botanical, geographical and geological origins in France
showed significant differences in the concentrations of covering the very same variety of botanical origins and
trace elements depending on prevailing rock types. geochemical characters of underlying rock types (i.e.
Trace elements in honey samples from a large area in crystalline rocks, carbonate rocks, loess soils) as the
Hungary were useful as environmental indicators [14]. royal jellies were also collected and investigated. Honey
Higher levels of trace elements in pollen, honey and bee samples were kept under room temperature conditions
tissues were described for soils on volcanic rocks in until analysis.
Kenya compared to samples deriving from metamorphic
rocks [15]. The trace elements lead (Pb), cadmium (Cd)
Sample treatment
and manganese (Mn) were analysed in honey samples of
various seasonal origins – higher Pb contents being
Royal jelly and honey samples were wet digested at
found for the summer months [16].
170 1C with HNO3 in pressurised PTFE bombs with
The purpose of the present study was the systematic
inserted quartz tubes [17]. Approximately 500 mg of
investigation of a greater number of trace and mineral
royal jelly and 500 mg of honey respectively, were wet
elements in royal jellies of defined botanical (i.e.
ashed with 1 mL HNO3 (subboiling dest.). The solutions
seasonal) and geological origins. We produced and
were subsequently filled up to 10 mL with high purity
investigated royal jellies from crystalline rocks, carbo-
water (Milli-Q, Millipore, Germany) and analysed.
nate rocks and loess soils from several regions of
Depending on the concentrations further dilution was
France. In addition, a commercial royal jelly sample
necessary, in some cases, if the concentrations were
from China was analysed.
relatively high. The pressure ashing in PTFE bombs is
state of the art, so no losses have to be taken into
account [17]. From our experiences contaminations
during sample pretreatment in the laboratory could be
Materials and methods
excluded. For the natural raw material royal jelly
possible contamination of elements as e.g. aluminium
Samples
(Al) from dust aerosols before sampling cannot be
excluded as this is well-known for other biological
Royal jelly samples from various botanical, geogra-
materials.
phical and geological origins were produced 2001 in
cooperation with apiaries in France. Geologically
defined royal jelly samples were produced in order to Analytical instruments
determine trace element variations in royal jelly
depending on the geochemical character of underlying Determinations of several elements (Table 1) in royal
rocks in the region (i.e. rock types). Altogether seven jelly were carried out by double focusing magnetic sector
royal jelly samples were analysed in this study. Four field inductively coupled plasma mass spectrometry (SF-
royal jellies derived from crystalline rocks of St. André ICP-MS) [18], using the ELEMENT1 (Thermo Finni-
de la Marche, Vendée-Maine, France (samples 1–4), one gan MAT GmbH, Bremen, Germany). Pneumatic
from carbonate rocks of Chézelles, Centre, France nebulisation (Meinhard), a water-cooled spray chamber
(sample 5), and one from loess soils of Lugny, Picardie, (Scott type), a peristaltic pump (0.9 mL/min) and a
France (sample 6). In addition, one commercial royal sample changer ASX-400 (CETAC, USA) were used for
jelly sample was obtained from loess soils in China sample introduction. Commercially available nickel-
(sample 7). cones were used in the interface.
ARTICLE IN PRESS
A. Stocker et al. / Journal of Trace Elements in Medicine and Biology 19 (2005) 183–189 185

Table 1. Elements in royal jelly and honey and methods used for analysis

Samples Methods Elements

Royal jelly ICP-OES K, Na, Mg, Ca, P, S, Cu, Fe, Zn, Al, Ba, Sr
ICP-MS
Royal jelly Resolution of 300 Bi, Cd, Hg, Pb, Sn, Te, Tl, W, Sb
ICP-MS
Royal jelly Resolution of 5500 Cr, Mn, Ni, Ti, V, Co, Mo
Honey ICP-OES Al, B, Ba, Ca, Cu, Fe, K, Mg, Mn, P, S, Si, Zn, Sr

We have determined concentrations of 28 trace compared to 94 honeys from the same geological origins
elements in royal jellies. The elements bismuth (Bi), in Figs. 1 and 2.
Cd, mercury (Hg), Pb, stannous (Sn), tellurium (Te), Royal jelly sample 3 from Vendée-Maine was
thallium (Tl), tungsten (W) and antimony (Sb) in royal analysed in solutions from two independent digestions
jelly (bulk material) were measured with SF-ICP-MS as of aliquots. Trace element values are given as mean of
described above at a resolution of 300. The elements two results 7 difference to the mean value (Table 2) to
chromium (Cr), Mn, nickel (Ni), titanium (Ti), vana- show the analytical uncertainty and the biological
dium (V), cobalt (Co) and molybdenum (Mo) were variability of the samples.
measured with SF-ICP-MS at a resolution of 5500 Concentrations of the mineral elements P, S, Ca, Mg,
(Table 1). The estimated analytical uncertainty was less K and Na were roughly identical in royal jelly samples
than 5%. (Table 2, Fig. 1). No significant difference could be
Inductively coupled plasma optical emission spectro- found for mineral element concentrations from royal
scopy (ICP-OES) was used for the measurement of the jelly samples from different botanical and geographical
elements potassium (K), sodium (Na), magnesium (Mg), origins.
calcium (Ca), phosphorous (P), sulphur (S), copper Concentration of the mineral elements P, S, Ca, Mg
(Cu), iron (Fe), zinc (Zn), Al, barium (Ba) and and K in the associated honeys (Fig. 1) showed
strontium (Sr) in royal jelly samples and for the significant variability depending on botanical origin
measurement of Al, boron (B), Ba, Ca, Cu, Fe, K, [11,12]. Mineral element concentrations in honeys varied
Mg, Mn, P, S, silicon (Si), Zn, Sr in honey samples (bulk within approximately one decimal power and had
material). Combined sequential/simultaneous ICP spec- significant lower concentrations than the royal jelly
trometers JY 70 and JY 66 ICP, respectively (Jobin samples.
Yvon Longjumeau cedex, France), a 1.5 kW RF- Thus concentrations of mineral elements in royal
generator, a computer system and a concentric pneu- jellies are accumulated compared to the associated
matic nebuliser were used for routine analysis [19]. honeys. Factors of accumulation are approximately
Again the analytical uncertainty was in the range of less 20-fold for P, 20-fold for S, 5-fold for Ca, 10-fold for
than 5%. Mg and 1-fold for K (Fig. 1).
Analytical accuracy and precision and limits of Al and Si are elements that are well known for
detection were determined using several bio-medical exogenous contaminations with dust aerosols. There-
control or certified reference materials as well as fore, Al and Si have to be regarded carefully. Al was
chemical and procedural blank values as described for found in highly differing concentrations. Higher Al
ICP-OES in [17,19] and for ICP-MS in [18]. values in the royal jellies (between 54.7 mg/kg (Table 2;
sample 3) and 27.6 mg/kg (sample 4)) were most likely
aerosol contaminations from former uranium mines in
Vendée-Maine. Al concentrations of 8.4, 4.7 and 1.6 mg/
Results kg were, therefore, probably more reliable (Table 2).
For the trace elements Zn, Fe, Cu and Mn, a similar
Contents of 28 trace and mineral elements of seven situation was found as for the mineral elements (Fig. 2).
royal jelly samples from defined botanical and geologi- Zn concentrations in royal jelly were highly adjusted, as
cal origins were analysed. Concentrations of 23 trace observed for the mineral elements. Fe, Cu and Mn had
and mineral elements are given in Table 2. Concentra- only a small range of variation. Mn was the only
tions of five trace elements in royal jelly were below element with smaller element concentrations in royal
limits of determination. Element concentrations of nine jellies as compared to the associated honeys (Fig. 2).
trace and mineral elements of the seven royal jellies are Factors of element accumulation in royal jelly are
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186 A. Stocker et al. / Journal of Trace Elements in Medicine and Biology 19 (2005) 183–189

Table 2. Mineral and trace elements in royal jelly samples from different seasonal (i.e. botanical), geographical and geological
origins: sample 3 was analysed for two independent sample digestions of aliquots

Crystalline rocks Carbonate rocks Loess soils Loess soils

(1) May 4 (2) May 17 (3) June 22b (4) July 2 (5) (6) (7)

P (mg/kg) 2060 2000 1949726 1960 1940 2350 2010


S (mg/kg) 1390 1210 1154716 1320 1290 1420 1340
Ca (mg/kg) 117 113 12079 122 113 145 129
Mg (mg/kg) 275 268 28277 269 264 312 28
K (mg/kg) 2770 2700 2462782 3050 2630 3120 2730
Na (mg/kg) 119 127 12772 106 107 129 142
Al (mg/kg) 0.8 40.2 54.7721.6 27.6 4.7 8.4 1.6
Zn (mg/kg) 20.6 20.3 20.170.1 19.4 22.4 24.8 24.4
Fe (mg/kg) 9.1 17.5 20.575.3 17.5 10.2 22.1 11.0
Cu (mg/kg) 4.1 7.4 8.171.8 7.9 4.6 8.0 4.0
Cr (mg/kg) 0.33 2.69 2.9771.35 2.62 0.65 2.93 0.34
Mn (mg/kg) 0.95 0.76 1.0670.16 4.35 0.70 1.48 0.78
Ni (mg/kg) 0.14 1.41 1.6571.05 1.45 0.33 1.70 0.15
Ti (mg/kg) o0.14a 0.71 1.5570.70 0.45 0.23 0.32 0.26
Sn (mg/kg) 196 277 143713 185 31 73 15
Hg (mg/kg) o1a 31 2675 31 2 36 1
Pb (mg/kg) 33 172 287785 17 50 32 51
Cd (mg/kg) 13 14 1973 12 2.2 6.9 1.3
W (mg/kg) 14 933 482071610 2.6 56 16 21
Te (mg/kg) 0.3 4.9 6.171.2 7.8 0.8 9.1 0.7
Sb (mg/kg) 0.4 1.3 5.472.3 1.3 0.8 1.5 0.5
Tl (mg/kg) 0.3 0.8 1.1570.05 0.3 0.4 0 0.1
Bi (mg/kg) 11 1.7 6.170.9 1.6 13.5 13 7.9
a
These values were below limit of determination.
b
See results section. Concentrations of Ba (o100 mg/kg), V (o200 mg/kg), Co (o200 mg/kg), Mo (o400 mg/kg) and Sr (o100 mg/kg) were below
limit of determination. Samples 1–4 were from Vendée-Maine, sample 5 from Centre and sample 6 from Picardie, France. Sample 7 was from China.
All samples were produced in 2001.
concentration (mg kg-1)

1000

100
90%
75%
50% percentiles
25%
10%
10

P S Ca Mg K Na

Fig. 1. Homeostasis of mineral elements in royal jelly and honey samples of various seasonal and geographical origins. Shown are
the 10%, 25%, 50%, 75%, and 90% percentiles of P, S, Ca, Mg, K and Na concentrations in seven royal jelly samples (grey bars),
and in 94 honey samples (white bars). Na was only measured in royal jelly samples.

approximately 30-fold for Zn, 20-fold for Fe and 15-fold botanical) differences and samples produced on crystal-
for Cu. line rocks had little higher Pb, Hg and Sn concentrations
Cr and Ni concentrations varied depending on compared to samples from carbonates and loess. The
seasonal and geological origins (Table 2). Pb, Hg and element Pb was biologically coupled with S. Ti, Cd and
Sn concentrations had similar patterns. Royal jelly W concentrations, analogous to the other heavy metals
samples from Vendée-Maine showed seasonal (i.e. Pb, Sn and Hg, also varied depending on seasonal
ARTICLE IN PRESS
A. Stocker et al. / Journal of Trace Elements in Medicine and Biology 19 (2005) 183–189 187

100

concentration (mg kg-1)


10

90%
1 75%
50% percentiles
25%
10%
0.1

0.01
Zn Fe Cu Mn

Fig. 2. Homeostasis of trace elements in royal jelly and honey samples of various seasonal and geographical origins. Shown are the
10%, 25%, 50%, 75%, and 90% percentiles of Zn, Fe, Cu, and Mn concentrations in seven royal jelly samples (grey bars), and in 94
honey samples (white bars).

effects and to a smaller degree depending on geological and as a consequence vary in honeys from different
origins (Table 2). botanical origins [11,12,21]. Highly varying concentra-
W concentrations were highly variable. The highest tions of mineral elements have been also described for
values were found in crystalline basements of the Vendée pollen of different plant species [5,10]. K, Na, Mg and
(Table 2). Te, Sb, Tl and Bi had patterns similar to the Ca are the predominant mineral elements in pollen.
other heavy metals. Concentrations in royal jelly Honey and pollen are the biochemical precursor
samples showed significant differences depending on substances of royal jelly, making royal jelly much more
seasonal and geographical origin. processed and modified than honey. In bee tissue, K was
Concentrations of the five trace elements Ba, V, Co, also found in high concentrations of 11 180 mg/kg [23].
Mo and Sr in royal jelly were analysed and were found It is therefore evident that homeostatic adjustment of K
to be below the limits of determination (Table 2). in royal jelly corresponds to the needs of the bee larvae.
Na concentrations in royal jelly samples were also
much adjusted. (Na was not measured in honeys.) Royal
jelly sample 4 from Vendée-Maine from the end of the
Discussion and conclusions royal jelly harvesting season showed a lower Na value of
106 mg/kg. An elevated Na concentration of 142 mg/kg
The most abundant mineral elements in royal jelly was found in a commercial royal jelly sample from
samples were K, Na, Mg, Ca, P, and S. Zn, Fe, Cu, Al China (Table 2, sample 7).
and Mn were abundant trace elements in royal jelly The [K]/[Na] ratios ranged from approximately 19 to
(Table 2; Figs. 1 and 2). 28 in the seven royal jelly samples, seasonal and
Concentrations of P and S in royal jelly were adjusted geographical variations were comparatively low. The
for the needs of the bee larvae. P is a structure element in [Mg]/[Ca] ratios had a relatively small range, from 2.2 to
the nucleic acids of royal jelly and construction element 2.3. [K]/[Na] ratios were more dependent on seasonal
for the larvae. S concentrations in the royal jelly are and geographical variation than the [Mg]/[Ca] ratios.
likely to be related with the disulphur bridges of Al concentrations differed greatly in the royal jelly
proteins. Homeostatic adjustments of P and S in royal samples. Values from 54.7 to 27.6 mg/kg were most
jelly samples are likely to be related to high and constant likely an aerosol contamination whereas values from 8.4
amounts of nucleic acids and phospho-proteins. to 0.8 mg/kg seem more reliable. Exogenous contamina-
Concentrations of Ca and K in honey depend on the tions of Al from aerosol dust are well known in trace
bioavailability in the soil and therefore on the chemistry element analysis. In Vendée-Maine open cast mining of
of the source rocks. Highly variable Ca and K uranium took place some decades ago and closed mines
concentrations were therefore found in honey samples can still play a role in Al aerosol contaminations. The
(Fig. 1). The different chemistry and geological age of honeybee is probably capable of adjusting to Al in lower
source rocks and resulting soils, e.g. crystalline rocks, concentrations. High Al amounts in the environment
carbonates and loess, lead to a different bioavailability certainly result in elevated Al concentrations in the royal
of the elements for the plants [20]. Furthermore, element jelly.
fractionation of the plants plays a role depending on the Homeostatic adjustment of the trace elements Zn, Fe,
deepness of the roots. The concentrations of mineral Cu and Mn was observed as for the mineral elements.
elements like Ca and K depend on the bioavailability, Zn concentrations were more strongly adjusted in royal
ARTICLE IN PRESS
188 A. Stocker et al. / Journal of Trace Elements in Medicine and Biology 19 (2005) 183–189

jelly compared to the concentrations of Fe, Cu and Mn The strictly homeostatic composition with regard to
(Fig. 2). The nurse bee seems to physiologically regulate trace and mineral elements shows the analogy to
zinc concentrations according to the needs of the bee mammalian milk where identical effects can be ob-
larvae. Homeostatic adjustment of Fe, Cu and Mn also served. This is comprehensible considering the model
seemed to occur, but to a lesser degree, leaving a that royal jelly excretion is a form of lactation on the
slight correlation depending on different source rocks insect level.
(Table 2, Fig. 2) as a consequence of different bio-
availability of the elements.
The royal jelly samples with low concentrations of Cr
Acknowledgements
were also low in Cu and Fe (Table 2). Ni and Cr in royal
jellies from Vendée-Maine showed low concentrations at
This work was granted by research contracts between
the beginning and higher concentrations in the middle
Gesellschaft für Strahlenforschung (GSF), Neuherberg,
and at end of the season. This effect of lower concen-
Germany and Centre National de la Recherche Scien-
trations of several trace elements at the beginning of the
tifique (CNRS) Orléans, France, the Centre de Co-
season (sample 1) could be observed for several other
opération Universitaire Franco-Bavarois (CCUFB/
trace elements, especially the heavy metals (Table 2).
BFHZ), Munich, the Université Franco-Allemand
This can be due to a late arrival of the trace elements in
(UFA/DFH), Sarrebruck, the Union Nationale de
the pollen and nectars in the mid of May. Sn values
l’Apiculture (UNAF), France and Syndicat National
show that the plants have a fractionation capacity from
d’Apiculture (SNA), France. We thank Prof. F. Korte
the phloem to the analysed product, the royal jelly.
for his initiating help and encouragement to start this
The lowest concentrations of the heavy metals Pb, Ti,
research.
Sn, Hg, Cd, W, Te, Sb, Tl and Bi were found at the
We thank for assistance and discussions:
beginning of the season (Table 2, sample 1). Higher
concentrations were found in samples from the same  P. Grill, I. Wendler, GSF Neuherberg (honey
geographical origin but later harvesting date. Heavy analysis).
metal concentrations in royal jelly also appear to be  Dr. M. Gänzle, TU München (biology), Prof. P.
influenced by bioavailability and plant physiological Horn, LMU München (geology), A. Mary, St. André
effects. Sr concentrations in royal jellies in this de la Marche, France and M. Mary, Chézelles, France
investigation series were below the limit of determina- and P. Charpentier, Lugny, France (apidology).
tion.  Dr. H. Horn, Universität Hohenheim-Stuttgart (pol-
Elias et al. [24] have described similar homeostatic len analysis).
effects concerning the natural discrimination of Pb, Ba  Dr. V.F. Medina, ERDC Vicksburg, USA (review of
and Sr in relation to Ca along similar nutrient pathways the manuscript).
i.e. soil/plant/herbivorous insects. Physiological regula-
tion of Cd has been found in human milk [25].
Nascarella et al. [26] have described hormesis and stage
specific toxicity of Cd in the queen blowfly, Phormia
regina. Homeostatic effects have also been reported in
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