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ORIGINAL PAPER
Uranium distribution in broiler organs and possibilitiesfor protection
Branislava Mitrovic • Gordana Vitorovic • Milijan Jovanovic •
Mirjana Lazarevic-Macanovic • Velibor Andric •
Mirjana Stojanovic • Aleksandra Dakovic • Dusko Vitorovic
Received: 7 May 2013 / Accepted: 21 September 2013 / Published online: 5 October 2013
� Springer-Verlag Berlin Heidelberg 2013
Abstract The aim of the present study was to investigate
the distribution of uranium (uranyl nitrate hexahydrate,
UN) in muscle and organs (kidney, liver, and brain) of
broilers, after a 7-day contamination with UN and admin-
istration of two different adsorbents (organobentonite and
organozeolite). The birds were contaminated during 7 days
with 25 mg/UN per day. Adsorbents were given via gastric
tube, immediately after contamination with UN. In group 1
that did not receive any adsorbents, histopathological
changes in the contaminated broilers were observed in
small intestine, liver, and kidney in the form of necrosis of
intestinal villi, oedema and cytoplasmic vacuolation of
hepatocytes, and dystrophic changes in the kidney tubules
epithelium. Organobentonite administered via gastric tube
(group 2) reduced uranium distribution by 66 % in kidney,
81 % in liver, and 34 % in brain. In group 3, administration
of organozeolite reduced uranium distribution by 67 % in
kidney, 68 % in liver, and 49 % in brain. In groups 2 and 3,
where the broilers received adsorbents immediately after
the UN contamination, no histopathological lesions were
observed.
Keywords Uranium � Toxicity � Broilers �Adsorbents � Organobentonite � Organozeolite
Introduction
In the literature, there are insufficient data on the transfer of
uranium and its toxicity in birds. Phosphate mineral pre-
mix, especially dicalcium phosphate, may contain uranium
from 30 to 200 ppm (corresponding to an activity range
from 388 to 2,444 Bq/kg) (Arruda-Neto et al. 1997).
Dicalcium phosphate can be used as mineral fertilizer, as
well as phosphate mineral premix for animal feed. When
importing dicalcium phosphate in Serbia, gamma-spectro-
metric analyses are mandatory. At this occasion, it was
found that the activity of uranium in dicalcium phosphate
may be up to 3,000 Bq/kg and import of mineral premix
was banned. This demonstrated the need to study transfer
of uranium and its toxicity in birds in more detail.
Uranium (U) is a naturally occurring radioactive and
chemically toxic heavy metal. The harmful effects of ura-
nium are mainly due to its chemical toxicity. Additionally,
ionizing radiation emitted during the decay of uranium can
increase the incidence of cancer in various tissues, as a
stochastic risk (NRC 2008). After contamination, uranium
accumulates mainly in the bones (66 %), kidneys (8 %),
and liver (16 %) (ICRP 1996), in humans. Some studies
showed—for humans, rabbits, rats, and mice—that the
kidneys are the primary target organ for toxicity of ura-
nium, where uranium caused renal damage, both structural
B. Mitrovic (&) � G. Vitorovic � M. Lazarevic-Macanovic �V. Andric
Department of Radiology and Radiation Hygiene, Faculty
of Veterinary Medicine, University in Belgrade, Bulevar
Oslobodjenja 18, 11000 Belgrade, Serbia
e-mail: [email protected]; [email protected]
M. Jovanovic � A. Dakovic
Department of Veterinary Pathology, Faculty of Veterinary
Medicine, University in Belgrade, Bulevar Oslobodjenja 18,
11000 Belgrade, Serbia
M. Stojanovic
Institute for Technology of Nuclear and Other Mineral Row
Materials, University in Belgrade, Bulevar Frans d‘Eperea 86,
11000 Belgrade, Serbia
D. Vitorovic
Faculty of Agriculture, University in Belgrade, Nemanjina 6,
11080 Zemun, Serbia
123
Radiat Environ Biophys (2014) 53:151–157
DOI 10.1007/s00411-013-0496-3
and functional (Vicente-Vicente et al. 2010; Gilman et al.
1998a, b, c; Olguin et al. 1997; Domingo et al. 1987).
Uranium can also accumulate in the liver and brain of mice
as observed by Ozmen and Yurekli (1998). Ghosh et al.
(2007) report that uranyl nitrate administrated in acute
nephrotoxic dose caused oxidative stress in brain and bone
of Wistar rats, manifested as a lipid peroxidation and his-
topathological damage.
In general, animal contamination with uranium can
occur through ingestion, inhalation, and skin contact.
Among these pathways, ingestion is the most common way
of contamination. In order to satisfy the nutritional
requirements for minerals, phosphate mineral supplements
(mostly monocalcium and dicalcium phosphate), which
may contain high concentrations of uranium, are added in
animal feed (Arruda-Neto et al. 1997; Izak-Biran et al.
1989). These mineral supplements were given to the ani-
mals from their early period of life to the slaughtering. In
an experiment performed with Beagle dogs from post-
weaning until the adult phase, where uranium mixed with
food was administered to the animals, it was observed that
uranium accumulates at same amounts in mineral bone and
bone marrow, and that saturation is reached only after
about 10 years (Arruda-Neto et al. 2004). These authors
reported that after a chronic ingestion period of about
5 years, for each ppm ingested (1 lg U/g food), accumu-
lation in bone and bone marrow is equal to 1 lg U/g bone
(in terms of U dry mass). However, anatomy, physiology,
and metabolic capability in birds are different when com-
pared to mammalians. The retention of ingesta and the pH
values at certain sites of the digestive tract are different in
each segment of digestive tract (Denbow 2000; Klasing
1999; Buyse et al. 1993; Shires et al. 1987).
In veterinary medicine, administration of protectors,
applied as a food additive, is one of the countermeasures to
reduce internal contamination with radionuclides (Mitrovic
et al. 2012, Slavata and Vitorovic 2004; Vitorovic et al.
2002; Howard et al. 2001), to eliminate heavy metals
(Papaioannou et al. 2005), and to protect animals against
mycotoxin intoxications (Oguz 2011; Rizzi et al. 2003;
Ortatatli and Oguz 2001; Parlat et al. 1999). Sorption of
uranium, under in vitro conditions, on modified bentonite
(Majdan et al. 2010a; Donat and Aytas 2005; Olguin et al.
1997) and organozeolite (Matijasevic et al. 2006) has a
very important role in environmental remediation. The
organobentonite reveals sufficient sorption ability towards
U (VI) both from acidic and from alkaline solutions
(Majdan et al. 2010b).
In the present work, the ability of organobentonite to
remove uranium (VI) at different solution pH values
(in vitro conditions), and further, the possibility of its use in
case of broiler contamination with uranium (in vivo
experiments) are described. Since organozeolites were also
demonstrated to show an affinity towards uranium under
in vitro conditions (Matijasevic et al. 2006), this chemical
was used here as a second adsorbent (kindly provided by
Matijasevic et al. (2006)). The uranium distribution in
kidney, liver, brain, and muscle, after a 7-day contamina-
tion with uranyl nitrate (UN), was determined. The
experiments were performed on broilers receiving UN and
adsorbents, via gastric tube, during the 7 days. In order to
determine the toxicity of uranium, histopathological
examinations of kidney, liver, brain, and small intestine
were performed.
Materials and methods
Adsorbents
Natural bentonite from Sipovo, a deposit in Bosnia, was
used as the starting material. The main mineral in the raw
material is montmorillonite, while accessory minerals are
quartz and calcite. After concentration, the bentonite
sample was activated with ‘‘Dodigen 1828’’ (Hoechst AG,
Germany). ‘‘Dodigen 1828’’ is a mixture of alkylammo-
nium salts with alkyl chain length of 14–18 carbon atoms.
The zeolitic sample used in these experiments was from
the Beocin deposit (Fruska Gora, Serbia). It mainly consists
of heulandite with smaller amounts of quartz, feldspar, and
calcite. The organozeolite was prepared by treatment with
hexadecyltrimethylammonium chloride (HDTMA) sup-
plied by Hoechst AG (Germany). The procedure for
preparation of organozeolite was described by Matijasevic
et al. (2006).
Uranium sorption (in vitro conditions)
In order to investigate the uranium (VI) adsorption on or-
ganobentonite (OB), different amounts (0.01, 0.025, 0.05,
0.1, 0.25, 0.5, 0.7, 0.9, and 1 g) of adsorbent were added to
50 ml of uranium (VI) solution. The adsorption of uranium
(VI) ions on organobentonite was studied at pH 3 and 6.
The pH of the solution was adjusted with HNO3. Uranium
(VI) solutions were prepared using uranyl nitrate hexahy-
drate (UO2(NO3)2�6H2O) (Sigma-Aldrich Co.). Uranyl
nitrate was used because a procurement procedure of ura-
nyl nitrate is simple. Also, most of the experiments
described in the literature were performed with uranyl
nitrate. Initial concentration of uranium (VI) ions was
constant in each probe (10 lgU/ml (500 lg U/50 ml) in
pure distilled water). The samples were shaken for 5, 10,
15, 30, 60, 120, 240, 360, and 1,440 min at mechanical
shaker [150 revolutions per minute (rpm)].
After shaking, solids were separated by filtration, and
the concentration of uranium (VI) remaining in solution
152 Radiat Environ Biophys (2014) 53:151–157
123
was determined using a fluorometric method. The per-
centage of uranium adsorbed (%) was calculated by:
Adsorption %ð Þ ¼ Ci � Cf=Cið Þ � 100
where Ci is the initial uranium (VI) concentration, and Cf is
the uranium (VI) concentration in final solution. All
experiments were performed in duplicates.
Uranium sorption in vivo conditions
Experiments were performed on thirty-five-day-old broilers
of linear hybrid Hybro, showing a mass of about 1,000 g.
By the method of the random sampling, 36 broilers were
selected. Food and water intake were ad libitum. The birds
were kept under constant temperature (21 ± 2 �C) with a
12:12-h (light–dark) cycle. They were divided into five
experimental groups, with six birds per group. The zero
group (0) was administered neither UN solution nor
adsorbents.
During the 7 days, birds in groups 1, 2, and 3 were
contaminated via gastric tube, with uranyl nitrate water
solution (UO2(NO3)2�6H2O) (Sigma-Aldrich Co.), in
quantity of 25 mg UN/per day. The control group (1)
received only UN and no protectors. After the UN con-
tamination, the broilers in groups 2 and 3 received or-
ganobentonite (OB) and organozeolite as adsorbents,
immediately after contamination. The broilers in group 2
received a dose of 2 g organobentonite daily, while broilers
in group 3 received 2 g organozeolite daily. In group 4,
broilers received only organobentonite (2 g/per day),
whereas the broilers in group 5 received only organozeolite
(2 g/per day). In our earlier investigation (Slavata and
Vitorovic 2004; Mitrovic et al. 2012), we found that 2 g of
adsorbents did not show any significant health effects.
On the eighth day, the birds were stunned and then
killed by cervical dislocation, and uranium concentration
was determined in muscle, kidney, liver, and brain of
broilers. Histopathological analyses were performed on
samples of small intestine, kidney, liver, and brain.
Sample preparation
Organs (kidney, liver, brain, and muscle) were weighed to
get the fresh weight and then dried at 105 �C. After drying,
all samples were dissolved by microwave digestion on
‘‘Milestone Ethos 1.’’
Quantification of uranium
Uranium content in the initial solution, filtrate, muscle and
organs of broilers (kidney, liver, brain) was determined by
fluorometry based on the fluorescence of uranium in a fused
mixture of NaF, Na2CO3, and K2CO3, on a ‘‘Jarrell Ash
26-000 Division.’’ Uranium extraction was done with
10 cm3 synergistic mixtures 0.1 M TOPO (tri-n-octylphos-
phine oxide) in ethyl acetate. Organic phase aliquots were
evaporated to dry, and the dry residue was heated to 700 �C
with a mixture of NaF (9 %) ? NaKCO3 (91 %). Fluores-
cence intensity was then measured with a fluorometer that
showed a linear dependency with uranium concentration.
The concentration of uranium was determined from standard
uranium calibration curves (detection limit 0.005 mg/kg,
correlation coefficient R [ 0.997) (Stojanovic et al. 2010).
Histopathological analyses
After the birds were killed, samples of small intestine,
kidney, liver, and brain were rinsed with NaCl 0.9 % and
fixed in 10 % formaldehyde solution, dehydrated, embed-
ded in paraffin, and cut into 5-lm-thick sections. The
resulting histopathological slides were stained with hae-
matoxylin and eosin (H&E).
Results
In vitro experiments
It is well known that uranium (VI) speciation is highly
dependent on pH (Gadelle et al. 2001): at low pH values,
U(VI) exists as uranyl cation, UO22?, while at higher pH
values, mononuclear (e.g., [UO2(OH)?]) as well as poly-
nuclear (e.g., [(UO2)2(OH)2]2?, [(UO2)3(OH)5]?) hydro-
lysis products are formed. Occurence of species such as
U2O52?, U3O8
2? has also been suggested (Misaelides et al.
1995), while uranium (VI) carbonate anionic complexes
may be formed at pH values higher than 9. Thus, the pH
values of the initial solution are important variable for the
adsorption of uranium (VI) ions on the adsorbents (Donat
and Aytas 2005).
In the present experiments, kinetics of uranium (VI) ions
adsorption at different pH values was studied. Figure 1
shows the results of uranium (VI) ions adsorption on or-
ganobentonite (0.5 g), for different contact times, at pH 3
and 6. The uptake of uranium (VI) ions by organobentonite
at pH 6 was initially rapid reaching 100 % after 5 min, and
at this level maintained constant during the whole experi-
ment. In contrast, uranium (VI) ions adsorption at pH 3 was
lower and significantly slower, but increased over time.
Desorption processes were not observed. Adsorption of
uranium (VI) ions at different amounts of organobentonite,
at pH 6 and 3, is shown in Table 1, for a contact time of
2 h. A preliminary experiment at pH 3 showed that when
the amount of organobentonite was \0.1 g, the adsorption
of uranium (VI) ions was low; thus, experiments with
lower amounts of organobentonite were not performed.
Radiat Environ Biophys (2014) 53:151–157 153
123
These results indicate that adsorption of uranium (VI)
ions, at pH 3, increases with increasing amount of or-
ganobentonite. However, much higher adsorption of ura-
nium was observed at pH 6 (Fig. 1), and uranium
adsorption also increased with increasing adsorbent mass
(Table 1). For organozeolite (OZ), Matijasevic et al. (2006)
also reported that adsorption of uranium increased with
increasing amount of organozeolite and that higher
adsorption was achieved at pH 6 than at pH 3. Note that
this organozeolite was also used for the in vivo studies
described below.
These results shown in Fig. 1 and Table 1 are used for
setting up the parameters for the in vivo studies described
below, where a mass ratio adsorbent:U of 80:1 (2 g of each
adsorbent and 25 mg U) was used.
In vivo experiments
In muscle and selected organs of broilers in groups 0, 4,
and 5, uranium could not be detected (\0.001 lg/g). In
contrast, uranium residues were detected in kidney, liver,
and brain of broilers in the control group (group 1) and in
groups where the broilers received adsorbents after the
contamination (groups 4 and 5; Table 2). The mean ura-
nium concentration in kidneys from group 1 was three
times higher compared to that from groups 2 (UN ? OB)
and 3 (UN ? OZ), while in liver, mean uranium concen-
tration in the control group was three to five times higher
compared to that in groups 3 and 2. Finally, uranium
concentration in brain from group 1 was about one and half
to two times higher than that from groups 2 and 3. No
effects of broilers’ food and water intake and behaviour on
uranium concentrations were observed.
Histopathological changes in broilers contaminated with
a dose of 25 mg 238U/daily were found in the kidney, liver,
and small intestine, in the form of dystrophic changes in
the kidney tubules epithelium (Fig. 2), oedema and vacu-
olization of the cytoplasm of hepatocytes (Fig. 3), and
necrosis of intestinal villi (Fig. 4). In contrast, the exam-
ined tissues of broilers that received adsorbents OB and OZ
after their contamination with UN (groups 2 and 3), and of
broilers that received only adsorbents OB and OZ (groups
4 and 5), did not show any difference from the normal
histological structure.
Discussion
The digestive tract of broilers is different to that of mam-
mals. The pH values in the digestive tract of broilers range
from 2.5 to 8 (crop 5.5, proventriculus/gizzard 2.5–3.5,
duodenum 5–6, jejunum 6.5–7.0, ileum 7.0–7.5, colon 8)
(Denbow 2000; Klasing 1999). The mean retention time of
feed in crop and gizzard is about 8 and 50 min,
Fig. 1 Adsorption of uranium (VI) ions on organobentonite (0.5 g),
at different contact times, for pH values 3 and 6
Table 1 Adsorption of uranium ions (%) for different masses of
organobentonite, at pH values 6 and 3, and for a contact time of 2 h
Mass of
adsorbent (g)
Uranium removal (%)
at pH 6
Uranium removal (%)
at pH 3
0.01 65.7 –
0.025 84.5 –
0.05 93.1 –
0.1 99.3 19.1
0.25 99.6 20.1
0.5 99.7 77.8
0.7 99.9 91.8
0.9 – 97.3
1 – 99.8
Table 2 Uranium residues (lg/g) in muscle and selected tissues of broilers
Group Muscle Kidney Liver Brain
UN control (group 1) 0.09 ± 0.03 1.25 ± 0.21 1.0 ± 0.13 0.41 ± 0.09
UN ? OB (group 2) 0.03 ± 0.01 0.42 ± 0.13 0.19 ± 0.06 0.27 ± 0.09
UN ? OZ (group 3) 0.07 ± 0.02 0.41 ± 0.02 0.32 ± 0.07 0.21 ± 0.05
Data are given as means of six animals in each group and corresponding standard deviation
UN uranyl nitrate, OB organobentonite, OZ organozeolite
154 Radiat Environ Biophys (2014) 53:151–157
123
respectively, while the mean retention time in the whole
intestinal tract is about 6 h in 800 g weight broilers (Buyse
et al. 1993; Shires et al. 1987). The present in vitro study
showed that the adsorption of uranium (VI) ions at pH 6 is
high and fast, and equilibrium is practically achieved
already after 5 min of contact between uranium (VI) ions
and organobentonite. Although adsorption of uranium (VI)
ions at pH 3 is lower, it was observed that the fraction of
uranium adsorbed increases with increasing contact time
between the adsorbent and the uranium (VI) ions. The
present results also show that administration of organo-
bentonite to broilers, immediately after the contamination
with uranium, will reduce the uranium distribution in tis-
sues and organs.
By examination of uranium distribution in broilers, the
target organs for uranium contamination could be identi-
fied. After 7 days of contamination with UN, broilers
showed a significant distribution of uranium in kidney and
liver. Uranium concentration in brain was three times less
than that in kidney and 2.5 times less than that in liver.
Additionally, in muscle, the uranium concentration was 14
times lower than in kidney, 11 times lower than in liver,
and 4.5 times lower than in brain, indicating that muscles
are not the major target for uranium deposition. Ozmen and
Yurekli (1998) found that after subacute uranyl acetate
exposure of mice, the radioactivity was higher in brain than
in kidney and liver.
After the contamination of broilers with UN and protec-
tion with adsorbents organobentonite and organozeolite,
uranium concentrations in selected organs and muscle were
less than those in the control group (group 1). It was shown
here that in broilers the application of organobentonite
(group 2) reduced uranium concentration by 66 % in kidney,
81 % in liver, 34 % in brain, and 67 % in muscle. In contrast,
in group 3, administration of organozeolite reduced the
uranium concentration by 67 % in kidney, 68 % in liver,
49 % in brain, and 22 % in muscle. Based on the presented
data, it can be concluded that the investigated adsorbents
showed a high efficiency of protection in liver and kidney,
while the efficiency of protection in brain and muscle was
lower. According to the present results, the efficiency of
protection in kidney, liver, and brain is on average 60 % for
organobentonite and 61 % for organozeolite.
Fig. 2 Renal cortex from broilers a in zero group (group 0):
glomerular and the tubular basement membrane are normal; HE
(haematoxylin and eosin) 940 (microscope magnification); b in
control group (group 1). Dystrophic changes in the kidney tubules
epithelium (arrow). HE 940
Fig. 3 Liver from broilers a in zero group (group 0): normal
histological liver structure. HE 920; b in control group (group 1):
oedema and vacuolization of the cytoplasm of hepatocytes. HE 920
Radiat Environ Biophys (2014) 53:151–157 155
123
The histopathological changes observed in kidney, liver,
and small intestine from birds of the control group (group
1) demonstrate the toxic effects of uranium. In case of oral
contamination, the digestive tract is the entry way of ura-
nium into the organism, and accordingly, changes were
indeed observed in the small intestine. In contrast to the
present study, however, no gastrointestinal effect was
observed in rats exposed to uranyl nitrate hexahydrate in
drinking water at 40 mg/kg per day for 28 days, or in
rabbits exposed to uranyl nitrate hexahydrate in drinking
water at up to 600 mg/L for 91 days (Gilman et al. 1998a,
b, c).
Physiological characteristics of the kidneys to reabsorb
and accumulate divalent metals make kidney as target
organ of heavy metals intoxication (Vicente-Vicente et al.
2010; Kurttio et al. 2002). Accordingly, in kidneys, dys-
trophic changes in the epithelium of the tubules were
observed here, which was confirmed by other authors after
acute, subacute, and chronic uranium exposures (Vicente-
Vicente et al. 2010; Gilman et al. 1998a, c; Ozmen and
Yurekli 1998; Haley et al. 1982). In rats, under chronic
exposure with UN, histopathological lesions were observed
primarily in the liver, thyroid, and kidney (Gilman et al.
1998c), even though the uranium levels in the liver were
below detection. In the present study, in broiler liver, the
uranium concentration was detectible and histopathological
changes were found in the form of oedema and cytoplasmic
vacuolation of hepatocytes. Minimal lesions in kidney and
liver of the rats receiving uranyl acetate orally have been
detected by Domingo et al. (1987).
In groups 2 and 3, where the broilers received adsor-
bents immediately after UN contamination, no histopa-
thological lesions were observed in the investigated organs
and tissues. Thus, the uranium concentrations that were
detected in these organs did not cause any pathological
effects. In broilers that received only adsorbents (groups 4
and 5), no histopathological changes were observed in any
of the investigated organs, suggesting that use of the
investigated adsorbents is safe.
Conclusion
Because ingestion is the main route of the contamination of
broilers with toxic substances, their feed must be safe, to
make sure that none of these toxic elements can enter the
human food chain. After years of successful field testing,
many feed suppliers and end-users have included a feed
additive (of only 0.5–5 %) in their feed supply programme.
Note that animals in intensive production are kept in indoor
facilities under strictly controlled environmental condi-
tions. Mineral supplements, such as monocalcium and
dicalcium phosphate, are a major source of uranium in
animal feed, and therefore, continuous monitoring of these
nutrients is necessary. The chickens’ ingestion of dicalcium
phosphate is about 2.93 g daily, which corresponds to
7.23 Bq/day due to 238U (Arruda-Neto et al. 1997). In order
to determine the possibility to protect broilers with or-
ganobentonite and organozeolite in case of alimentary
contamination with uranium, a rather high concentration of
uranyl nitrate was used in the present study.
The results obtained in the present study show that
uranium in broilers primarily accumulates in kidney and
liver compared with brain and muscles. In animal nutrition,
adsorbents are used as feed additives for elimination of
various toxins and improvement of meat production. In all
situations where there may be a risk of alimentary con-
tamination with uranium, the use of organobentonite and
organozeolite is therefore recommended. Currently, other
types of adsorbents are also studied, and the results will be
published once available.
Acknowledgments This work was supported by the Ministry of
Education, Science and Technological Development of Serbia, in the
frame of Project Nos. 31003 and 34103.
Fig. 4 Small intestinal from broilers a in zero group (group 0):
normal structure of intestinal villi. HE 910; b in control group (group
1): fusion, shortening, and necrosis of small intestinal villi. HE 910
156 Radiat Environ Biophys (2014) 53:151–157
123
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