A review: Natural and artificial radionuclides and radiation hazard parameters in the soil of mountain regions in Serbia

This review paper discusses the content of natural (40K, 238U, 226Ra, and
 232Th) and artificial (137Cs) radionuclides in the soil of the mountains of
 Maljen, Tara and Kopaonik in the Republic of Serbia over 2002-2015. In
 addition, the paper gives radiation hazard parameters, i.e., radium
 equivalent activity, absorbed dose rate, annual effective dose equivalent,
 external hazard index, annual gonadal dose equivalent, and excess lifetime
 cancer risk outdoors that we calculated from the obtained content of the
 natural radionuclides in the soil samples. We compared the parameters to
 previously published results for different parts of the country and looked
 into the radioecological status of the investigated areas.


Introduction
Ionizing radiation and radioactivity are an integral part of the environment. Natural radionuclides, characterized by a long half-life, are present in rocks, minerals and soil. These primordial terrestrial radionuclides are divided into two groups.

Materials and Methods
The soil samples were collected over 2002-2015 in the areas of the mountains of Maljen, Tara, and Kopaonik ( Figure 1). The mountains of Tara and Kopaonik are nature parks and thus all their reserves are under the state protection. The studied areas present some of favorite tourist destinations for sports and recreation. The soil samples were collected from the surface down to a depth of 20 cm. In the laboratory, the samples were crushed, dried at 105 °C , sieved, homogenized and put into Marinelli beakers (0.5 ml and 1 l). All samples were hermetically sealed and stored for 21 days to ensure equilibrium between 226 Ra and its daughters.
We used gamma-ray spectrometric measurements on High Purity Germanium detectors (ORTEC and Canberra), with a relative efficiency of 18%, 20% and 30%, and an energy resolution of 1.85 keV (1332.5 60 Co), to determine the activity concentrations of the investigated radionuclides.
The analysis of each measured gamma-ray spectrum was performed by a software program GAMMA VISION-32. All obtained results are expressed as (mean ± standard deviation).
The activity concentrations of 40 K and 137 Cs were derived directly from their 1460.8 keV and 661.66 keV gamma energies, respectively. For other radionuclides, we included the following steps in the analysis: -We assumed equilibrium conditions between the parent nuclide 238 U and its daughters, 234 Th (63.2 keV) and 234m Pa (1001 keV).
-We obtained the 226 Ra activity concentration from the gamma energy of 186.1 keV corrected for 235 U, and 226 Ra daughters in equilibrium, 214 Bi (609.3 keV, 1120.2 keV and 1764.5 keV) and 214 Pb (351.9 keV).
-We used three photo peaks of 228 Ac (338 keV, 911.2 keV, and 969 keV) for the activity concentration of 232 Th.

Radium equivalent activity
Since the distribution of 226 Ra, 232 Th, and 40 K in the soil is not uniform, we used radium equivalent activity (Ra eq ) to compare the specific activity of materials with different amounts of 226 Ra, 232 Th, and 40 K. The definition of Ra eq is based on an assumption that 370 Bq/kg of 226 Ra, 259 Bq/kg of 232 Th, and 4810 Bq/kg of 40 K produce the same gamma dose rate. We calculated Ra eq using ( Beretka and Mathew, 1985): Ra eq (Bq/kg) = C Ra + 1.43C Th + 0.077C K (1) where C Ra , C Th , and C K are the activity concentrations of 226 Ra, 232 Th, and 40 K (in Bq/kg), respectively.

Absorbed dose rate
We converted the mean activity concentrations of 226 Ra, 232 Th, and 40 K into absorbed dose rate ( ) using conversion factors under an assumption that all decay products of 226 Ra and 232 Th are in equilibrium with their precursors (UNSCEAR, 2008): (nGy/h) = 0.462C Ra + 0.604C Th + 0.042C K (2)

Annual effective dose equivalent
To estimate the annual effective dose equivalent (AEDE), the conversion coefficient from the absorbed dose in the air to the effective dose must be considered. We used the absorbed dose rate data (Eq. 2), adopted the conversion factor of 0.7 Sv/Gy (UNSCEAR, 2008), and assumed that on average, people in Serbia spend 20% of their time outdoors, and thus obtained: External hazard index Beretka and Mathew (1985) defined the external hazard index (H ex ) as: For H ex values less than one, the radiation hazard is insignificant. The external hazard index equal to one corresponds to the upper limit of radium equivalent activity (370 Bq/kg).

Annual gonadal dose equivalent
We used the following equation (Arafa, 2004) to calculate annual gonadal dose equivalent (AGDE) to the population arising from the presence of naturally occurring radionuclides 226 Ra, 232 Th, and 40 K in the soil: AGDE (µSv/y) = 3.09C Ra + 4.18C Th + 0.314C K (5)

Excess lifetime cancer risk outdoors exposure
Excess lifetime cancer risk outdoors exposure (ELCR outdoor ) gives the probability of developing cancer over a lifetime at a given exposure level. We calculated ELCR outdoor using (UNSCEAR, 2000;ICRP, 1990): where DL is the duration of life (70 years average) and R f is the risk factor (in Sv), i.e. fatal cancer risk per sievert. For stochastic effects, we used R f = 0.05 mSv for the whole population (ICRP, 2007).

Results and Discussion
Mountains are complex ecological and very sensitive ecosystems. The characteristics of mountain ecosystems vary depending on altitude, climate conditions, geological characteristics, biomes, water flows, etc. Any changes in biotic or abiotic elements can cause an interruption in the ecosystem.
Specific activities of natural radionuclides in the soil depend on geological and geographical characteristics of a given region. In the mountain regions of Maljen, Tara and Kopaonik, serpentine soils are present. Characteristics of this soil type are extremely stressful for plant growth (Kostić et al., 1998;Vicić et al., 2014) -since they are susceptible to erosion, and often shallow and rocky, vegetation is usually sparse and poor (Tatić and Veljović, 1991;Jakovljević et al., 2001;Stevanović et al., 2003). The geological background of Mt. Kopaonik is represented by granites, serpentinites, slates, marbles, andesites, and limestones. The differences in geological characteristics between the investigated mountains also affect the content of radionuclides in the soil, which will be summarized below.
The presence of anthropogenic radionuclides, such as 137 Cs, is mainly a consequence of the nuclear accident in Chernobyl in 1986. The ensuing soil contamination was a result of a number of factors, such as a distance from the accident location, rainfall index, and soil characteristics (UNSCEAR, 2000).

The mountain of Maljen
Maljen is a mountain located in the west of Serbia. It spreads in the east-west direction for approximately 25 km. The highest peak is Kraljev sto (elevation -1100 m a.s.l.). The geologic structure of Mt. Maljen consists of ultrabasic rocks (peridotites and serpentinized peridotites). Magnesium oxide present in the soil makes this area unfavorable for plant survival (Tatić and Veljović, 1991).
The soil samples from Mt. Maljen were collected at four altitudes over 2002(Mitrović et al., 2009. Table 1 gives the gammaspectrometric results. The mean activity concentrations of the radionuclides on Mt. Maljen were 254 Bq/kg for 40 K, 33 Bq/kg for 238 U, 33 Bq/kg for 226 Ra, 29 Bq/kg for 232 Th, and 97 Bq/kg for 137 Cs (Table 1). According to the UNSCEAR report (2000), the world average activity concentrations in the soil are 420 Bq/kg, 33 Bq/kg, 32 Bq/kg, and 45 Bq/kg for 40 K, 238 U, 226 Ra, and 232 Th, respectively. Our results showed that the content of natural radionuclides at lower altitudes was above the world average values. However, as altitude increased, the activity of natural radionuclides in the soil decreased by a factor of 4-6. This finding can be explained by different geochemical characteristics of the soil at different altitudes, and by the fact that soils in lower areas are generally subject to agro-technical measures and use of fertilizers based on phosphate and potassium (Bolca et al., 2007).
In contrast to this finding, there was a several-fold increase in the 137 Cs activity concentration from an altitude of 200 m (19 Bq/kg) to 1100 m (259 Bq/kg), which could be explained by an increased amount of rainfall at higher altitudes after the Chernobyl accident. Contamination of the soil with 137 Cs is a starting point for transfer of this radionuclide to plants and onwards through the food chain. Its presence was detected in mosses, mushrooms, game meat and milk of animals from the test sites (Mitrović et al., 2009). The highest content of 137 Cs was found in sheep meat (45.8 Bq/kg) and goat milk (24.1 Bq/kg) sampled from animals grazing at 1000 m a.s.l.
Based on the measured activity concentrations of natural radionuclides in the soil (Table 1), we calculated radiation hazard parameters for Mt. Maljen (Table 2). The radium equivalent activity was below 170 Bq/kg (Table 2). For comparison, a value of 370 Bq/kg is the criterion limit for Ra eq in building materials (Beretka and Mathew, 1985), and its corresponding annual effective dose equivalent is 1 mSv, which, in turn, represents the dose limit for the general population. Further, the locations at lower altitudes showed an absorbed dose rate higher than the world average of 59 nGy/h (UNSCEAR, 2008). The calculated annual effective dose equivalents at lower altitudes were also higher than the world mean of 70 µSv/y (UNSCEAR, 2000), while the annual gonadal dose equivalent values were lower than the level of 1 mSv/y, which is a recommended limit by the International Commission on Radiological Protection (2007) for the general public. According to UNSCEAR (2000), the gonads, bone marrow, and bone surface are considered as the organs of importance since they are active. The probability of cancer incidence in a population during the lifetime due to an exposure to natural radionuclides (ELCR outdoor ) in the soil at lower altitudes was slightly higher than the world average value of 0.29x10 -3 (UNSCEAR, 2000), but the mean ELCR outdoor value was lower (0.20x10 -3 ).  Beretka and Mathew (1985); b UNSCEAR (2008); c UNSCEAR (2000); d ICRP (2000); e ICRP (2007); f UNSCEAR (2000).
As a summary of the above results, the obtained external hazard index for altitudes above 200 m was less than one (Table 2), i.e., less than the limit recommended by ICRP (2000), implying that the investigated area is radioecologically safe to use.

The mountain of Tara
Farther west and south from Maljen is the mountain of Tara. It covers an area of 250 km 2 and geologically belongs to the Dinarides. The highest peak is Kozji rid (1591 m a.s.l.). The climate is distinctly mountainous, and the winter period is cold with plenty of snow. The soil is mainly uncultivated, dominated by the forest ecosystem (80%). The soil is composed of various limestones (MgCO 3 , CaCO 3 ) and shale (Si) rocks. Forests mainly consist of beech, spruce and fir. Table 3 gives the activity concentrations of radionuclides in the soil of Mt. Tara, while Table 4 shows the calculated radiation hazard parameters. In all soil samples, the activity concentrations of natural radionuclides were below the world average (Table 3), except the altitude of 1100 m where the content of 238 U, 226 Ra, and 232 Th was higher (Djurić et al., 1996;Mitrović et al., 2009;Rakić et al., 2014).
The obtained results showed that the level of natural radionuclides' activity in noncultivated soil of the mountains of Maljen and Tara was similar (Tables 1 and 3). Popović et al. (2009) reported that the mean activities of 226 Ra, 232 Th, and 40 K in the soil from Mt. Tara collected over a period of 1983-1993 were 42 Bq/kg (22-92 Bq/kg), 46 Bq/kg (24-69 Bq/kg) and 613 Bq/kg (356-1126 Bq/kg), respectively. Differences in radionuclides' content in the soil are a consequence of soil type. For example, higher activity concentrations of 40 K, 238 U, and 232 Th can be found in shale soils than in the soil composed mainly of limestone rocks (Djurić et al., 1996). The values of radiation hazard parameters on all sample locations were below the recommended maximum values (Tables 2 and 4). The exception again was the soil collected at 1100 m a.s.l. where absorbed dose rate ( ), annual effective dose equivalent (AEDE) and excess lifetime cancer risk (ELCR outdoor ) were about 1.2fold higher than the recommended levels. Anthropogenic 137 Cs was also detected in the soil (Table 3). In 1991, five years after the Chernobyl accident, the activity concentration of this radionuclide in the surface layers was significantly lower in limestone soils (88 Bq/kg) than in shale soils (462 Bq/kg) (Djurić et al., 1996;Popović et al., 1996;Popović and Spasić, 2006;Popović et al., 2009), and it is still present in the soil (Rakić et al., 2014).
Transfer of this radioisotope from the soil to plants strongly depends on the soil type and characteristics of the plant species. The study by Mitrović et al. (2009) showed that radiocesium was present in the food chain: soil-plants-animals. Between 2002 and 2007, the medium activity concentration of 137 Cs was 5.1 Bq/kg in the grass, 2.9 Bq/kg in sheep milk, and 6.5 Bq/kg in sheep meat. Small ruminants, such as sheep and goats, are good bioindicators for radiocesium contamination of the environment, because the ingestion of soil can be a major source of radiocontamination for free-grazing ruminants (Assimakopoulos et al., 1993).
After the Chernobyl accident, the activity concentrations of 134 Cs and 137 Cs in herbal teas from Serbia reached 5000 Bq/kg (Petrović, 2010), but results obtained 28 years later showed a significant reduction in the 137 Cs concentration in teas from mountain regions (Mitrović et al., 2014). In herbal teas collected from Mts Maljen and Tara, high activity concentrations of 137 Cs (77 Bq/kg and 73 Bq/kg, respectively) were observed in plant species V. myrtillus (bilberry). Some organisms, e.g. bilberry but also mosses, mushrooms and game, are good bioindicators of environmental pollution with radiocesium (Grdović et al., 2010;Mitrović et al., 2013Mitrović et al., , 2016aRakić et al., 2014).

The mountain of Kopaonik
The south-western part of Serbia is dominated by Kopaonik, which is one of the highest mountain ranges in the country. It extends in the northwest-southeast direction for 80 km, and has a width of around 40 km in the middle. The highest peak is Pančićev vrh (elevation -2017 m a.s.l.). The Kopaonik National Park covers an area of about 12000 ha, and it is a very popular tourist destination. The climate is subalpine with the annual average precipitation rate up to 1000 mm.
The results of gamma spectrometric determination of radionuclides in the soil collected on nine locations at Mt. Kopaonik during 2013-2016 (Mitrović et al., 2014(Mitrović et al., , 2016Džoljić et al., 2017) and radiation hazard parameters are presented in Tables 5 and 6, respectively.
The mean activity concentrations of radionuclides at Mt. Kopaonik were 723 Bq/kg for 40 K, 78 Bq/kg for 238 U, 75 Bq/kg for 226 Ra, and 76 Bq/kg for 232 Th (Table 5), which is two-fold higher than the world average activity concentrations of these radionuclides in the soil (UNSCEAR, 2000). The obtained differences between the results can be attributed to the geological structure at the sampling locations. For example, at Lisina, a sampling site with an elevation of 1300 m, the geological period belongs to the Palaeozoic, and rocks are comprised of granite, granodiorite and quartz, known for its high content of radionuclides. On the other hand, higher up at Gobelja, metamorphic rocks (crystalline shales) are found. Furthermore, the results showed an increase of natural radionuclides 238 U, 226 Ra, and 232 Th with altitude. An exception was the Đerekare location where somewhat higher radionuclide content was detected. Mt. Kopaonik was under a prolonged attack during the NATO action against the Federal Republic of Yugoslavia in 1999. The bombing led to the destruction of the terrain and disruption of the forest ecosystem (UNEP/UNCHS BTF, 1999). The gammaspectrometric analysis of the soil taken from the Gobelja location where severe bombing activity took place, showed that activity concentrations of 238 U and 226 Ra were in equilibrium, implying a natural origin of the radionuclides (Mitrović et al., 2016). This study, however, did not investigate soil samples from the bombing craters. The average activity concentration of 137 Cs (47 Bq/kg) on Mt. Kopaonik was two-fold lower than on Mt. Maljen (97 Bq/kg) and Mt. Tara (98 Bq/kg). These variations can be explained by a different deposition of Chernobyl radiocesium, differences in forest type (Koarashi et al., 2016), physical and chemical properties of soils (Korashi et al., 2012), as well as the sedimentary structure of this location (Mitrović et al., 2016).
The radium equivalent activity in the soil was mostly below 370 Bq/kg ( Table 6). The exceptions were the locations of Lisina and Pančićev vrh where Ra eq exceeded this limit (415 Bq/kg and 458 Bq/kg, respectively). As a consequence of the high activity concentration of natural radionuclides in the soil, the values of absorbed dose rate ( ) and annual effective dose equivalent (AEDE) were higher than the global average of 58 nGy/h (UNSCEAR, 2008) and 70 µSv/y (UNSCEAR, 2000), respectively. However, at lower altitudes, in Brus and Jošanička banja, these two parameters were below the global means (Table 6). In all locations except Lisina and Pančićev vrh, the annual gonadal dose equivalent (AGDE) values were lower than 1 mSv/y. Similarly, the average value for the external hazard index (H ex ) was less than one (Table 6). Still, values higher than 1 were recorded in Lisina and Pančićev vrh. The probability of cancer incidence in a population during the lifetime due to an exposure to natural radionuclides in the soil (ELCR outdoor ) at higher altitudes was higher than the world average value of 0.29x10 -3 (UNSCEAR, 2000).
In addition to the natural radionuclides, the artificial 137 Cs was detected in the soil, grass, spruce, cow milk and moss samples from Mt. Kopaonik (Mitrović et al., 2016;Džoljić et al., 2017). In the soil, the lowest activity concentration of 137 Cs was recorded in the area of Pančićev vrh, and the maximum in Jošanjička banja (Table 5). A decrease in the 137 Cs content in the soil with an increasing altitude is probably due to stronger soil erosion at higher altitudes (Nešić et al., 2009).

Radionuclides in the soil of Serbia
Determination of radionuclides' content in the soil has been a subject of many studies with the purpose of risk assessment and protection of the humans, nonhuman biota and the environment from radioactive pollution. Studies performed by Momčilović et al. (2010) andTanič et al. (2014) in the area of an abandoned uranium mine (Grabovnica mine) at Mt. Stara Planina showed that the terrestrial gamma dose rate due to 238 U (31-237 Bq/kg), 232 Th (6-109 Bq/kg), and 40 K (64-977 Bq/kg) in the soil was two-fold higher than that of the surrounding area. In the vicinity of the mine compounds, the radionuclide content was within the usual range for this mountain or slightly higher. In a part of Mt. Stara Planina farther south, at sampling points of Smilovci, Smilovsko jezero, Kamenica, and Gornji Krivodol, the activity concentrations of natural radionuclides in the soil were lower and ranged between 393 Bq/kg and 543 Bq/kg, 29 Bq/kg and 57 Bq/kg, 25 Bq/kg and 51 Bq/kg, and 28 Bq/kg and 69 Bq/kg for 40 K, 238 U, 226 Ra, and 232 Th, respectively (Vranješ et al., 2016). Apart from the natural radionuclides, 137 Cs was also detected in the environment of Mt. Stara Planina, i.e. in the soil, mosses and medicinal plants (Vranješ et al., 2016).
It is also worth noting that many studies have been conducted to determine the uranium content in various environmental samples from locations where depleted uranium ammunition was used during the NATO bombing in 1999 (Miljević et al., 2001;Esposito et al., 2002;Popović et al., 2008Popović et al., , 2010Sarap et al., 2014). These locations are now included as an integral part of the monitoring program at the territory of the Republic of Serbia (Official Gazette RS, 2010).

Conclusion
Determining natural radioactivity in the soil is a necessary step in the evaluation of the radiation hazard parameters. The average values of activity concentrations of 238 U, 226 Ra and 232 Th at Mts Maljen and Tara were within the range of values obtained for other parts of Serbia and worldwide (UNSCEAR, 2008). However, the measured concentrations were approximately two-fold higher at Mt. Kopaonik.
The radiation hazard parameters obtained for Mts Maljen and Tara were similar to values reported for other parts of Serbia implying that the investigated areas were radioecologically safe for humans.
Mt. Kopaonik showed the average values of absorbed dose rate, annual effective dose equivalent and external hazard index two-fold higher than at Mts Maljen and Tara. At two particular locations, Lisina and Pančićev vrh, the values of absorbed dose rate and annual effective dose equivalent were about four-fold higher than those on Mts Maljen and Tara. External hazard index was also higher than one, indicating an elevated radiation hazard.
The values of annual gonadal dose equivalent, as a measure of the genetic significance of the annual dose equivalent received by the population, were less than 1 mSv in the investigated areas, except on Mt. Kopaonik, locations Lisina and Pančićev vrh, where this parameter was higher than 1 mSv.
The calculated excess lifetime cancer risk implied that the chance of contracting cancer for residents at the study area of Mts Maljen and Tara was below the global average of 0.29x10 -3 (UNSCEAR, 2000). However, the probability of cancer incidence on Mt. Kopaonik was higher than the world average.
Anthropogenic 137 Cs was detected in all investigated mountain regions of Serbia.