Open access peer-reviewed chapter - ONLINE FIRST

Radionuclide Contamination as a Risk Factor in Terrestrial Ecosystems: Occurrence, Biological Risk, and Strategies for Remediation and Detoxification

Written By

Peter Ostoich, Michaela Beltcheva, Jose Antonio Heredia Rojas and Roumiana Metcheva

Submitted: February 1st, 2022 Reviewed: March 11th, 2022 Published: April 21st, 2022

DOI: 10.5772/intechopen.104468

The Toxicity of Environmental Pollutants Edited by Daniel Dorta

From the Edited Volume

The Toxicity of Environmental Pollutants [Working Title]

Dr. Daniel Dorta and Prof. Danielle Palma De Oliveira

Chapter metrics overview

20 Chapter Downloads

View Full Metrics


Radionuclide contamination poses serious hazards for terrestrial ecosystems. Beyond the readily apparent damage to the biota at high doses, low doses of ionizing radiation produce stochastic effects: mutation, carcinogenesis, and genomic instability. The proposed chapter is a review of the biological and ecological effects of radionuclides. The authors discuss, beyond the Chernobyl accident, other contamination events. The review includes the biological and ecological effects of the three principal technogenic contaminants in terrestrial ecosystems: Cs-137, Sr-90, and I-131. Ecological risks to terrestrial small mammals are assessed in detail. In addition, the chapter provides some of the lesser-known methods of remediation and detoxification, including the use of modified natural zeolites as environmental remedies and bio-sorbents. Presented herein is little-known information on environmental protection against radioactive contamination.


  • radionuclides
  • radioecology
  • contamination
  • remediation
  • detoxification
  • zeolites

1. Introduction: the essence of radionuclides—emission types and biological effects

Radionuclides are unstable isotopes of different chemical elements. Usually, this instability is due to excess energy in the atomic nucleus, leading to the release of particles with different energies in a process called radioactive decay. Natural radionuclides emit three types of radiation: alpha (α), beta (β-), and gamma (γ). Of these types, α-particles have the strongest biological effects, causing 20 times more biological damage than an equivalent dose of β- or γ radiation [1, 2]. While α- and β-particles tend not to penetrate into matter, γ-radiation, especially at the higher end of the energy spectrum, penetrates deep into living and non-living matter. This means that, when considering the biological and ecological effects of radionuclide contamination, α- and β-emitters are only relevant if incorporated into living organisms. In contrast, γ-emitters are relevant as both internal and external components of the total absorbed dose. In the context of anthropogenic contamination, it needs to be taken into account that some of the man-made radionuclides emit other types of radiation. For example, radioisotopes used in medical PET scans such as 18F, 11C, 13N, 15O are positron (β+) emitters. Other, more exotic man-made radionuclides such as Californium-252 (252Cf) are capable of spontaneously emitting neutrons. Both positron and neutron emitters require specific equipment for handling and detection of the radiation sources [1]. Some radionuclides emit multiple types of particles. The anthropogenic radionuclide 137Cs emits β particles at two energies: 511 and 1173 kiloelectronvolts (keV), and γ-rays at 32 and 661.6 keV [3, 4].

The biological effects of radionuclides are mainly due to the emitted ionizing radiation (IR). IR interacts with biomolecules directly by damaging them or indirectly—by producing reactive oxygen species (ROS), which in turn damages biomolecules. According to the paradigms of classical radiobiology, the principal target of IR on a cellular level is genomic DNA—it can be damaged directly or indirectly, leading to cell cycle arrest and an activation of DNA repair systems, followed by recovery, cell death, or mutagenesis [5, 6]. Sparsely ionizing radiations such as β- particles and γ-rays cause around 70% of DNA damage indirectly through ROS, while densely ionizing radiations, such as α-particles and high-energy cosmic particles, cause only about 30% of the biologically significant damage indirectly [7]. Researchers have elucidated the biological effects of high and medium doses of radiation. Nevertheless, biological effects at low doses remain insufficiently understood and a subject of much debate [18]. Currently, radiation risk is extrapolated linearly to the low doses by using the Linear Non-Threshold (LNT)mathematical model [1, 9]. However, other hypotheses include radiation hormesis, which is the idea that small doses of radiation are beneficial [10], and low-dose hypersensitivity, which is the assumption that low doses of radiation are more mutagenic because they do not activate DNA repair systems [11]. While radiation hormesis has been well researched recently [10], it has still not been taken into account in radiation protection calculations, where every minimal dose of radiation is assumed to carry a small but non-negligible risk [12]. On the other hand, the low-dose hypersensitivity hypothesis is supported by recent studies, raising questions about the validity of current assumptions in radioprotection [13]. Living organisms tend to display different radiation sensitivity. Mammalian species are very sensitive to radiation, while insects tend to be comparatively radioresistant. The champion of radiation resistance is the bacterium Deinococcus radiodurans, which can withstand an acute dose of 5000 Gray with almost no loss of viability. Similarly, tardigrades can withstand 5000 Gray with 50% loss in viability (LD50 = 5000 Gy). For comparison, the LD50 for humans is around 6 Gray, for mice around 6.4 Gray, and for goats only around 2.4 Gray [14].

A significant concern in radionuclide-contaminated areas arises from the process of bioaccumulation. Similar to other chemical elements from their respective groups, radioisotopes are incorporated preferentially into different target organs and tissues. Thus, 137Cs, a chemical analogue of potassium, is preferentially accumulated into nerve and muscle tissue. 90Sr, an analogue of calcium, has a very strong affinity for bone and hematopoietic tissue. Some of the properties of the three most environmentally significant anthropogenic radionuclides are presented below (Table 1).

RadionuclideSymbolHalf-life (λ)Emitted radiationTarget tissues and organsBiological effects
Cesium-137137Cs30.17 yearsβ-(511, 1173 keV), γ (32, 661.6 keV)Nerve, muscleDifferent cancers
Strontium-9090Sr28.8 yearspure β-(546 keV)BoneBone cancer, leukemia
Iodine-131131I8.02 daysβ-(333.8, 606.3 keV), γ (364.5, 636.9 keV)Thyroid glandThyroid cancer

Table 1.

The most significant anthropogenic radionuclides and their biological effects (data adapted from [3, 4]).

As evident from the table, the most significant environmental contaminants of the above are 137Cs and 90Sr due to their long half-lives and persistence in nature. 131I was only a very significant contaminant in the first year following the Chernobyl accident, causing ~4000 excess thyroid cancers in the most significantly affected populations of Russia, Belarus, and Ukraine [15].


2. Radionuclide occurrence in nature: natural and anthropogenic sources

Natural radioactivity, including external terrestrial γ radiation, internal α-, β-, and γ-radiation from naturally occurring radionuclides, cosmic radiation, and exposure to radon (222Rn) and thoron (220Rn) and their radioactive progeny molecules, accounts for ~95% of the annual radiation dose for the terrestrial biota [1]. The global annual dose for an average person is 3.6 millisieverts/year (mSv/a), of which 82% is due to natural radiation exposure, around 15% is due to medical exposure, and only about 0.8% is due to anthropogenic contamination of the environment. Natural radioactivity has been a subject of concern for decades. Globally, there are areas with increased natural radiation, often due to thorium (232Th) deposits in the form of monazite rocks. Two such areas are Guarapari, Brazil, and the state of Kerala in southern India. The area of Ramsar, Iran, has enormously increased natural radioactivity due to radioactive hot springs containing 222Rn and its progeny. Although annual doses in these areas reach an average of 35–40 mSv/a, compared to 3.6 mSv/a average in Europe and 2.5 mSv/a in Bulgaria, modern biomedical studies report no excess cancer risk, leading researchers to believe that a 10-fold increase in natural radioactivity is harmless [16].

In contrast, environmental contamination by anthropogenic radionuclides without doubt creates serious risks. The Chernobyl accident is the most prominent example of environmental damage due to technogenic sources, although it is not the only one; Chernobyl caused significant chronic morbidity and mortality in people and enormous damage to the environment and economies in Europe. This is mostly due to 131I, 137Cs, and 90Sr, and their tendencies for bioaccumulationand biomagnificationin terrestrial ecosystems [17]. Although the Chernobyl accident is the best-known example, there are many other significant contamination events in the period 1945–2011 (Table 2).

Accident site, yearCountryINES scaleDateAccident typeRadioactivity released to the atmosphere, PBqIodine-131 released, PBqCesium-137 released, PBq
Chernobyl, 1986USSR726.04.1986Reactor meltdown12,000176085
Fukushima, 2011Japan711.03.2011Reactor meltdown630<380<37
Mayak (Chelyabinsk-40), 1957USSR629.09.1957Nuclear waste explosion1850Not knownNot known
Chalk River, 1952Canada512.12.1952Reactor meltdown0.3Not knownNot known
Windscale, 1957UK510.10.1957Reactor fire1.60.70.02
Simi Valley, 1959USA526.07.1959Partial reactor meltdown>200Not knownNot known
Beloyarsk, 1977USSR51977Partial reactor meltdownnot knownNot knownNot known
Three Mile Island, 1979USA528.03.1979Partial reactor meltdown1.6<0.007Not known

Table 2.

The most significant radioactive release accidents, their IAEA INES severity scale, and radioactivities released to the environment (data from [18]).

One aspect evident from the table is that, according to atmospheric radioactivity released, the Chernobyl accident exceeds all other INES scale 5–7 accidents combined. At the same time, during this accident, only about 30% of the core radioactivity was released, suggesting that a full-blown reactor explosion can cause even greater damage to the environment. Another noteworthy peculiarity is that most reactor accidents so far occurred either with new or experimental power plants (Chernobyl, Chalk River, Simi Valley, Beloyarsk) or military reactors (windscale). Nevertheless, the Fukushima accident in 2011 presents a new precedent—the reactors in the plant were old, nearing the end of their design life. Since this is true for many of the currently operating reactors, this presents a new, threatening perspective. Aging, crumbling nuclear infrastructure may present a new, unmitigated radiation hazard in the future.


3. Radionuclides and nature: significant risks and unknowns

Some of the risks to ecosystems posed by radionuclide contamination are well understood. They include, at high doses >1 Gray acute dose, teratogenesis in developing embryos, stunted plant growth, and visible damage to the flora and fauna. These are deterministic effects, and they occur definitely after exposure to strong doses of ionizing radiation and are dose dependent (Figure 1).

Figure 1.

Deterministic effects of ionizing radiation: Dead pine trees near Chernobyl, Ukraine in 1990 (left, taken from [19]), and experimental radiation teratogenesis in mouse embryos (right, photograph by Dr. Roberts Rugh, taken from [1]).

As shown in Figure 1, pine trees are very radiosensitive; they can serve as a bioindicator of severe radioactive contamination at doses exceeding 3 Sv acute exposure [19]. The other depicted deterministic effect is teratogenesis in pregnant mammalian species. At doses exceeding 1 Sv acute in uteroexposure, the number of resorbed fetuses decreases, and so does the number of offspring born with malformations [1].

Perhaps more worrying are the stochastic effects, which occur with a small probability even at low radiation doses. These include radiation mutagenesisand, as a consequence of it, radiation carcinogenesis[1, 12]. Based on data from experiments with specially bred laboratory mice and results from the radiobiological monitoring of humans, exposed to γ-rays and neutrons during the bombings of Hiroshima and Nagasaki, it is estimated that the doubling dose of radiation-induced mutagenesis is 1 Gy. This means that an acute exposure to 1 Gy of γ-rays doubles the spontaneously occurring rate of mutation [20, 21]. Nevertheless, this perspective is being challenged. For example, Belarussian researchers observed transmission of chromosomal damage in the progeny of wild rodents from the vicinity of Chernobyl, indicating genomic instability[22]. An international team observed a higher mini- and microsatellite mutation rate in the children of Chernobyl liquidators [23]. Both of these findings support the theory that even low doses of radiation can be harmful to the biota, as well as current and future generations of humans. Another, more recent venue of research with significant progress is the radiation-induced bystander effect (RIBE) phenomenon, in which non-irradiated cells show similar cytotoxicity and genetic damage to their irradiated neighbors [24, 25]). The results from bystander effect studies generally support the theory of low-dose hypersensitivity and highlight possible molecular mechanisms for increased radiation risks in the low-dose range [24, 25]). Radiation risk is still to be taken very seriously, and every effort should be made to keep radioactive contamination of ecosystems to a minimum.


4. Estimation and appraisal of radioactive contamination and its effects on the components of terrestrial ecosystems

Radioecology is a sub-discipline of ecology concerning the presence and effects of radioactivity on Earth’s ecosystems. Some of the risks of ionizing radiation were known in the early twentieth century. Nevertheless, the discipline de factostarted developing in the period following World War II and the bombings of Hiroshima and Nagasaki [26]. The advent of the Atomic Age not only gave the impetus to study radiation effects on ecosystems, but also gave them powerful tools in the form of radioactive isotopes, which could be used as tracers [26, 27]. Initially, studies were carried out by the US Atomic Energy Commission (AEC) at several sites crucial to the Manhattan Project, principally Oak Ridge, Tennessee, and Hanford, Washington; many of these studies dealt with the cycling with biogenic carbon, phosphorus and oxygen through ecosystems and were conducted with radioactive tracers (14C, 32P, and others) [27]. In parallel, studies were conducted in the former USSR in the closed town of Ozyorsk (Chelyabinsk-40). Some studies were conducted in secret; most of them dealt with dispersal and deposition of bomb radionuclides and with the bioaccumulation of radioactivity in crop plants and farm animals [28, 29, 30].

Without a doubt, the most significant contamination event in the context of terrestrial ecosystems is Chernobyl. It is estimated that, at the time of the accident, around 10% of the total core radioactivity was released, including 100% of all noble gases and around 30% of volatile atoms including 30% of the core radiocesium (134Cs and 137Cs), 55% of the core 131I, and ~ 45% of the core 132Te. Less volatile radionuclide species such as radiostrontium (89Sr and 90Sr) were also released in smaller amounts (~5% of core inventory), as well as <3.5% of the core transuranic nuclides (neptunium, plutonium, curium) [31, 32]. The core inventories and releases are summarized in Table 3.

Chernobyl core inventories at the time of accidentRadioactive release
RadionuclideSymbolHalf-life (λ)Core activity, PBq% core activityReleased, PBq
Krypton-85*85Kr10.76 years3510035
Xenon-133*133Xe5.3 days65001006500
Iodine-131131I8.02 days3200551760
Cesium-134134Cs2.0 years1803054
Cesium-137137Cs30.17 years2803085
Tellurium-132132Te78 hours2700451150
Strontium-8989Sr52.0 days23005115
Strontium-9090Sr28.8 years200510
Barium-140140Ba12.75 days48005240
Zirconium-9595Zr1.4 hours56003.5196
Molybdenum-9999Mo65.9 hours48003.5168
Ruthenium-103103Ru39.26 days48003.5168
Ruthenium-106106Ru1.0 year21003.573
Cerium-141141Ce32.5 days56003.5196
Cerium-144144Ce284.9 days33003.5116
Neptunium-239239Np2.4 days27003.595
Plutonium-238238Pu86.0 years13.50.035
Plutonium-239239Pu24,110 years0.853.50.03
Plutonium-240240Pu6580 years1.23.50.042
Plutonium-241241Pu13.2 years1703.56
Curium-242242Cm163 days263.50.9

Table 3.

Core inventories and releases of the most important contaminants originating from the Chernobyl accident. Data obtained from [31, 32, 33].

noble gases

transuranic nuclides

The most significant release of radioactivity from the damaged reactor was in the form of noble gasses (85Kr and 133Xe). Nevertheless, fast atmospheric dispersal and the lack of chemical reactivity of noble gasses mean that radioactive krypton and xenon resulted only in trace global contamination. In contrast, the volatile iodine-131, released in significant quantities during the reactor fire, was the predominant problem in contaminated areas during 1986. It is estimated that up to 4000 additional thyroid cancers among people can be attributed to this nuclide [4]. In the long term, the most significant contribution of radiation dose to the biota is attributed to radiocesium (134Cs, 137Cs), particularly 137Cs, due to its long half-life (30.17 years), its propensity to accumulate in plant and fungal matter and animal nerve and muscle tissue. The contribution of 90Sr to the background dose is also significant, but much lower and often indistinguishable from pre-Chernobyl global fallout from atmospheric nuclear testing [34].

Radioecological research after 1986 in Europe involved multinational teams working in the Chernobyl exclusion zone (ChEZ) and the most contaminated areas of Belarus and Russia (Gomel and Bryansk regions), as well as many studies on a national level focusing on areas with known contamination. Among the projects conducted in the ChEZ, several exemplary studies of the bioaccumulation of different radionuclides in wildlife stand out [17, 19, 34, 35]. Researchers have demonstrated that the appropriate sentinel species for radioecological studies comprise small rodents including representatives of family Cricetidae like Myodes glareolusSchreber, 1870, Microtus arvalisPallas, 1778, Microtus oeconomusPallas, 1776 as well as European murid species: the yellow-necked wood mouse Apodemus flavicollisMelchior, 1834 and the wood mouse Apodemus sylvaticusLinnaeus, 1758.

During the 200 s, researchers reported very high internal doses in Cricetidae, particularly the bank vole (M. glareolus) due to high dietary intake of 137Cs [17, 34]. This has been confirmed by subsequent monitoring studies in the ChEZ [19, 35, 36], as well as in Alpine ecosystems in Bulgaria [37, 38]. Recent monitoring data suggest that M. glareolusis potentially the best rodent zoo monitor for residual contamination in Europe. A selection of results from two groups of monitoring programs, mentioned above is presented in Table 4.

Chesser et al., 2001 [17]Six different biotopes within the Chernobyl Exclusion ZoneVery high internal doses from 137Cs in dry muscle of M. glareolusfrom areas with high and medium contamination; average 137Cs body burden in M. glareolus2902–24,720 Bq/g. High body burden of 137Cs in Sorex araneus—2592–5901 Bq/g).
Beresford et al., 2008 [36]Three different biotopes within the Chernobyl Exclusion ZoneHigh total-body internal doses from 137Cs in M. glareolus2260 ± 1290 Bq/g; much lower doses from 90Sr in different species of small rodents (for M. glareolus81.3 ± 22.1 Bq/g, for Microtussp. 107 ± 35.0 Bq/g, for Apodemussp. 66.6 ± 28.3 Bq/g).
Beresford et al., 2020a [19]Reference (low-contamination) biotopes within the Chernobyl Exclusion ZoneComparatively high doses from 137Cs in M. glareolusfrom low-contamination “reference areas” in the ChEZ, total body burden of 137Cs in M. glareolus = 649 Bq/g; comparatively high total body burden of 137Cs in Microtussp. (952 Bq/g); Much lower doses from 137Cs in Soricidae (161 Bq/g for S. araneus, 121 Bq/g for S. minutus).
Iovtchev et al., 1996 [37]Two localities (Musala peak and Skakavtsite), Rila Mountain, BulgariaComparatively high whole-body total β-activities in wild rodents from both localities (2.5–3.0 Bq/g for Apodemusspecies, 3.25 Bq/g for Chionomys nivalisfrom Musala Peak, 2.75 Bq/g for M. glareolusfrom Skakavtsite).
Beltcheva et al., 2019 [38]Two localities (Musala peak and Skakavtsite), Rila Mountain, BulgariaOverall 10-fold reduction in whole-body total β-activities in wild rodents from both localities. Highest residual activities observed in M. glareolus(0.52 Bq/g). β-activities in other rodents show more significant reduction (0.23–0.37 Bq/g for Apodemussp., 0.38 Bq/g for Ch. nivalis).

Table 4.

A summary of the findings of five radioecological studies using small mammals as zoo monitors.

The summarized works show evidence for the high value of M. glareolusas a monitoring species for residual radioactivity from the Chernobyl accident due to its propensity to accumulate radiocesium. While accounting for the differences in values obtained by the various research groups, and the different time frames, another aspect of Chernobyl contamination becomes apparent: There are significantly higher depositions and animal body burdens of radiostrontium (90Sr) within the Chernobyl exclusion zone, as opposed to very low amounts of 90Sr present at greater distances from the accident site; this can be explained by the much lower volatility of strontium compared to cesium. This is one of the main reasons why 90Sr is still a significant contaminant within the ChEZ, but in most of Europe the largest part of the Chernobyl-associated dose burden to the biota comes from 137Cs.

During recent monitoring studies, conducted in Bulgaria in the period 1996–2020, small mammals such as rodents and insectivores were selected mainly due to their positions in the food chain like primary consumers, rapid maturity, large population number, and rapid biological reaction to the environmental changes [38]. The possible biological response of the organism was studied at different levels of organization of living matter, and evaluated the population number and structure, food spectrum, total beta-activity in target tissues, and organs of the investigated animals, standard hematological methods—to determine hemoglobin contents, hematocrit, and morphological characterization of erythrocytes, as well as cytogenetic methods. The food spectrum was analyzed as a basis for further investigations on the transfer of beta-emitters through the rodent populations and the whole ecosystem.

The total body burden of β-emitters of a species depends on the trophic chain position, food, life mode, physicochemical composition of the atmospheric precipitation, total suspended dust content in atmospheric air, and other factors. The total β-activities in Bq/kg of some small mammal species were investigated at two different altitudes in Rila Mountain, Bulgaria. The results, obtained in 2019–2020, are presented on Table 5.

Moussala Peak
2925 m a.s.l.
/mean ± SD/, Bq/kg
Beli Iskar (Skakavtsite area), 1400–1500 m a. s. l.β-activity
/mean ± SD/, Bq/kg
Ap. flavicollisn = 12230.3 ± 7.2Ap. flavicollisn = 13366.3 ± 8.1
Ch. nivalisn = 12382.0 ± 8.3M. glareolusn = 22424.2 ± 5.3

Table 5.

Whole-body total β-beta activities at two localities (Rila Mountain, Bulgaria), 2019–2020 [38].

All values were below 480 Bq/kg and were considered as referent.

Significant differences between mice and voles were obtained only due to the difference in their food specialization. Mice are omnivorous, while voles are mainly herbivorous species. Green vegetable parts accumulate radiocesium more actively than seeds and the quantity of the consumed low-caloric green food by animals is higher.

The comparison of the results obtained with the data 20 years ago makes it obvious that the values of total β-activity decreased by about 10 times in the period 1995–2019. Data obtained in the bodies of different monitor species of small mammals from Rila Mountain during 1995 varied from about 3500 Bq/kg in the yellow-necked wood mouse to 5000 Bq/kg in the snow vole. The total level of beta-activity in bank vole and yellow-necked wood mouse from Beli Iskar region during 1995 was between 2000 and 3000 Bq/kg [37].

High doses of radiation can influence the normal function of the blood and disturb the hematopoiesis. These were possible basophilic granulations that appear in enhanced, but also disturbed erythropoiesis, basophilic DNA fragments observed in a blood smear, frequently as a result of decreased spleen function, anemia, and overloaded bone marrow. However, the given results do not suggest such changes, and they have not been established.

A correlation between total beta-activity loading and chromosome aberration frequency in bone marrow cells was established. The percentage of chromosome aberrations in mice was about 1.6% and breaks were 0.2% and in herbivorous voles respectively 7.0 and 2.5%. The percentage of aberrant bone marrow cells of mice from the investigated regions is visibly lower than in vole species. This fact correlates with the recorded total body burden of β-emitters in herbivorous species in comparison with the omnivorous murids.


5. Principal remediation strategies for radioactive contamination

The issue of remediating radioactively contaminated terrestrial ecosystems dates back to the early years of the Atomic Age (1945–1965) when protection measures were a secondary consideration to weapons production. Tests were conducted in contaminated areas such as near Hanford, Washington, and Ozyorsk (Chelyabinsk-40) [27, 29].

After 1986, to protect the environmental health and resolve the liabilities due to eventual radioactive contamination, severely contaminated countries and the responsible institutions have undertaken certain remediation and protection measures:

  1. mechanical/physical methods—creation of barriers, burial/demobilization of radioactive sources; deep tilling of agricultural fields for facilitating downward migration of radioisotopes;

  2. forestry management—clearing and burial of severely contaminated coniferous forests presenting a fire hazard, natural succession/ecosystem restoration, and manual afforestation of contaminated agricultural areas with deciduous trees;

  3. selective use of soil additives—addition of lime to increase soil pH and limit the uptake of 90Sr by plants, use of fertilizers containing phosphorus, and potassium in order to reduce 137Cs bioaccumulation in plant matter, the addition of complexing agents such as powdered zeolites, and other aluminosilicate minerals in order to demobilize 137Cs; addition of hydroxyapatite (HAP) to prevent 90Sr cycling in ecosystems;

  4. crop selection in agricultural areas—production of non-food/feed crops such as cotton, flax, timber, and biofuels; use of land with low levels of contamination for sugar and oil production, whereby most residual radioactivity is removed during the refining processes;

  5. careful livestock farming—feeding farm animals clean fodder, administration of powdered zeolites as bio-sorbents, the addition of salt licks containing Prussian Blue to reduce 137Cs uptake by grazing animals.

Most of these strategies are discussed in detail elsewhere [39, 40, 41, 42, 43, 44]. All of the methods were applied to some degree within the ChEZ and the highly contaminated areas of the former USSR [42]. By far, the most widespread method used was the deep tilling of agricultural fields. Nevertheless, one of the strategies for remediation, the use of zeolites for demobilization and biodetoxification of 137Cs has only been tested on a small scale in the ChEZ, while, at the same time, being the most promising approach for countering the toxicity of radiocesium [39, 45].


6. Zeolites as bio-detoxifiers of radionuclides

Natural zeolites are one of the most interesting groups among minerals, some of which (clinoptilolite, mordenite, chabazite) have enormous potential in science and technology due to their high sorption capacity and the presence of deposits with huge reserves in many countries, including Bulgaria. In the early years of zeolite research, Ames (1960) found that clinoptilolite from the Hector deposit, California, is highly selective for Sr2+ and Cs+ [46]. Other heavy metals, especially monovalent ones, were also well adsorbed—respectively ion-exchanged by this natural zeolite. The author introduced an order of selectivity of clinoptilolite, which is:


The ion exchange properties of clinoptilolite and its selective sorption are especially valuable in the control of radioactive waste from nuclear energy production. The mineral has been successfully used as a sorbent of radionuclides from water and contaminated soils, as well as a food additive to limit 137Cs absorption in livestock [39, 41, 45].

Very significant research on zeolites has been conducted in Bulgaria for the past five decades, with two deposits of clinoptilolite in the Eastern Rhodope Mountains—Beli Plast and Beliya Bair-Zhelezni Vrata—being particularly suitable for bio-sorbents of heavy metals and radionuclides in the form of additives to food and livestock feed [47]. Recently, it was demonstrated that modified natural clinoptilolite from the Golobradovo deposit in the Eastern Rhodopes was practically non-toxic to laboratory mice and facilitated significantly the excretion of Pb2+ions from the gastro-intestinal tract of the experimental animals, thus protecting them against lead toxicity [48, 49]. In parallel, other Bulgarian researchers validated the use of zeolites from the Eastern Rhodopes in decontamination procedures and as soil fertilizer and even developed a clinoptilolite-based artificial soil (“Balkanin”) that was used for growing vegetables in space onboard the Mir station [50]. In the early 1990s, researchers from the Bulgarian Academy of Sciences developed a specially modified natural clinoptilolite (CLS-5) as a bio-sorbent for radiocesium (134Cs and 137Cs) and radiostrontium (89Sr and 90Sr) [51]. In a modified form and labeled KS-3, CLS-5 was used in the production of over 55,000 personal radiation protection emergency kits, most of which were distributed among the personnel of the Kozloduy Nuclear Power Plant and the people from the surrounding areas (Figure 2).

Figure 2.

Modified natural zeolites as part of a radiation protection emergency kit: Plastic vials containing CLS-5 (left), and the entire emergency kit (right) [51].

Two plastic vials containing CLS-5 with a quantity of 7 grams each have been integrated in the radiation emergency kit. The other components of the radiation protection kit are a painkiller syrette, a syrette with an antiemetic, a broad-spectrum antibiotic, potassium iodide (KI) tablets, and CBT (a radioprotector for abating acute exposure to radiation), bandages, and ethanol for disinfection [51].

As evident from the material presented, research into zeolites as bio-sorbents of radionuclides and heavy metals is fairly advanced in Bulgaria. The past achievements in developing modified clinoptilolite derivatives as 90Sr and 137Cs sorbents, and current and ongoing basic research in clinoptilolites as a countermeasure to Pb2+ and Cd2+ intoxication in mammalian species promise to yield the interesting results.


7. Conclusion

Ionizing radiation is one of the best understood cytotoxic and genotoxic agents. Nevertheless, much remains to be understood about the behavior of radionuclides in nature and the biological responses they induce. The radiobiology of low-dose, protracted irradiation is still an open area of research.

At the same time, bioaccumulation of certain radioisotopes along food chains poses serious ecosystem risks, or as the doyen of modern ecology Eugene Odum stated: “we could give nature an apparently innocuous amount of radioactivity and have her give it back to us in a lethal package!” [26].

The mitigation of environmental risks from radionuclides involves responsible management of the nuclear fuel cycle, as well as careful monitoring and safeguarding of nuclear installations. Among the strategies discussed in the chapter, all have been applied to a varying degree in severely contaminated agroecosystems and forest ecosystems. Perhaps the most promising venue of detoxication research is the application of zeolites as immobilizers and bio-detoxifiers for radiocesium and radiostrontium. Nevertheless, no method can fully remediate a contaminated ecosystem, meaning that prevention of radioactive contamination remains the first and best defense against anthropogenic radioactive pollution.



This work is supported by the National Science Fund of the Republic of Bulgaria, Project KP-06-PN44/3, 12.12.2020: “Crystal-chemical and structural characteristics of modified natural clinoptilolite and correlation between its sorption properties, ion exchange capacity for heavy metals and biological response in vivo and in vitro”.


  1. 1. Hall E, Giaccia A. Radiobiology for the Radiologist. New York, London: Lippincott Williams and Wilkins; 2006. p. 576
  2. 2. UNSCEAR. Sources, Effects and Risks of Ionizing Radiation, Annex B. New York: United Nations; 2020. p. 240
  3. 3. Besson B, Pourcelot L, Lucot E, Badot PM. Variations in the transfer of radiocesium (137Cs) and radiostrontium (90Sr) from milk to cheese. Journal of Dairy Science. 2009;92(11):5363-5370
  4. 4. Holm LE. Thyroid cancer after exposure to radioactive 131I. Acta Oncologica. 2006;45(8):1037-1040
  5. 5. Puck TT, Marcus PI. Action of X-rays on mammalian cells. The Journal of Experimental Medicine. 1956;103(5):653-666
  6. 6. Blakely E, Chang P, Lommel L, Bjornstad K, Dixon M, Tobias C, et al. Cell-cycle radiation response: Role of intracellular factors. Advances in Space Research. 1989;9(10):177-186
  7. 7. Pettersen EO, Wang H. Radiation-modifying effect of oxygen in synchronized cells pre-treated with acute or prolonged hypoxia. International Journal of Radiation Biology. 1996 Sep;70(3):319-326
  8. 8. National Academies of Sciences, Engineering, and Medicine; Division on Earth and Life Studies; Nuclear and Radiation Studies Board. In: Kosti O, editor. The Future of Low Dose Radiation Research in the United States: Proceedings of a Symposium. Washington (DC): National Academies Press (US); 2019
  9. 9. Trott KR, Rosemann M. Molecular mechanisms of radiation carcinogenesis and the linear, non-threshold dose response model of radiation risk estimation. Radiation and Environmental Biophysics. 2000 Jun;39(2):79-87
  10. 10. Schirrmacher V. Less can be more: The hormesis theory of stress adaptation in the global biosphere and its implications. Biomedicine. 2021;9(3):293
  11. 11. Joiner MC, Marples B, Lambin P, Short SC, Turesson I. Low-dose hypersensitivity: Current status and possible mechanisms. International Journal of Radiation Oncology, Biology, Physics. 2001;49(2):379-389
  12. 12. Hawk C, Hyland J, Rupert M, Colonvega M, Hall S. The 2007 recommendations of the International Commission on Radiological Protection. ICRP publication 103. Annals of the ICRP. 2007;37(2-4):1-332
  13. 13. Heuskin AC, Michiels C, Lucas S. Low dose hypersensitivity followingin vitrocell irradiation with charged particles: Is the mechanism the same as with X-ray radiation? International Journal of Radiation Biology. 2014 Jan;90(1):81-89
  14. 14. Bond VP, Robertson JS. Comparison of the Mortality Response of Different Mammalian Species to X-Rays and Fast Neutrons.Technical Report BNL-7603. NY, United States: Brookhaven National Laboratory; 1963
  15. 15. Williams ED. Chernobyl and thyroid cancer. Journal of Surgical Oncology. 2006;94(8):670-677
  16. 16. Dobrzyński L, Fornalski KW, Feinendegen LE. Cancer mortality among people living in areas with various levels of natural background radiation. Dose Response. 2015;13(3):1559325815592391
  17. 17. Chesser RK, Rodgers BE, Wickliffe JK, Gaschak S, Chizhevsky I, Phillips CJ, et al. Accumulation of 137Cesium and 90Strontium from abiotic and biotic sources in rodents at Chornobyl, Ukraine. Environmental Toxicology and Chemistry. 2001;20(9):1927-1935
  18. 18. Lelieveld J, Kunkel D, Lawrence MG. Global risk of radioactive fallout after major nuclear reactor accidents. Atmospheric Chemistry and Physics. 2012;12:4245-4258
  19. 19. Beresford NA, Barnett CL, Gashchak S, Maksimenko A, Guliaichenko E, Wood MD, et al. Radionuclide transfer to wildlife at a 'Reference site' in the Chernobyl Exclusion Zone and resultant radiation exposures. Journal of Environmental Radioactivity. 2020a;211:105661
  20. 20. Russell WL, Russell LB, Kelly EM. Radiation dose rate and mutation frequency. Science. 1958;128(3338):1546-1550
  21. 21. Sankaranarayanan K. Estimation of the hereditary risks of exposure to ionizing radiation: History, current status, and emerging perspectives. Health Physics. 2001;80(4):363-369
  22. 22. Goncharova RI, Riabokon' NI. Biological effects in natural populations of small rodents in radiation-polluted territories. Dynamics of chromosome aberration frequency in a number of generations of European bank vole (Clethrionomys glareolusSchreber). Radiatsionnai Biologiia Radioecologiia. 1998;38(5):746-753
  23. 23. Dubrova YE, Nesterov VN, Krouchinsky NG, Ostapenko VA, Neumann R, Neil DL, et al. Human minisatellite mutation rate after the Chernobyl accident. Nature. 1996;380(6576):683-686
  24. 24. Osterreicher J, Prise KM, Michael BD, Vogt J, Butz T, Tanner JM. Radiation-induced bystander effects. Mechanisms, biological implications, and current investigations at the Leipzig LIPSION facility. Strahlentherapie und Onkologie. 2003;179(2):69-77
  25. 25. Wang R, Zhou T, Liu W, Zuo L. Molecular mechanism of bystander effects and related abscopal/cohort effects in cancer therapy. Oncotarget. 2018;9(26):18637-18647
  26. 26. Odum E. Fundamentals of Ecology. Philadelphia: W. B. Saunders Company; 1959. p. 546
  27. 27. Creager A. Life Atomic: A History of Radioisotopes in Science and Medicine. Chicago: University of Chicago Press; 2013. p. 512
  28. 28. Bradley DJ, Schneider KJ. Radioactive Waste Management in the USSR: A Review of Unclassified Sources, 1963-1990: Technical Report. Richland, WA, United States: Pacific Northwest National Lab (PNNL); 1990. p. 235
  29. 29. Ilyin L. Chernobyl: Myth and Reality. Moscow: Megapolis Publishing; 1995. p. 358
  30. 30. Akleyev AV, Kostyuchenko VA, Peremyslova LM, Baturin VA, Popova IY. Radioecological impacts of the Techa River contamination. Health Physics. 2000;79(1):36-47
  31. 31. Kirchner G, Noack CC. Core history and nuclide inventory of the Chernobyl core at the time of accident (TPR-NS--29-No1). Nuclear Safety. 1988;29(1):1-5
  32. 32. Güntay S, Powers D, Devell L. The Chernobyl reactor accident source term: Development of a consensus view. IAEA: INIS. 1995;41(8):183-193
  33. 33. Kai M, Homma T, Lochard J, Schneider T, Lecomte JF, Nisbet A, et al. ICRP Publication 146: Radiological protection of people and the environment in the event of a large nuclear accident: Update of ICRP PUBLICATIONS 109 AND 111. Annals of the ICRP. 2020;49(4):11-135
  34. 34. Chesser R, Sugg D, Lomakin M, Van den Bussche R, DeWoody A, Jagoe C, et al. Concentrations and dose rate estimates of 134,137-cesium and 90-Strontium in small mammals at Chornobyl, Ukraine. Environmental Toxicology and Chemistry. 2000;19(2):305-312
  35. 35. Beresford NA, Scott EM, Copplestone D. Field effects studies in the Chernobyl Exclusion Zone: Lessons to be learnt. Journal of Environmental Radioactivity. 2020;211:105893
  36. 36. Beresford NA, Gaschak S, Barnett CL, Howard BJ, Chizhevsky I, Strømman G, et al. Estimating the exposure of small mammals at three sites within the Chernobyl exclusion zone-a test application of the ERICA Tool. Journal of Environmental Radioactivity. 2008;99(9):1496-1502
  37. 37. Iovtchev M, Metcheva R, Atanasov N, Apostolova M, Bogoeva L, Zivkov M, et al. Investigation on total β-activity of indicator vertebrate species from Rila National Park. OM2. 1996;4:38-42
  38. 38. Beltcheva M, Metcheva R, Geleva E, Aleksieva I, Ostoich P, Ravnachka I, et al. Total β - activity in monitor species small rodents from two different altitudes in Rila Mountain (Bulgaria). AIP Conference Proceedings. 2019;2075:130004
  39. 39. Phillippo M, Gvozdanovic S, Gvozdanovic D, Chesters JK, Paterson E, Mills CF. Reduction of radiocaesium absorption by sheep consuming feed contaminated with fallout from Chernobyl. The Veterinary Record. 1988;122(23):560-563
  40. 40. IAEA. Technologies for Remediation of Radioactively Contaminated Sites. Vol.1086. Vienna: IAEA publications; 1999. pp. 1-110
  41. 41. Jacob P, Fesenko S, Firsakova SK, Likhtarev IA, Schotola C, Alexakhin RM, et al. Remediation strategies for rural territories contaminated by the Chernobyl accident. Journal of Environmental Radioactivity. 2001;56(1-2):51-76
  42. 42. Vidal M, Camps M, Grebenshikova N, Sanzharova N, Ivanov Y, Vandecasteele C, et al. Soil- and plant-based countermeasures to reduce 137Cs and 90Sr uptake by grasses in natural meadows: The REDUP project. Journal of Environmental Radioactivity. 2001;56(1-2):139-156
  43. 43. Smiciklas I, Dimovic S, Plecaš I. Removal of Cs1+, Sr2+ and Co2+ from aqueous solutions by adsorption on natural clinoptilolite. Applied Clay Science. 2007;35:139-144
  44. 44. Handley-Sidhu S, Mullan TK, Grail Q , Albadarneh M, Ohnuki T, Macaskie LE. Influence of pH, competing ions, and salinity on the sorption of strontium and cobalt onto biogenic hydroxyapatite. Scientific Reports. 2016;18(6):23361
  45. 45. Pöschl M, Balás J. Reduction of radiocaesium transfer to broiler chicken meat by a clinoptilolite modified with hexacyanoferrate. Radiation and Environmental Biophysics. 1999;38(2):117-124
  46. 46. Ames L. The cation sieve properties of clinoptilolite. American Mineralogist. 1960;45(5-6):689-700
  47. 47. Djourova E, Aleksiev B. Zeolitic rocks related to the second acid Paleogene volcanism to the east of the town of Kardzhali. In: Konstantinos S, editor. Geologica Rhodopica 2. Thessaloniki: Aristotel University; 1990. pp. 489-499
  48. 48. Beltcheva M, Metcheva R, Popov N, Teodorova SE, Heredia-Rojas JA, Rodríguez-de la Fuente AO, et al. Modified natural clinoptilolite detoxifies small mammal's organism loaded with lead I. Lead disposition and kinetic model for lead bioaccumulation. Biological Trace Element Research. 2012;147(1-3):180-188
  49. 49. Beltcheva M, Metcheva R, Topashka-Ancheva M, Popov N, Teodorova S, Heredia-Rojas J, et al. Zeolites versus lead toxicity. Journal of Bioequivalence & Bioavailability. 2015;7(1):12-29
  50. 50. Ivanova T, Stoyanov I, Stoilov G, Kostov P, Sapunova S. Zeolite gardens in space. In: Kirov G, Filizova L, Petrov O, editors. Natural Zeolites. Proceedings of the Sofia Zeolite Meeting’ 95, PENSOFT, Sofia. 1997: 3-10
  51. 51. Popov N, Jilov G, Popova T. Study of the use of natural clinoptilolites and their modifications as effective sorbents of Sr and Cs and heavy metals from water solutions and drinking waters. In: Proceedings of the 5th International Conference of Natural Zeolites “Zeolite-97”, September 21-29, 1997. Ischia (Naples), Italy; 1997

Written By

Peter Ostoich, Michaela Beltcheva, Jose Antonio Heredia Rojas and Roumiana Metcheva

Submitted: February 1st, 2022 Reviewed: March 11th, 2022 Published: April 21st, 2022