Radioactively contaminated areas: Bioindicator species and biomarkers of effect in an early warning scheme for a preliminary risk assessment

Highlights

• Knowing the most used biomarkers and bioindicators used in radioactive areas.

• Understanding of the response similarities between human and non-human biota.

• Identifying the knowledge gaps.

• Proposing an early warning scheme, to perform a screening evaluation of radioactive areas.

• Permitting routine assessments without disturbing and alarming local populations.

Abstract

Concerns about the impacts on public health and on the natural environment have been raised regarding the full range of operational activities related to uranium mining and the rest of the nuclear fuel cycle (including nuclear accidents), nuclear tests and depleted uranium from military ammunitions. However, the environmental impacts of such activities, as well as their ecotoxicological/toxicological profile, are still poorly studied. Herein, it is discussed if organisms can be used as bioindicators of human health effects, posed by lifetime exposure to radioactively contaminated areas. To do so, information was gathered from several studies performed on vertebrates, invertebrate species and humans, living in these contaminated areas. The retrieved information was compared, to determine which are the most used bioindicators and biomarkers and also the similarities between human and non-human biota responses. The data evaluated are used to support the proposal for an early warning scheme, based on bioindicator species and on the most sensitive and commonly shared biomarkers, to perform a screening evaluation of radioactively contaminated sites. This scheme could be used to support decision-making for a deeper evaluation of risks to human health, making it possible to screen a large number of areas, without disturbing and alarming local populations.

Introduction

Uranium is the heaviest naturally occurring element existing in the earth’s crust [1], [2]. Natural uranium is a mixture of three isotopes, U-234 (²³⁴U), U-235 (²³⁵U) and U-238 (²³⁸U), which are chemically the same, but with different radioactive properties [2]. There are three kinds of mixtures (based on the percentage of the composition of the three isotopes): natural, enriched and depleted uranium. In natural uranium, the most common isotope is ²³⁸U (99.274%), followed by ²³⁵U (0.720%) and ²³⁴U (0.005%) [2], [3]. Enriched uranium has been subjected to a process that increased the percentage of ²³⁵U and ²³⁴U isotopes in its composition. Although most processes enrich in both ²³⁴U and ²³⁵U, the laser enrichment enhances the concentration of ²³⁵U only. Depleted uranium is the by-product of the enrichment process which, consequently, has lower levels of these two isotopes, when compared with natural uranium [2]. Enriched uranium is classified by the percentage of ²³⁵U. For nuclear energy purposes it typically contains 3% of ²³⁵U, however when uranium is enriched for nuclear weapons it contains as much as 97.3% of ²³⁵U [2]. ²³⁵U is important for both nuclear energy and nuclear weapons, since it is the only isotope existing in nature that is fissile (it can be broke apart by slow (thermal) neutrons), producing a chain reaction that releases high amounts of energy [4].

The end of the cold war in the late 1980’s, was characterized by conferences on disarmament and subsequently followed by less or no further demand for nuclear weapons, and dilution of highly enriched uranium with depleted uranium [5]. This latter initiative resulted in a severe drop of uranium prices worldwide, and consequently the closure of many uranium mines, uranium processing facilities and chemical plants for the recovery of uranium from phosphate ore [5]. However, in 2004 the uranium price started to rise, caused by a continuous and increasing demand for nuclear fuel and the construction of new nuclear power plants, mainly in China and India, but also in other newly industrialized countries around the world. This was mainly caused by the rise of world market prices for fossil fuels with a great impact on the world economy, particularly in developing countries with low financial resources [5].

In the next 10 years, the market is expected to grow significantly, according to the World Nuclear Association (WNA). The Global Nuclear Fuel Market Report reference scenario (post Fukushima accident) forecast a 31% increase in uranium demand between 2013–23. Moreover, with electricity demand expected to grow 37% by 2040, according to the Organization for Economic Co-operation and Development’s (OECD) International Energy Agency [6], there is plenty of opportunity for nuclear energy to grow in a world concerned with limiting carbon emissions. Hence, according to the WNA, world mine production has expanded significantly since 2005, providing, at the present time, over 90% of the requirements of power utilities. The increase in energy demand has raised the interest in opening new mines in many countries and has increased the uranium mining activity in the main uranium producing countries [5], [7].

Anthropogenic sources of environmental concern relating to uranium, its radioisotopes and other radionuclides include uranium mining and milling and the improper disposal of tailings, uranium conversion and enrichment, uranium fuel fabrication, nuclear weapons production and testing, production of phosphate fertilizers from phosphate rocks containing uranium and nuclear accidents [2], [8]. The natural uranium progeny (²³⁸U) is composed by a substantial number of radionuclides, however, the longer-lived members, namely ²²⁶Ra, ²²²Rn, ²¹⁰Po and ²¹⁰Pb contribute about 99.75% of the total dose received by the general public and by any organisms exposed to contaminated environmental matrices, namely as a result of uranium extraction and processing [5], [9]. Uranium itself is mildly radioactive, due to its very long half-life (4.5 billion years), which means that each atom of uranium decays very infrequently, resulting in a low specific activity [7]. Therefore, uranium’s chemical toxicity is the primary concern and the main environmental health hazard [7]. Thorium is estimated to be three times more abundant in the Earth’s crust than uranium and occurs mostly as ²³²Th [10]. Population may be exposed to ²³²Th and its daughters mainly through diet and through external gamma radiation, when for example thorium-rich building materials are used, producing significant effective doses to the population [10]. The long-lived thorium (14.5 billion years) decays initially to ²²⁸Ra, which has a 5.75 years half-life, being the longest lived of all elements of the ²³²Th progeny. Ingestion dose coefficients of ²²⁸Ra are up to one order of magnitude higher than for 226Ra [10]. As such, critical exposure events can play an important role on the total dose received by humans (mainly by infants) [10]. Therefore, representative surveys are highly encouraged to estimate background values and average annual population intake and also to detect possible critical exposures [10].

Nowadays, the general public is more alert to the contamination of the natural environment and to its impacts on public health, particularly with regard to contaminants of radiological importance [11]. Considering the natural environment, these concerns are related to the risk of environmental degradation and contamination, reduced ecosystem viability and biodiversity, aesthetics, public amenities, access to land, and quarantine of land for future beneficial land use [11], [12], [13], [14]. Regarding human health, the exposure to environmental levels of uranium, metals associated to uranium ore and radionuclides (natural and artificial) have been associated with many health problems, as they exert negative effects at the molecular, cellular, tissue and organ levels. These contaminants can negatively affect important physiological processes, including kidney function, bone development and hematopoiesis [7], [15], [16]. At the molecular level, uranium (and other metals) and radionuclides may also induce genomic instability by affecting pathways like DNA repair, regulation of nuclear transcription factors, regulation of gene expression, apoptosis, cell growth, reactive oxygen species (ROS) generation and by replacing essential metals in metabolic pathways [17], [18], [19], [20]. All of these events may lead to the development of serious genetic diseases, like cancer. Therefore, the potential detrimental effects of these contaminants in the environment and in organisms (human and non-human) exposed to them, highlight the need to establish an early warning scheme based on non-human biota, specifically designed for areas contaminated with radioactive materials, to easily identify those in which risks to human health are likely to occur. This would be very important in the establishment of measures to mitigate contamination before more serious effects on human health arise, due to chronic exposure to uranium and radionuclides. Risk assessors generally assess either harms on ecological health (using bioindicators) or human health (using biomarkers of exposure or effect) [21]. Bioindicators are organisms or communities whose responses to environmental disturbances are observed to evaluate a situation, providing clues about the condition of the whole ecosystem [22]. Since it is often difficult to directly monitor aspects of condition or health of natural populations and of humans, bioindicators are often useful surrogates [21]. The careful selection of bioindicators will allow risk assessors to optimize the amount of information obtained [21]. However, though there are case studies where both human and ecological risk assessments were performed, the majority still rely on the chemical analysis of environmental samples, neglecting the assessment of biological effects, that could be performed by means of using both human and ecological health indicators [21].

In this review, we discuss whether non-human organisms (namely vertebrates and invertebrates) can be used as potential bioindicators of humans exposure and health effects caused by the environmental exposure to radioactively contaminated areas which include uranium and its descendants as well as metals associated with uranium ores. Thus, information has been gathered from studies performed in areas contaminated by uranium mining and milling, uranium mineralization areas, nuclear power plants and nuclear fuel facilities, nuclear accidents and nuclear weapons production, testing and use. In a weight of evidence approach, this compilation allows us to determine which are the most used bioindicators and biomarkers, which biomarkers are the most sensitive to the exposure to these contaminants and which are the endpoints displaying more consistent responses between different taxa. Thus, based on the information collected it is possible to understand whether the responses are similar in humans and non-human species, so that a reasoned choice of bioindicator species could be made and also knowledge gaps can be identified. Based on this information, it will be possible to propose an early warning scheme (EWS), integrating bioindicator species and the most sensitive and commonly shared biomarkers. The EWS is intended to be a fast and economic tool to perform a screening evaluation of these contaminated areas, in a less intrusive and alarming approach. It could be a part of a decision support-system aimed at screening sites for the evaluation of risks to humans and ecosystems. Plants, which have been used, to some extent, in studies performed in these contaminated areas, mainly in the Chernobyl area, should also be included in this EWS. These studies provide information on the ability of these contaminants to be transferred along the food chain, and also on the potential of metal- and radionuclide-contaminated areas to cause genetic alterations and clastogenic effects in human and non-human biota. Moreover, the induction of these kinds of effects in plants show the ability of these contaminants to compromise primary productivity and the sustainability of biodiverse plant communities, likely to affect the normal functioning of entire ecosystems and the services provided by them. This EWS could support routine assessments of a large number of areas, in a cost-effective way and will support decision-making processes regarding the proper management of these areas in order to mitigate the risks to human health.