Chapter 4. Environmental, health and socio-economic impacts of soil pollution
Soil pollution and risk to human health
The role of soils on human health is widely recognized among the scientific community (Abrahams, 2002; Brevik and Sauer, 2015; Brevik et al., 2017; Brevik and Burgess, 2013; Oliver, 2008; Oliver and Gregory, 2015) and has also been acknowledged in the international political arena inclusion within the Sustainable Development Goal 3, regarding healthy lives and well-being for all (UN, 2017). Soil-borne diseases and diseases and death attributable to soil pollution must be monitored to accurately assess the indicators 3.3.5.6 and 3.4.1.7, and the target 3.9 “By 2030, substantially reduce the number of deaths and illnesses from hazardous chemicals and air, water and soil pollution and contamination”, which currently lacks any measurable indicator for soil pollution.
The lack of an indicator is due to the complexity of relating soil pollution to health outcomes (Filippelli et al., 2020). Soil pollution often has a long-term impact and many variables determine the relationship between exposure to soil pollution and disease, such as:
- - Contaminant(s) and concentrations: humans are exposed to multiple contaminants at specific times and throughout their lives. The mixtures of contaminants to which we are exposed vary throughout our lives and can have synergistic, antagonistic or additive effects.
- - Routes of exposure: there are three main routes of exposure (inhalation, ingestion, and dermal absorption), which are often combined and occur simultaneously.
- - Source media of exposure: soil contaminants can reach humans through soil, dust, air, water or food. All can occur separately or simultaneously.
- - Individual vulnerabilities and community specificity: people with pre-existing illnesses, or more vulnerable individuals such as foetuses, neonates and children will be more sensitive than healthy adults. Certain communities are at higher risk of exposure because of their traditions and food culture (e.g. geophagists), socio-economic status and proximity to pollution sources.
This section aims to present recent scientific evidence linking soil pollution with human health impacts and major exposure pathways, and to emphasize the need for improved monitoring of health risks including the development of harmonized and reliable indicators for soil pollution.
According to the information gathered by FAO for this report, only 49 countries have an institution with a mandate to collect health data related to environmental impacts, but frequently the collected information is not publicly available. At the global level, WHO has established, under the Global Health Observatory, an indicator of the burden of disease attributable to the environment which includes all diseases and deaths attributable to air, soil and water pollution with chemicals or biological agents; ultraviolet and ionizing radiation; built environment; noise and electromagnetic fields; occupational risks; agricultural methods and irrigation schemes; anthropogenic climate changes and ecosystem degradation; and individual behaviours related to the environment, such as hand-washing, and the ingestion of contaminated food by unsafe water or dirty hands (WHO, 2020a). However, one of the main routes of entry for soil contaminants into the human body is through the ingestion of unsafe food. Although the WHO indicator mentioned above refers to food externally contaminated by parasites, food with high concentrations of inorganic or organic contaminants is not included.
The most recent global data dates back to 2012, but this data indicates that about 23 percent of global deaths (12.6 billion deaths) were attributable to environmental factors (Figure 14), reaching 28 percent for children younger than 4 year old (Prüss-Ustün et al., 2016). Some countries face considerable concern in this regard, such as India, People’s Republic of China, Lao People’s Democratic Republic, or the Democratic People’s Republic of Korea, where more than 30 percent of deaths are attributable to an unhealthy environment (WHO, 2016a).
Figure 14. Percentage of total deaths attributable to the environment by 2012, representing the burden of disease that could be avoided by modifying the environment.
However, there is no accurate national or global estimate of the burden of disease attributed solely to soil pollution or soil-borne diseases. The negative impact of soil pollution on human health may be underestimated, mainly because of the lack of information in the least developed countries, where there is little or no investment in pollution identification and quantification, and risk assessment (Landrigan et al., 2018). This is also the case in many developed countries, where measures to assess and control or remedy polluted soils are not of a precautionary nature and are only implemented after damage has been detected. Furthermore, a system of harmonised indicators has not yet been established to collect data on the impact of soil pollution on human health at national level and with comparison at regional or global level.
Another constraint to establishing a global monitoring system for health problems attributable to soil pollution is the difficulty of establishing cause-effect relationships between soil pollution and the burden of disease and death associated with exposure. Exposure typically occurs at low concentrations over long periods of time or even over a lifetime, unless a major accident occurs, such that establishment of strong relationships that trigger political and social action difficult.
4.3.1. Pathways for exposure
Human beings are in close contact with the environment and the natural resources on which our well-being depends. All components of the environment - water, air, land, organisms - are interconnected and interrelated. Soil is the key link in the functioning of ecosystems.
- Ninety-five percent of our food is produced directly or indirectly from the soil, including both plant and animal products that depend on the nutrients provided by the soil (FAO, 2015b).
- Soil regulates the exchange of gases with the atmosphere and contributes to both the storage and release of greenhouse gases, such as CO2, N2O or CH4, but also of volatile and gaseous contaminants such as mercury, radon, volatile organic contaminants or some POPs (Bao et al., 2015; Kaushal et al., 2014; Lei et al., 2021).
- Soils accumulate less than 1 percent of the global water, but this tiny amount is essential to sustain terrestrial ecosystems. Soils filter water from rainfall or irrigation, store water, support plant growth water needs, and allow the redistribution vertically and horizontally to ground and surface water bodies, thus regulating quality and quantity (O’Green, 2013).
Contaminants can move relatively freely between environmental compartments, from soils to plants and animals, to the atmosphere, and to water bodies and vice versa. Therefore, a polluted soil environment poses a risk to our health.
There are four main routes of exposure to soil contaminants: i) accidental ingestion of contaminated food, dust, and polluted soil particles, ii) intentional ingestion of soil, iii) inhalation of soil particles, contaminated dust and vapours, indoors and outdoors, and iv) dermal contact (Figure 15). However, given the interconnectivity of the components of the environment, it is often very difficult to discern the origin of the pollution and to quantitatively attribute the health damage to a specific source.
Figure 15. Main exposure pathways to soil pollution.
Accidental ingestion of contaminated food, dust, and polluted soil particles
Contaminated food intake is the main pathway for soil contaminants to the human body, accounting for more than 90 percent of contaminant intake (Science Communication Unit, University of the West of and England, Bristol, 2013). WHO estimates that about one-tenth of the world’s population becomes ill each year from eating contaminated food, and about 420 000 people die annually from diseases resulting from acute or chronic poisoning (WHO and FAO, 2018). Humans can ingest contaminants via crops, as a result of plant accumulated contaminants from the soil, or from contaminated soil particles attached to plants, but also from meat and dairy products sourced from grazing and game animals that feed on contaminated fodder or prey. The deposition of contaminated soil particles and dust on food or food utensils is also an accidental route of contaminant transfer to humans. This exposure route is especially relevant in infants and children due to their hand-to-mouth behaviour.
Usually, the food we consume has low concentrations of contaminants, because in many countries quality controls measures are followed according to national or international standards, which establish tolerable intake doses based on scientifically demonstrated evidence. At the international level, food quality standards are developed by the Joint FAO/WHO food standards programme and the Codex Alimentarius, with 188 Member Countries and 1 Member Organization (the European Union) all of whom are committed to adopt the standards when developing food control systems and regulations (Figure 16). The Joint FAO/WHO food standards programme meets regularly to establish and update threshold values for contaminants in food according to state-of-the-art scientific evidence (Table 2). All documents produced by the Joint FAO/WHO Expert Committee on Food Additives (JECFA), are freely accessible8 and the database allows search by type of contaminant. These documents provide detailed information on risk assessment, toxicological and epidemiological studies, sampling guidelines and analytical methods, dietary intake assessment and indications for controlling contaminants presence in food.
Figure 16. Member nations of the FAO/WHO Codex Alimentarius Commission.
However, threshold values for contaminants in food or tolerable limits refer to single contaminants, while multiple contaminants are often detected in polluted soils, transfer to crops, and concentrate during post-harvest treatments. Multiple contaminants can have antagonistic, summatory or synergistic effects. Levels of contaminants in blood and tissue can accumulate over time and may cause chronic diseases (Gall, Boyd and Rajakaruna, 2015). Thus low levels of multiple contaminants enter our bodies, and the combined effects are largely unknown (Słojewska and Gutowska, 2019).
Cases of poisoning after the ingestion of contaminated crops grown on polluted soils have been reported worldwide. International agencies, such as WHO or FAO, are working to establish maximum or tolerable daily, weekly or monthly doses of contaminants that can be ingested with food based on risk assessments, ecotoxicological experiments and observed effects in populations at polluted sites. Table 2 summarises the tolerable intake level for certain contaminants present in food stuffs, the main health effects observed and the food products in which these contaminants are mostly found. It is noteworthy that pesticides are not included in the table despite being major soil contaminants. This is because detailed information on their health effects is provided in the UNEP report (UNEP, 2021).
Table 2. Tolerable intake dose for certain contaminants present in food and the main health effects produced.
Intentional ingestion of soil
Geophagy or intentional soil ingestion is the most common type of pica, an eating disorder that involves eating items that are not typically thought of as food and do not contain significant nutritional value. The average daily soil intake of a geophagist is about 50 g of soil, although it can vary between 5 and 70 g of soil (Frazzoli et al., 2016). Geophagy has occurred for millennia in different human communities around the world, but also in other species (Panichev et al., 2016; Young and Miller, 2019). Well-documented cases are predominantly in the tropics, especially in sub-Saharan Africa, and in aboriginal communities in Australia and the Pacific (Kambunga et al., 2019b; Rowland, 2002), and associated to people with a weaker immune system, pregnant women and children, or people suffering anaemia and other micronutrients deficiencies (George et al., 2015; Huebl et al., 2016; Young and Miller, 2019).
The ingestion of soil particles, especially clays, can be beneficial as a food detoxifier due to absorption of pathogens, cations, and other toxicants (Macintyre and Dobson, 2017; Pebsworth et al., 2019) or by preventing the absorption in the body and satisfying certain micronutrient deficiencies (Young and Miller, 2019). Nevertheless, exposure to trace elements, radionuclides, organic contaminants such as pesticides or PAHs, and antimicrobial resistant bacteria may be increased by the ingestion of polluted soil particles (Egendorf et al., 2020; Frazzoli et al., 2016; Gundacker et al., 2017; Lar, Agene and Umar, 2015; Young and Miller, 2019). However, there are few detailed assessments of the quality of sold soil preparations, the bioavailability of contaminants, and the potential health risks posed by the ingestion of polluted soil particles (Frazzoli et al., 2016).
Health effects reported in geophagists and attributed to the consumption of contaminated soil particles vary from oxidative stress and acute or chronic toxicity to cancer and neurological disorders (Gwenzi, 2020). In the case of geophagy during pregnancy, the ingestion of associated contaminants can also have detrimental effects on the foetus such as growth retardation or premature births (Kambunga et al., 2019a, 2019b; Lar, Agene and Umar, 2015).
Geophagy is less likely to occur than accidental ingestion, although it is important in some communities where women practice geophagy especially during pregnancy and it is also relevant for small children. Young children are especially vulnerable to ingesting contaminated particles from play habits in parks and gardens and hand-to-mouth contact, and dermal contact is also a common route of exposure for soil contaminants in children. For example, an increased risk of mercury exposure was observed in children in a legacy mining city in Slovenia due to ingestion of polluted soils; while the risk for adults is below tolerable daily limit values after considering all possible routes of exposure (Bavec, Biester and Gosar, 2018).
Inhalation of soil particles, contaminated dust and vapours, indoors and outdoors
Inhalation of soil contaminants is more frequent in the case of occupational exposure. This may include workers from polluting industries exposed to inorganic and organic contaminants as vapours from soil and via dust, farmers exposed to agrochemical vapours and droplets, workers in landfills and pollution remediation companies exposed to soil contaminants during handling, transport and burial/digging work. Exposure conditions, contaminant concentrations and bioavailability are highly variable and include a regulatory component in terms of personal protection measures. Occupational exposure is beyond the scope of this report and is not addressed in detail.
The general population can also be exposed to soil contaminants by inhalation. Urban soils and the urban indoor and outdoor environment may contain locally released contaminants (such as those sourced from vehicle exhaust gases, lead containing paints, textile chemicals, household chemicals, etc.) - see Chapter 3), but also global contaminants that can be found far from the emitter, posing a risk to the 55.7 percent of the world’s population living in urban environments (World Bank, 2019). In addition, residential areas neighbouring industrial sites can be affected by industrial emissions, as observed in the Namibian city of Tsumeb affected by smelter-derived emissions (Fry et al., 2020) or the city of Mount Isa, in Queensland (United States) affected by lead mining emissions (Zheng et al., 2021). In both cases, trace elements deposited in soils and urban dust pose a risk to local populations, for whom inhalation of polluted dust represents a minor, but still considerable, route of exposure (Fry et al., 2020; Zheng et al., 2021).
Contaminated soil particles can be mobilized during outdoor work in gardens or farms, by wind erosion, or even brought indoor on shoes and clothing from the working environment or parks. For example, Kang and co-workers observed that about 10 percent of asbestos-related disorders were attributable to household exposure, which occurs when a family member exposed to asbestos at work comes home in work clothes and affects the rest of the family (Kang et al., 2018). Mobilized soil particles become part of the particulate matter of the outdoor and indoor air, remaining temporarily in the air environment, to be inhaled or deposited on food and cooking utensils, or to be ingested unintentionally. Children are particularly vulnerable to the inhalation of contaminated soil particles because of their playing habits, which lead them to spend more time in contact with the soil (Egendorf et al., 2020). Mobilized soil particles can transport various contaminants that can be absorbed differently in the respiratory, digestive and gastrointestinal system. Qin, Nworie and Lin (2016) and van der Kallen, Gosselin and Zagury (2020) have observed that oral and inhalation bioaccessibility of trace elements increases as soil particle size decreases, with most bioavailable forms being sorbed to the < 2 µm soil fraction, except for arsenic that was mainly retained in coarser fractions. In these studies, arsenic and chromium had a relatively low oral and inhalation accessibility and hence were less prone to be absorbed into the gastric and gastrointestinal systems. Copper showed the highest oral and inhalation bioaccessibility in both cases (van der Kallen, Gosselin and Zagury, 2020; Qin, Nworie and Lin, 2016).
Some inorganic contaminants, such as radon, asbestos and some forms of trace elements, are mostly absorbed into the human body by inhalation. Radon is a radioactive gas that does not interact with other elements but sorbs to dust particles. Once inhaled, radon (and its decay products) emits alpha and beta particles to the respiratory tract (ATSDR, 2012b). Lung cancer has been attributed to radon after long-term exposure, and this was first reported in uranium mine workers and later assessed in residential environments (Garzillo et al., 2017). Inhalation is also the primary entry route for asbestos and erionite fibres present in air (Lippmann, 2014; Wolfe et al., 2017). Although particularly important for occupational exposure, asbestos fibres can also be inhaled by people in areas surrounding mining sites or by accidental exposure during gardening and recreation activities due to erosion or weathering of soils and rocks containing asbestos (ATSDR, 2014). The main symptoms of asbestos exposure are shortness of breath, persistent dry cough, chest tightness or pain, and lung cancer and mesothelioma have also been attributed to asbestos exposure (Kettunen et al., 2017). Trivalent chromium is relatively stable in soils being strongly sorbed onto clay and organic matter surfaces, and thus its uptake by plants is relatively low. However, hexavalent chromium, an anion highly mobile, is frequently found in indoor and outdoor environments as particle-bound chromium or chromium dissolved in droplets. Inhalation of chromium has severe health effects in the respiratory tract, including damage to the nasal mucosa and perforation of the nasal septum with acute exposure, and damage to the lower respiratory tract which leads, leading to asthma or lung cancer (ATSDR, 2012a; Sawicka, Jurkowska and Piwowar, 2020). Metallic mercury is also highly volatile at room temperature and inhalation of mercury vapours can cause acute respiratory syndrome, chemical pneumonia, respiratory distress, respiratory failure, and ultimately death (Cortes, Peralta and Díaz‐Navarro, 2018; WHO, 2017b).
Inhalation is also a major route of exposure for volatile and semi-volatile organic contaminants (VOCs and SVOC, respectively), including some pesticides, dioxins, PAHs, phthalates, BTEX, PBDEs and PCBs (see Chapter 2) (Carpenter, 2015). Volatile organic contaminants can diffuse to indoor air from subsurface contaminated soils and are also present in the outdoor environment (Wei et al., 2018). Many of these contaminants are endocrine disruptors, neurotoxic and carcinogenic (IARC, 2012). Besides the industrial and agricultural sources, daily household products are an important source of VOCs and SVOCs in indoor environments. Indoor dust may contain soil particles and associated soil contaminants, including household chemicals (Huang et al., 2014). The inhalation of contaminants causes respiratory diseases, such as asthma, acute respiratory infections or lung cancer, but also cardiovascular disease and neurodevelopmental disorders, associated to indoor and occupational exposure (Carpenter, 2015; Li et al., 2019b; Lucattini et al., 2018).
Dermal contact
The skin is the largest organ in our body. It has a major protection function against environmental factors, such as chemicals, pathogens, radiation and other external threats, and also contributes to regulation of temperature and water loss (WHO, IPCS and IOMC, 2014). The skin is a three-layered organ composed of the epidermis, the dermis and the subcutis. The epidermis is in turn formed of multiple layers (Figure 17): the stratum corneum, which is the outermost layer, the stratum lucidum, the stratum granulosum, the stratum spinosum, and the stratum basale (the deepest portion of the epidermis). The stratum corneum is the first and more important line of defence, therefore the route of dermal sorption of contaminants is low for the majority of contaminants. The composition and structure of these layers reduce permeability to environmental contaminants, but many chemicals and elements can pass through this barrier and enter the circulatory system for distribution throughout the body (WHO, IPCS and IOMC, 2014).
Figure 17. Anatomy of the epidermis.
Dermal contact or exposure to polluted soil occurs during recreational activities, gardening, or construction-related activities, but also from contact with household items in/on which contaminated dust has been deposited (Ferguson et al., 2008). Children are again the most vulnerable to this exposure pathway due to play habits in open spaces and poor hygiene (Egendorf et al., 2020; Tsou et al., 2018).
Dermal exposure to soil contaminants can cause skin diseases, such as dermatitis caused by irritation or allergies, hives, acne or even cancer. But systemic effects can also be observed if the skin barrier is bypassed, such as when contaminants enter and spread through the circulatory system. The health risk caused by exposure through dermal contact depends on the concentration of the contaminant in the soil and the form in which the contaminant is found (bound to soil particles, dissolved in solution, forming a NAPL9, etc.); the time of exposure (frequency and duration of contact); toxicokinetic considerations; and intrinsic receptor factors such as the surface of the exposed skin, the dermal adhesion of the solid particles to the skin, the thickness of the liquid films on the skin, and/or the residue transfer factors (US EPA, 2015a). Numerous studies have analysed the dermal absorption of multiple contaminants, such as pesticides, trace elements, plasticizers, among others, using in vivo tests with experimental animals or in vitro or ex vivo tests with human corpses and skin of other mammals, and several models have been developed (Blanco et al., 2008; Fabian, Teubl and Binder, 2014; Frasch et al., 2014; Oppl et al., 2003; Schneider et al., 1999; US EPA, 2015a). However, probably due to the complexity and variety of existing models and testing methods (OECD, 2019b; WHO, IPCS and IOMC, 2014), most existing studies on dermal exposure do not consider any of the key variables for understanding and estimating potential risk from this route of exposure (Chaparro Leal, Guney and Zagury, 2018; Marin Villegas, Guney and Zagury, 2019; Spalt et al., 2009). The WHO reports on dermal absorption and dermal exposure (WHO, IPCS and IOMC, 2014; WHO, 2006) and the OECD guidelines for testing chemicals (OECD, 2019a) provide a detailed revision of all existing models and tools for assessing risk through dermal contact.
4.3.2. Soil health and human health links
Soil can have both a positive and negative impact on human health. Healthy soils provide the necessary nutrients and clean water to plants in order to produce our nutritious food. Human beings are increasingly aware of the influence of their diet on their general health. Governments also recognise the impact of diet on economic output and long-term population health. However, we take account of the entire life cycle of the food we eat, often focusing only on the quality of the final processing stages without considering the health of the soil that is required to sustain the 95 percent of food produced from the soil (FAO, 2015a). Nutrient-poor soils result in plants that are deficient in macro- and micronutrients, which can result in major nutritional deficiencies that primarily affect the development and survival of children when these are the main food source for a community (Oliver, 2008). Currently, about 2 billion people are estimated to suffer from micronutrient deficiencies worldwide (Ritchie and Roser, 2017).
Healthy soils are also the source of multiple antibiotic compounds and other chemicals used to produce various medicines and vaccines. Recently, a new family of antibiotics produced by soil microorganisms with no known resistance has been identified (Ling et al., 2015), which clearly illustrates the great potential of soils to support the management of drug-resistant diseases that kill about 700 000 people every year currently, and are estimated to reach 10 million deaths per year by 2050 (IACG, 2019).
In addition, soils receive pharmaceuticals and veterinary medicines from many different sources, such as improper disposal of expired medicines, urban and industrial waste, application of treated animal manure to the soil, irrigation with wastewater, but also open defecation and residues from food and livestock production. These medicines and wastes, and resistant microorganisms, entering the soil environment, can generate resistance in soil-microorganisms, losing the potential to produce new medicines and causing new health problems in humans and animals. Therefore, when antimicrobial resistance is discussed in a global context, it is considered as a “one health” problem. The environment (including soil), animals and humans are interconnected and what affects the health of one affects the health of all (CDC, 2019). In this regard, UNEP is developing a detailed report on the environmental impacts of antimicrobial resistance, including the causes of development and spread of resistance in the environment, to be published in 2021.
According to the 2017 Lancet Commission on pollution and health, soil pollution is on the rise globally and particularly affects the most vulnerable, widening the gap in development, health and well-being between rich and poor (Landrigan et al., 2018). Humans are exposed to soil contaminants either by direct soil ingestion, dermal contact or inhalation of polluted soil, or indirectly by transfer of contaminants into the food chain (Oliver, 2008; Rodríguez Eugenio, McLaughlin and Pennock, 2018).
Soils also host pathogen organisms, which may pose a serious risk to human health and the environment, exacerbated by imbalances in soil health (Oliver and Gregory, 2015). WHO estimates that around of 24 percent of the global population is affected by soil-transmitted helminths (parasitic worms), affecting primarily poorest communities without sanitary measures (Figure 18). In 2015, about 12 percent of the global population (892 million people) had no access to water, sanitation and hygiene (WASH) services and practiced open defecation in water courses and land, releasing human pathogens into the environment (WHO and UNICEF, 2017). The soils is the ideal environment for survival of human pathogens, from which these can be transferred to other hosts in contact with contaminated soil (Holcomb et al., 2020; Julian, 2016; Pickering et al., 2012).
Figure 18. Global distribution of total population of pre-school age children (Pre-SAC) aged =>1 and <5 and school age children (SAC) aged =>5 and <15 living in all the endemic areas in a country and which require preventive chemotherapy (PC) for soil transmitted helminthiasis as per data obtained by 2018.
4.3.3. Main health consequences of soil pollution
It has been mentioned several times in this report that humans are exposed to a wide variety of chemicals and natural elements that can endanger health, often in low doses, and that cumulative effects are only expressed after long periods of exposure. Many diseases, such as cancer, may not appear until decades after exposure has occurred, making it difficult to identify the cause.
Toxicological studies on humans are very difficult to conduct because of the ethical issues involved in human experimentation. Limited data are available on humans, mainly related to acute exposure, such as after an industrial accident (Eskenazi et al., 2018; Yablokov et al., 2016) or in occupational exposure studies (Adetunde et al., 2014; Alicandro et al., 2016; Fréry et al., 2020). Environmental exposure studies in the general population can be useful, although they often focus on very specific local populations. Exposure assessment is a critical step in environmental epidemiological studies, although the studies are often incomplete. The exposure of an individual or a population can change over time, and exposures to multiple chemicals are common throughout our lives. Drawing global conclusions from multiple local studies is complex because data are often collected over different time periods, using different experimental designs, and under different exposure conditions.
The effects of chemical exposures can vary, depending on the age of exposure (in utero, childhood, adult), the route of exposure (ingestion, inhalation, dermal), the amount and duration of exposure, exposures to multiple chemicals simultaneously, and other personal susceptibility factors, including genetic variability.
In addition, exposure to environmental contaminants can occur through multiple pathways described in the following sections. Environmental compartments (soil, water, air, organisms) are interrelated with a continuous exchange of matter and energy. Therefore, clearly attributing certain diseases to exposure of contaminants in the soil is complex.
Nevertheless, some attempts with epidemiological studies have been carried out in different countries by researchers and physicians (Anderson and Wolff, 2000; Boffetta, 2004; Kasuya, 2000; Marinaccio et al., 2015; Santoro et al., 2017; Wigle et al., 2008), and the competent authorities in some countries regularly carry out epidemiological studies of certain contaminants in humans (Figure 19).
Figure 19. Availability of epidemiological studies carried out by governmental organizations or departments on the impacts of certain soil contaminants on human health.
WHO has identified ten top contaminants of human health concern (WHO, 2010), of which nine are soil contaminants, due to the well-known impacts on human health and wide geographical incidence (Figure 20). Organic and inorganic contaminants exhibit four main mechanisms of toxicity, acting as endocrine disruptors, or carcinogens, neurotoxins or teratogens. They can also induce cellular oxidative stress and the production of stress proteins (Landrigan et al., 2018; Stohs and Bagchi, 1995).
Figure 20. WHO’s top 10 chemicals of public health concern.
Endocrine disruptor
The endocrine system secrets diverse hormones involved in the control of the metabolism, maturation, growth, body and neurological development, and reproduction. As defined by the International Programme on Chemical Safety, “an endocrine disruptor is an exogenous substance or mixture that alters function(s) of the endocrine system and consequently causes adverse health effects in an intact organism, or its progeny, or (sub)populations” (IPCS, 2002).
Endocrine disruptor contaminants have several mechanisms of action. They can show a similar chemical structure to hormones and substitute for these in the hormone receptors, alter the normal hormone functioning, alter the synthesis or metabolisms of hormones or initiate processes at abnormal times in life (Figure 21) (Kortenkamp et al., 2011). Endocrine disruptive chemicals interfere with reproduction in humans, and advances in molecular technologies are providing insight into the causative mechanisms, which include gene mutation, DNA methylation, chromatin accessibility and mitochondrial damage (Messerlian et al., 2017). There is compelling evidence that frequent exposure to environmental toxins has large potential to mediate overall fertility potential (Xue and Zhang, 2018), DNA methylation (Gonzalez-Cortes et al., 2017), apoptosis (Clemente et al., 2016) and chromatin/DNA fragmentation (Gaspari et al., 2003).
Figure 21. Endocrine disruptor’s mechanism of action. An endocrine disruptor can decrease or increase normal hormone levels (left), mimic the body’s natural hormones (middle), or alter the natural production of hormones (right).
Although some uncertainties still exist about the mechanisms of action of endocrine disruptors in human health, growing evidence in wildlife, experimental animals and human populations call for immediate action on the presence of these contaminants in the environment (Bergman et al., 2013; IPCS, 2002). Some of the effects that have been attributed to environmental exposure to endocrine disruptors include the decline in fertility including in sperm quantity and mobility, precocious puberty, and hormone-related cancers (breast, ovarian, prostate, testicular and thyroid cancers). As highlighted by Bergman et al. (2013), more than 800 chemicals have or may have endocrine disrupting effects. However, existing studies encompass only a small fraction of these chemicals’ effects on intact organisms. Some of the most studied endocrine disruptors present in polluted soils are arsenic, BPA, dioxins, PAHs, PCBs, phthalates, several pesticides (DDT, HCH, fenitrothion), and polybrominated diphenyl ethers (PBDEs).
Genotoxicity and mutagenicity
Genotoxicity refers to the ability of any contaminant to damage the genetic information in a cell, causing changes in chromosomes or DNA and gene mutations (Stammberger, Czich and Braun, 2013). When genotoxicity involves unscheduled DNA synthesis, sister chromatid-exchanges or DNA chain breaks, these are not necessarily transmissible from cell to cell or generation to generation, although cancer and local alterations may occur. Mutagenicity, on the other hand, involves the production of transmissible genetic alterations. Cells prevent expression of the genotoxic damage by either DNA repair or apoptosis (cell death); however, the damage may not always be rectified and this leads to mutagenesis (Gupta, 2016).
Damage to the genetic material can occur in the somatic cells (Figure 22), which are responsible for the formation of tissues and organs, or in the germ cells, which are responsible for the formation of the gametes, (i.e., the ovules and sperm cells), which hold the genetic information transmitted to the embryo. If mutations affect somatic cells, cancer results, and a variety of genetic and degenerative diseases occur, such as accelerated ageing, immune dysfunction and cardiovascular and neurodegenerative diseases. Mutations in germ cells can lead to miscarriages, infertility or hereditary damage in the offspring and possibly transmission to subsequent generations (Bingham, 2017).
Figure 22. Main DNA damages caused by genotoxic agents.
Radiation, trace elements such as chromium, cadmium, nickel and cobalt, and PAHs are common soil contaminants that have genotoxic and mutagenic effects (White and Claxton, 2004).
Teratogenicity
Teratogenicity refers to the ability of any contaminant (physical, chemical or biological) to induce abnormalities in the foetus after exposure during pregnancy (Genetic Alliance and District of Columbia Department of Health, 2010). Abnormal foetal development produced by teratogenic agents can manifest itself as malformation(s), growth retardation, impaired neurodevelopment, functional disorder, or even prenatal death of the fetus. The first quarter of pregnancy has the highest risk for the foetus due to exposure to teratogens (Figure 23). Soil contaminants characterized as teratogens are, for example, arsenic, ionizing radiation from radon and its decay products, organic mercury compounds, PCBs, certain pesticides and industrial solvents (The Collaborative on Health and the Environment, 2019).
Figure 23. Stages of organ development and critical periods when the fetus is most susceptible to teratogen-induced birth defects. Dark blue denotes the highly sensitive periods when major defects can occur and the organ affected in each phase. Light blue indicates the stages that are less sensitive to teratogens and where minor defects can be induced. CNS = central nervous system.
Neurotoxicity
Neurotoxicity occurs when exposure to contaminants (neurotoxicants) causes adverse effects on the structure and/or the normal activity of the nervous system (Spencer and Lein, 2014). Autism, attention deficit disorder, intellectual disability and reduced IQ, or cerebral palsy are some common neurodevelopmental disorders. Neurodevelopmental disorders can have a genetic component but can also be related to environmental factors, including exposure to environmental contaminants. A long list of environmental (and soil) contaminants have recognized neurotoxic effects in humans (Grandjean and Landrigan, 2006). Lead, mercury, and PCBs are well-studied soil contaminants with neurotoxic potential (US EPA, 2013). Other contaminants such as arsenic, DDT and organochlorine pesticides, manganese, tin, PBDEs, PAHs, phthalates and bisphenol A have also been associated with neurotoxic effects (Figure 24). The neurotoxic potential of many contaminants of emerging concern has been observed in in vitro and in vivo studies on animals, but there is still much research necessary to elucidate the possible effects of all existing chemicals in the environment and the possible interactions between contaminants (Lei et al., 2015; Yang et al., 2019).
Figure 24. Main effects of soil contaminants on human health, indicating the organs or systems affected and the pollutants causing them.
Although neurotoxicity can be expressed throughout our lives, foetal exposure causes the greatest effects in brain development (Grandjean and Landrigan, 2006). Infants and children are also highly vulnerable to neurotoxicant contaminants exposure, and effects can be irreversible and more harmful during these early developmental stages than in adulthood (Miodovnik, 2011).
Carcinogenicity
According to the Globally Harmonized System of Classification and Labelling of Chemicals, carcinogenicity refers to the ability of a physical phenomenon (e.g. ionizing radiation), or of a chemical or biological agent to cause cancer or increase its incidence (United Nations, 2011).
The International Agency for Research of Cancer (IARC-WHO) has developed a classification on the identification of carcinogenic hazards to humans, organized into four groups according to the potential carcinogenic risk (Cancer is the second leading cause of death in the world; in 2018, one in five people developed cancer and it was the cause of one in six deaths in 2018 (WHO, 2020b). Environmental and occupational exposures were responsible for 12 to 29 percent of annual deaths at the beginning of the 21st century, but this value could be much higher today (Prüss-Üstün and Corvalán, 2006). Table 3). The IARC list includes many soil contaminants that have been addressed in this report. The risk of cancer is determined by the exposure to a single contaminant or a mixture of contaminants, through different routes (ingestion, dermal contact or inhalation), in a given period of time (punctual, temporary or throughout life) (Murdoch and Krewski, 1988).
Table 3. International Agency for Research of Cancer (IARC-WHO) classification of agents according to their carcinogenic risk.
Cancer is the second leading cause of death in the world; in 2018, one in five people developed cancer and it was the cause of one in six deaths in 2018 (WHO, 2020b). Environmental and occupational exposures were responsible for 12 to 29 percent of annual deaths at the beginning of the 21st century, but this value could be much higher today (Prüss-Üstün and Corvalán, 2006).
Although the following sections mention some human diseases attributable to exposure to some of the most common soil contaminants, other more complete sources are available. Some of the more complete databases and monographs that provide specific details include the Toxicant and Disease Database prepared by the Collaborative on Health and the Environment for a broader view of the health effects of many contaminants (The Collaborative on Health and the Environment, 2019), multiple documents on the IARC monographs (IARC, 2020b), the eChem Portal of the OECD (OECD, 2020), and the indicators provided by the Global Health Observatory of WHO (WHO, 2016a), and the National Toxicology Program of the United States of America Department of Health and Human Services (NTP, 2019).
4.3.3.1. Health consequences of exposure to trace elements
Determining precisely the cause of chronic health conditions such as developmental delay or cancer is highly complex, since these conditions often develop after prolonged periods of exposure to the carcinogens and teratogens compound(s) and it may take years to manifest and be detected.
Some trace elements are essential to human (mammals) metabolism, like boron, copper, chromium, zinc, nickel and molybdenum, but others have no known function, such as cadmium or lead (Oliver and Gregory, 2015). Several trace elements, both essential and non-essentials, have been demonstrated to result in toxic effects when in high concentrations and can cause different diseases, from vascular disorders to neurological and developmental deficits. For example, a study of the cancer incidence and the levels of trace elements in topsoil in Spain found a significant relationship between increased concentration of several trace elements in soils and certain cancers, such as cancers of the digestive system in areas with high concentrations of cadmium, copper, lead and zinc in soils, bladder cancer in soils with high cadmium concentrations, oesophageal cancer in areas with higher levels of lead, and brain cancer in soils with arsenic (López-Abente et al., 2018).
Availability and toxicity of inorganic contaminants mainly depends on soil properties such as organic carbon content, type and content of clay, cation exchange capacity or pH, and on the amount of contaminants released into the environment (Carré et al., 2017).
Arsenic
Arsenic may be involved in DNA methylation and cancer prevention (Oliver and Gregory, 2015), however chronic exposure can cause skin lesions such as hyperpigmentation, keratosis and ulceration, respiratory system problems, cardiovascular disease, neurological and developmental alterations, haematological and immunological disorders, reproductive complications and cancer (Abad-Valle et al., 2018; Kapaj et al., 2006). Arsenicosis is a disease related to the exposure to arsenic (Huq et al., 2006) According to the (JECFA, 2011c) evidence strongly supports an association between inorganic arsenic ingestion and skin cancer, urinary bladder and lung and skin lesions.
Contaminated drinking water is the major source of arsenic to humans, which is particularly relevant in some South and Southeast Asian countries (see Chapter 6) (Singh et al., 2015). Arsenic in drinking water comes mainly from the alteration of arsenic-containing minerals, which leaches from the soil into the groundwater. The current threshold value for arsenic in water is 10 μg/L, although this value might not be enough protective due to the high toxicity of arsenic (Ahmad and Bhattacharya, 2019). The irrigation of agricultural soils with arsenic-contaminated groundwater is an important exposure pathway due to the retention and long-term transference of arsenic from soils to crops (Dahal et al., 2008; Gillispie et al., 2015). In Bangladesh, arsenic-contamination of groundwater and the subsequent irrigation of agricultural areas with contaminated water has led to the transfer of arsenic to soils, accounting for as much as 5.5 kg of arsenic per hectare each year (Huq et al., 2006), transferring to vegetables and cereals, resulting one of the worst health issues in the country, affecting millions of people (Islam et al., 2017; Khan et al., 2010; Naujokas et al., 2013).
Populations chronically exposed to arsenic show severe health deterioration, including cancers, melanosis, hyperkeratosis, restrictive lung disease, peripheral vascular disease, gangrene, diabetes mellitus, hypertension and ischemic heart disease (WHO, 2018b), with high incidence in the south and south-eastern parts of Asia, but also in the United States (Naujokas et al., 2013). Children are especially sensitive to arsenic intake due to an immature detoxifying system that is not able to methylate arsenic into less toxic forms (Egendorf et al., 2020). Arsenic may also be responsible for the emergence of chronic kidney diseases of unknown aetiology that have been reported in agricultural areas of Sri Lanka and which are possibly linked to the use of arsenic-rich fertilizers (Jayasumana et al., 2015). More than 3 billion people worldwide are exposed to chronic low-level arsenic through the ingestion of rice that could be related to a higher cardiovascular disease risk (Xu et al., 2020).
Cadmium
Cadmium is one the main foodborne contaminants related to health problems, and therefore was included in regulations proposed by the FAO/WHO Expert Committee on Food Additives (JECFA). In Asia, rice produced in cadmium-contaminated soils is the main route of exposure to cadmium (Chen et al., 2016). The provisional tolerable weekly intake (PTWI) for cadmium is 25 µg per kg of body weight (WHO, 1993). Cadmium mainly accumulates in the liver and kidneys and is long-persistent in human body (WHO, 1993). It can cause kidney damage, renal tubular dysfunction, pulmonary emphysema and itai–itai disease, which cause osteoporosis and wear of bone structures by cadmium replacement of calcium in bones (Kirkham, 2006). Additionally, dietary cadmium intake from contaminated rice has been associated with an increased risk of postmenopausal breast cancer (Itoh et al., 2014). Cadmium-poisoned patients are characterized by the presence of osteoporosis, severe bone pain and ease of bone breakdown and renal tubular dysfunction (Aoshima, 2016). The main organs affected by chronic cadmium poisoning are the kidneys, which causes a deficiency of D vitamin and weakening of bones (Baba et al., 2013).
One of the best-known cases is the itai-itai disease caused by the ingestion of food contaminated with cadmium from polluted soils. This was first reported in Japan, in the Jinzu River basin around 1912, where rice paddy soils were polluted due to continued irrigation with the river water contaminated by zinc mine waste upstream (Aoshima, 2016). The area is considered as endemic for the itai-itai disease although cadmium poisoning has also been reported in other areas worldwide. Cadmium exposure through intake of contaminated rice is unequivocally related to proximal renal tubular dysfunction in humans, however, no direct relationship has been established with any other crop due to zinc phytotoxicity associated with cadmium uptake (Chaney, 2015).
Chromium
Chromium is present in nature mainly as two stable oxidative states, trivalent and hexavalent chromium (Cr(III) and Cr(VI)). Trivalent chromium (Cr(III)) has been considered an essential element involved in the metabolism of glucose, fat and protein, and in various enzyme reactions (Bielicka, Bojanowska and Wiśniewski, 2005), although more recent studies may challenge this assumption (Di Bona et al., 2011; EFSA Panel on Dietetic Products, Nutrition and Allergies, 2014). Chromium is mainly present in the reduced form in the majority of soils (Séby and Vacchina, 2018), but in some cases, hexavalent chromium can be highly mobile in soils and migrate to drinking groundwater. Hexavalent chromium has been detected in harmful concentrations in drinking water in many parts of the world (Hausladen et al., 2018; Kaprara et al., 2015; Mishra and Bharagava, 2016; Tseng, Lee and Chen, 2019).
Chromium can be mobilized from polluted soils in the form of aerosols causing lung cancer (WHO, 2003). Cr(III) is poorly absorbed by the organism if ingested, although its absorption increases with inhalation. On the other hand, hexavalent chromium (Cr(VI)) is a recognized genotoxic and carcinogenic element. Its effects have been widely demonstrated and accepted through inhalation exposure (Soares, Vieira and Bastos, 2010). Health effects attributed to Cr(VI) via ingestion are gaining relevance (Sun, Brocato and Costa, 2015). Cr(VI) is thought to be rapidly reduced to Cr(III) when ingested with contaminated food by the acidic conditions of the saliva and gastric juices (Sun, Brocato and Costa, 2015), although a low percentage remains as Cr(VI) and may cause cancer (McLean et al., 2012). When Cr(III) penetrates cells, it binds to DNA and induces DNA damage, chromosomal aberrations, alterations in the epigenome and instability of microsatellites, along with inflammatory and immunological responses (McLean et al., 2012; Sun, Brocato and Costa, 2015). Genetic and epigenetic changes can lead to the proliferation of malignant cancer cells (Nickens, Patierno and Ceryak, 2010). Another line of study suggest that reduction of Cr(VI) in Cr(III) produces reactive oxygen species that cause inflammation, DNA damage and mutation.
Copper
Copper is an essential element involved in the formation of redox enzymes and iron metabolism, and is essential for the development of key metabolic systems, such as central nervous system, the cardiovascular system and the immune function (Collins, 2017; Oliver and Gregory, 2015). Copper is found in our bodies in nanograms per gram to micrograms per gram concentrations (Collins, 2017). Our body presents a delicate copper homeostasis that regulates copper balance and excess of copper is excreted through liver and gastrointestinal secretions. However, due to an immature biliary excretion system, copper exposure poses a higher risk to the foetus and neonates (Royer and Sharman, 2020). Chronic and acute exposure to ionic copper, mainly through ingestion of contaminated food or occupational exposure, alters the body’s homeostasis and causes several diseases. Excess copper promotes the formation of reactive oxygen species and causes the inactivation of enzymes, gastrointestinal distress, hepatic necrosis and even sperm dysfunction (Kasperczyk et al., 2015). Severe acute toxicity can lead to methemoglobinemia, hepatic necrosis, cardiac and renal failure and ultimately death (Royer and Sharman, 2020). The excess of copper in children is associated with the idiopathic copper toxicosis, characterized by high levels of copper in the liver, which presents abnormalities, and can lead into death (Coenen and Houwen, 2019). This syndrome has been identified in India and Tyrol, associated with the ingestion of copper-contaminated food (Coenen and Houwen, 2019).
Lead
Lead is one of the most widespread soil contaminants worldwide, with major occurrence in industrial, mining and urban areas. Lead exists in insoluble Pb2+ forms in soils, and is strongly sorbed to clay minerals and organic molecules (Alloway, 2012). Lead cannot be degraded by microorganisms and is highly toxic to plants and soil-dwelling organisms (Amari, Ghnaya and Abdelly, 2017; Oliver and Gregory, 2015). Lead can enter the human body through different pathways, but intake with contaminated food grown in polluted soil is a matter of concern. WHO and FAO have recently withdrawn the previous PTWI of 0.025 mg/kg of body weight determining that no protective value ensures health protection after long-term exposure (WHO, 2011). Severe cases of lead poisoning have been reported worldwide, and about 1 million deaths per year are attributable to lead poisoning (O’Connor et al., 2020). Lead exposure is responsible for nearly 1.5 percent of the global burden of disease and affects 800 million children worldwide (UNICEF and Pure Earth, 2020).
Lead has a range of effects on human health depending on the concentrations in blood, and affects virtually all organs (WHO, 2017a). Lead exposure causes brain damage, resulting in intellectual disability. Children exposed to lead during pregnancy and early development show lower IQ and deficit in cognitive ability (UNICEF and Pure Earth, 2020). Lead exposure is also attributed to aggressive or violent behaviour (Mathee et al., 2018). In adults, lead exposure results in haematological effects, producing an increase in blood pressure and other cardiovascular diseases (EC, 2006). Recent morbidity and mortality data associated with lead exposure show that the greatest risk is in disadvantaged communities, who will suffer more from the consequences of stressors that reduce IQ, as these are populations in which IQ is usually already lower than the average (Gilbert and Weiss, 2006), and less developed countries where regulations do not exist or are less strictly enforced (O’Connor et al., 2020).
Mercury
Concerns about mercury poisoning started in 1956, when severe methylmercury poisoning occurred in the city of Minamata, Japan, due to the ingestion of mercury-contaminated fish from Minamata Bay. Almost 3 000 people developed neurological disorders, affected by so-called Minamata disease (Yorifuji et al., 2015).
Mercury is one of the most widespread contaminants. It has been extracted and used practically since the beginning of the human Neolithic age and has significant global mobility (Beckers and Rinklebe, 2017). Mercury has numerous and well-known health effects in humans, including cardiovascular, reproductive, and developmental toxicity, neurotoxicity, nephrotoxicity, immunotoxicity, and carcinogenicity, and as such is considered by WHO as one of the top ten contaminants of health concern (WHO, 2017b).
Mercury is naturally found in soils at global average concentration around 0.1 mg/kg, although values are highly variable (Beckers and Rinklebe, 2017; Kabata-Pendias, 2010). Mercury is present in soils in three forms: elemental or metallic mercury, and inorganic and organic complexes of ionic mercury (Hg2+). Humans are mainly exposed to mercury as the organic form of methylmercury, which is a potent neurotoxin, easily absorbed by the gastrointestinal tract. The main route of exposure is through the ingestion of contaminated fish and shellfish, but ingestion through other foods such as rice, cabbage, spinach, radish, lettuce and corn occurs when grown in mercury-polluted soils (Table 2) (Qiu et al., 2008; Shao et al., 2012). Plants can absorb dissolved mercury from the soil solution, accumulate it in the roots or translocate it to other tissues (Beckers and Rinklebe, 2017). Rice-rich diets with rice produced in or near mining areas can be an important source of mercury exposure, even more relevant than contaminated fish consumption for inland populations (Li et al., 2015b). Intake of methylmercury-contaminated rice is of particular concern in some regions of China and Indonesia (Rothenberg, Windham-Myers and Creswell, 2014), but this may be relevant in other regions where imported contaminated rice is consumed (Brombach et al., 2017). High concentrations above tolerable daily intakes have also been reported in other crops and grains in areas heavily polluted in China (Li et al., 2017b). According to the FAO/WHO Expert Committee on Food Additives (JECFA) guidelines, the provisional tolerable weekly intake for total mercury and methylmercury intake with food are 4 µg/kg and 1.6 µg/kg of body weight, respectively (JECFA, 2007a, 2011a).
Occupational exposure is especially relevant for small-scale artisanal gold mining workers and their families, who are exposed to direct inhalation of mercury vapours during the burning of mercury-gold amalgam balls for gold extraction, but are also affected by soil pollution from mercury deposition in the ground and from soil vapour emissions (Beckers and Rinklebe, 2017; Pure Earth, 2017).
Mercury, in its vapour and organic forms, may cross the blood-brain and placental barriers (Cariccio et al., 2019; Kern et al., 2020). High bioaccumulation occurs especially in the liver, brain, kidney and muscles (Branco et al., 2017) with half-life of years to decades in human tissues (Bjørklund et al., 2017b). Mercury, both in inorganic ionic form (Hg2+) and as methylmercury, alters the electron transport chain of mitochondria and consequently increases the production of oxidative species that contribute to cell apoptosis and neurodegenerative disorders (Belyaeva et al., 2012; Mori et al., 2011). Babies are especially vulnerable as they can be exposed both by transfer through the placenta during pregnancy and through breast milk, leading to reduced and impaired development of the foetal and neonatal brain (Straka et al., 2016). Genchi et al. (2017) also attribute cardiovascular diseases to mercury exposure.
The main symptoms and effects of exposure to mercury are intellectual disability, primitive reflexes, hyperkinesia, deafness, blindness, cerebral palsy, cerebellar ataxia, convulsions, strabismus, dysarthria, deformities of the limbs, paraesthesia, and ultimately loss of neural cells, resulting in ataxia and constriction of the visual field (Beckers and Rinklebe, 2017; Cariccio et al., 2019; Yorifuji et al., 2015). Effects depend on the mercury concentration and speciation, and on the exposure route (Beckers and Rinklebe, 2017).
Zinc
Zinc is the most abundant trace element in soils, with background concentrations of 10 to 100 mg/kg (Alloway, 2012). Zinc is an essential element, involved in gene expression, spermatogenesis and DNA metabolism and repair. Zinc deficiency affects the response to oxidative stress and gene expression and is associated with high mortality and morbidity, especially in children (Caulfield and Black, 2004). Globally, zinc deficiency is attributed for a loss of 16 - 28 million disability-adjusted life years (DALYs)10 (Caulfield and Black, 2004; Fischer Walker, Ezzati and Black, 2009).
On the other hand, zinc pollution is found in soils near mining areas or where metallurgical industrial activities take place. Volcanic activities, forest fires and dust storms are also a significant source of zinc pollution (Alloway, 2012). Zinc is highly mobile and relatively bioavailable in soils (Baran et al., 2018). Elevated concentrations of zinc in soils can have phytotoxic and ecotoxic effects on soil-dwelling organisms, which produce physiological and biochemical changes that prevent the uptake, limiting entry into the food chain (Alloway, 2012; Ferreira et al., 2018). Therefore, zinc poisoning is rare in humans although is an important consideration in environmental pollution (Plum, Rink and Haase, 2010).
4.3.3.2. Health consequences of exposure to other inorganic contaminants
Other inorganic soil contaminants must also be considered although these are usually less of a concern than trace elements because of generally lower concentration and lower toxicity.
Nitrates and phosphates
Nitrogen is an essential element for all living organisms. It is one of the major nutrient requirements for plant growth and is frequently a limiting factor for plant growth in many soils. Non-reactive nitrogen (N2) is the most abundant gas in the atmosphere and can only be used by plants by the action of N-fixing soil organisms, some of which are symbiotic such as Rhizobium species with legumes, or Azolla spp with blue green algae, and others that are free living organisms closely related with the plants, such as Azotobacter spp (Shridhar, 2012). Once fixed, nitrogen is present in soils in a multiple of forms, such as organic nitrogen, ammonium, nitrite and nitrate (Powlson, 1993). To address nitrogen soil deficiencies, synthetic and organic fertilizers are applied to soils to fulfil plants’ needs, but in many cases, nitrogen inputs have been larger than the crop needs (Sutton et al., 2011). This excess in soil has led to nitrate leaching to groundwater due to its high solubility with transport to surficial water bodies and oceans in runoff. Together with an excess of phosphorous and other nutrients such as sulphur and other minor trace elements, nitrogen surplus produces important environmental consequences (see section 4.2.3).
The ingestion of green leafy vegetables is the main route of exposure to nitrate for humans, representing between 60 to 80 percent of nitrate intake (Weitzberg and Lundberg, 2013). Some crops also show increased nitrate content due to high concentrations in the soil, especially green vegetables such as lettuce, spinach, rocket and beetroot, which can accumulate more than 1 000 mg/kg nitrates. Although other internal and external factors control the nitrate content in plants, when nitrogen fertilizers are applied immediately before harvesting, plant concentrations are greater, and thus this practice should be avoided (Tamme, Reinik and Roasto, 2010). According to the data considered by the Joint FAO/WHO Expert Committee on Food Additives, nitrates and nitrites do not result in genotoxic nor carcinogenic effects in humans, but due to other health effects an acceptable daily intake of 0–3.7 mg/kg b.w. of nitrate ion is recommended, although this is not applicable for infants younger than 3 months old (JECFA, 2002).
The major health effect associated with nitrogen pollution is methemoglobinemia caused by the ingestion of nitrate-polluted water (Ludlow, Wilkerson and Nappe, 2020; Rehman, 2001). Nitrates favour the oxidation of haemoglobin into methaemoglobin due to the oxidation of Fe2+ to the Fe3+. Methaemoglobin is not able to transport oxygen in blood causing hypoxia in tissues (Ludlow, Wilkerson and Nappe, 2020) Methemoglobinemia has been diagnosed mainly in infants under three months of age, although a number of cases have also been reported in children and adults. The main symptoms of methemoglobinemia are cyanosis, asphyxia, and suffocation (Rehman, 2001; Tamme, Reinik and Roasto, 2010). Additionally, high levels of nitrate consumption have been identified as a risk factor in the development of stomach cancer and have been linked to other disorders such as reduced cognitive developmental, mainly attributed to nitrosation inside the body after consumption (Balazs Carolina et al., 2011; Fan and Steinberg, 1996; Tamme, Reinik and Roasto, 2010). Ingested nitrates are converted to nitrite and nitric oxide by oral and gastric bacteria, and can also be converted into nitrosamines in acidic stomach, which were thought to be responsible of carcinogenicity, although recent evidence does not show clear evidence of this, but instead suggests a positive role of dietary nitrates on human health (Ma et al., 2018; Weitzberg and Lundberg, 2013). In another study, Inoue-Choi and co-workers (2015) found evidence of a link between dietary nitrate intake and ovarian cancer in postmenopausal women (Inoue‐Choi et al., 2015).
Phosphorous is also an essential macronutrient for organisms and is the second most limiting factor in soils for crop growth (Shen et al., 2011). It is applied to soils as phosphate fertilizers and in organic fertilizers such as manures or sewage sludge. Although phosphorous is relative immobile in soils, over-fertilization leads to leaching and transport through runoff of phosphate to water bodies contributing to their eutrophication (Schröder et al., 2010). Additionally, an excess of phosphorous in an available form – phosphate- in soil is taken up by plants and accumulated in edible parts (Fernandes et al., 2017). Dietary phosphorus intake is the largest source of this essential element for humans, and intake has increased in recent decades with the addition of phosphate salts to processed foods for preservation (Calvo and Uribarri, 2013a). The natural content of phosphorus in protein-rich foods (dairy products and meat) and in those crops grown on over-fertilized soils are also an important source of dietary phosphorus (Calvo and Uribarri, 2013a). Although about 98 percent of the phosphorus ingested is excreted in faeces and urine (Erem and Razzaque, 2018), important health effects in the cardiovascular system may result, with more acute effects in individuals suffering from previous renal dysfunction (Calvo and Uribarri, 2013b; Erem and Razzaque, 2018). Elevated levels of phosphates in human serum alter the functioning of bone-derived fibroblast growth factor 23 and parathyroid hormone, and also alter calcium metabolism to compensate for the increase in phosphate. Both hormones and calcium are involved in bone metabolism and renal and cardiovascular functioning (Calvo, Moshfegh and Tucker, 2014). Elevated serum phosphate is related to oxidative cellular stress, bone deterioration, renal dysfunction and arterial calcification (Calvo and Uribarri, 2013a).
Radionuclides
Soils can contain natural radionuclides (e.g. polonium-210, lead-210, potassium-40, radium-226/228, thorium or uranium) or radionuclides derived from anthropogenic activity (cesium-137 and strontium-90), such as nuclear power waste and accidents (e.g. Chernobyl), uranium, copper, gold and polymetallic mining, nuclear weapons testing and use (e.g. Hiroshima and Nagasaki), or radiological medical waste (Steffan et al., 2018). Humans are exposed to radiation through two main pathways: external exposure by being close to a source of radiation, or internal exposure when radionuclides enter the body (WHO, 2016b). This section will only focus on the internal exposure, which is related to radionuclides in soil. Radionuclides can enter our body as any other contaminant, by inhalation of radioactive gases or contaminated particles, by ingestion of contaminated food and water, and by dermal contact with contaminated soil (UNSCEAR, 2020). However, direct inhalation of radionuclides (e.g. radon) and ingestion of contaminated food are the main sources of internal ionizable radiation, while inhalation and ingestion of soil particles contaminated with radionuclides have a much lower impact on cancer risk (Spasic Jokic, Zupunski and Gordanic, 2016). The WHO considers that soil gas infiltration in indoor air is the greatest source of exposure of radon (WHO, 2009).
Radon is the most common natural radionuclide present in soils around the world. It is an inert gas from the uranium and thorium decay series, highly mobile in soil, and accumulates in indoor ambient air (ATSDR, 2012b). The main route of exposure to soil radon is through inhalation. We are normally exposed to low concentrations of radon (global range of annual dose 2-10 millisieverts (mSv)11), which together with the natural external radiation we receive from the sun and the cosmos, represent the natural background radiation, which on average is about 10 mSv per year (UNSCEAR, 2020). Once radon (or any other radionuclide) enters our body and starts disintegrating, emitting radiation is measured in activity instead of dose, for which the unit is becquerels (Bq). One becquerel (Bq) represents one disintegration of a radioactive atom per second (UNSCEAR, 2020). In some places in the world, the radon exposure is much higher than the global average (Figure 25). Radon exposure is responsible for 3 percent of lung cancer deaths in the 66 countries that are included as having reliable radon surveys (Gaskin Janet et al., 2018).
Figure 25. World map of average national residential radon levels with data up to 2007.
Radon is considered a potent carcinogenic to humans (IARC, 2020a). According to evaluation carried out by CAREX Canada, the cancer risk from radon is orders of magnitude higher than other environmental contaminants, such as formaldehyde, asbestos or car engine exhaust (Gue, 2015).
Ingestion represents an important share of the radiation dose we receive (Committee on the Analysis of Cancer Risks in Populations near Nuclear Facilities-Phase I et al., 2012). International standards limit the internal radiation from foodstuff to 1 mSv/y over the natural background doses (Guillén Gerada, 2016). Humans are also exposed to other radionuclides present in soils through ingestion of contaminated plants and animals. Soil-to-plant transfer of radionuclides, such as polonium-210, lead-210, potassium-40 or radiocaesium-137 is relevant for human health, because radionuclides are translocated to edible parts and present a carcinogenic risk (Adesiji and Ademola, 2019; Cleveland, Hinck and Lankton, 2021; Gwynn, Nalbandyan and Rudolfsen, 2013). Transfer of man-made radionuclides from soil to plants and animals also represents an important source of carcinogenicity risk, as reported by Mitrović and co-workers, who observed high levels of radiocaesium in mushrooms, and cow, sheep, goats and wild animal milk and meat, although the effective dose derived from ingestion was below the international standard (Mitrović et al., 2009). However, the health effects attributed to ionisable radioactivity from foodstuff is highly variable among populations because this depends on background, anthropogenic radionuclide concentrations, and dietetic habits (Guillén Gerada, 2016).
Natural and human-made radionuclides emit ionizing radiation that causes alterations in DNA, which leads to mutations and alterations of cells. Our cells have a DNA repair mechanism that consists of repairing the mutations produced in the DNA or killing the cells if repair is not possible. If the number of cells killed is too large, this leads to organ dysfunction (Figure 26). In addition, sometimes these repair mechanisms are unsuccessful and the changes in DNA are transmitted through cell division, and ultimately lead to the formation of a cancer (UNEP, 2016). Exposure to low levels of ionizing radiation over long periods has been associated with different cancers, such as thyroid, leukaemia, salivary gland, lung, bone, oesophagus, stomach, colon, rectum, skin, breast, kidney, bladder, and brain cancer (IARC, 2014; UNSCEAR, 2020). Exposure to ionizing radiation has a long-term effect on the risk of cancer, and the effects may become apparent after several years or decades of exposure (IARC, 2020c). A clear example of the effect of radiation on increased cancer risk was seen in the population of Ukraine, Belarus, and the western part of the Russian Federation affected by high-dose exposure following the Chernobyl nuclear accident in childhood or adolescence. One-quarter of thyroid cancers that developed in adulthood have been attributed to these radionuclide exposures (IARC, 2020c). UNSCEAR sets an equivalent cancer-causing dose limit above 10 mSv/year, and above 1 000 mSv/year for immediate cancer development and death (UNSCEAR, 2020).
Figure 26. Radiation-induced DNA damage and cell repairing mechanisms.
The population can also be exposed to other radionuclides, such as uranium. Naturally occurring uranium is present in almost all parent rocks and soils (ATSDR, 2013). In addition, uranium can accidentally be released into the environment from fertilizer application, nuclear power facilities, nuclear accidents, and mining operations (see Chapter 3). Depleted uranium, a less radioactive form, has multiple military applications and has been used in numerous armed conflicts around the world (Hon, Österreicher and Navrátil, 2015). Depleted uranium-contaminated areas are distributed all over the world, not only in war zones, but also in experimental and training sites (Callahan, Kostecki and Reece, 2004).
Plants can uptake uranium from polluted soils (Boghi, Roose and Kirk, 2018; Sevostianova et al., 2010) and uranium can also attach to the plant roots, which when ingested by humans can cause diverse health damage (Schnug and Lottermoser, 2013). Accidental ingestion of uranium-polluted soil particles could also represent an important route of exposure for certain populations (Callahan, Kostecki and Reece, 2004). Uranium is relatively mobile in soils, especially alkaline soils with low clay and organic carbon content, and can be leached into groundwater or transported by runoff to neighbouring water bodies (Almahayni and Vanhoudt, 2018; Bigalke et al., 2018). Therefore, the intake of contaminated food and drinking water is the main route of exposure for the majority of the population. People living close to uranium mining areas, agricultural areas fertilized with uranium-rich fertilizer, or in areas where depleted uranium weapons have been used are exposed to higher levels of uranium (ATSDR, 2013; Schnug and Lottermoser, 2013). Inhalation of uranium-contaminated particles is also a potential route of exposure, which can lead to the absorption into the bloodstream of up to 5 percent of inhaled uranium (ATSDR, 2013).
Concerns of uranium effects on human health have led to an extensive body of research and epidemiological studies. Uranium affects human organs and tissues both due to the emitted radiation and chemical interactions, with the latter being predominant (Almahayni and Vanhoudt, 2018; ATSDR, 2013). Uranium is rapidly metabolized forming different compounds such as salts, or carbonate and citrate complexes (Bjørklund et al., 2017a). The kidneys are the main organ affected by uranium, where it accumulates and is slowly excreted through urine, causing changes in renal tubules (Faa et al., 2018; McDiarmid et al., 2006). Uranium also exerts a genotoxic effect on human cells, which may even affect the birth sex-ratio, as was observed in the Iraqi population affected by the depleted uranium weapons bombings. In this case the rate of male new-borns was much lower than in normal populations (Faa et al., 2018). The International Agency for Research on Cancer does not consider uranium as carcinogenic to humans (IARC, 2020a); and studies showing a higher incidence of lung cancer among uranium miners have attributed the cancer risk to radon (ATSDR, 2013).
Asbestos
The effects of naturally occurring asbestos on health are well-known especially for occupational exposure (Barlow et al., 2017). Asbestos is responsible for approximately half of occupational cancer deaths and 80 percent of mesothelioma cases (WHO, 2014). According to the IARC Monograph from 2012, all types of asbestos are included in Group 1 as carcinogenic to humans (IARC, 2012). Although many international and national efforts have occurred to reduce asbestos mining and use, and to increase the safe disposal (Spasiano and Pirozzi, 2017), asbestos are still mined and used in many countries posing a significant risk to human health now and into the future (Frank and Joshi, 2014; Røe and Stella, 2017).
Although environmental exposure to asbestos is less relevant than occupational or indoor air exposure in housing and buildings containing friable asbestos materials, environmental exposure can be relevant for some populations, mainly those living in asbestos-rich areas (Corsica in France, Cyprus, Turkey, and New Caledonia), close to asbestos mining areas and factories, where asbestos have been landfilled, and for farmers working on asbestos-polluted soils (Andujar et al., 2016; Turci et al., 2016).
The inhalation of these small fibres or asbestos-contaminated dust is linked to mesothelioma, a cancer that most frequently appears in lungs but can also affect the abdomen or pericardium (Molinari and Stevenson, 2020). Exposure to asbestos is also related to lung and larynx cancer, lung fibrosis or asbestosis and cancer of the ovary (Andujar et al., 2016; WHO, 2019b). The effects of asbestos exposure, even at low doses of 1 fiber/mL per year, can be apparent after several decades (Collaborative on Health and the Environment, 2019; Markowitz, 2015), and once diagnosed with mesothelioma, the patient has a life expectancy of one to two years (Molinari and Stevenson, 2020).
Asbestos fibres adhere to the parietal pleura and produce cytotoxicity and DNA damage, which ultimately leads to genetic modifications. The genetic modifications can lead to non-malignant damage and to cancer (Frank and Joshi, 2014). Non-malignant damage can express as asbestosis (scarring of the lungs or fibrosis), or as the formation of pleural and parenchymal plaques (Figure 27), which are benign fibrous lesions that thicken the parietal or diaphragmatic pleura (Røe and Stella, 2017). When the genetic modifications of chromosomes lead to the multiplication of tumour cells, this further leads to the formation of cancer in different organs. The most solid evidence of the relationship between asbestos exposure and cancer are related to mesothelioma, lung cancer, larynx cancer and ovarian cancer (IARC, 2012).
Figure 27. Lungs affected by pleural mesothelioma.
4.3.3.3. Health consequences of exposure to organic contaminants
Organic contaminants are generally found in all environmental compartments in low concentrations, and many persist in the environment for decades or centuries. Humans are exposed to anthropogenic organic contaminants through as the main three pathways: inhalation, dermal contact, and ingestion of contaminated food or polluted soil particles. Exposure to organic contaminants has been linked to chronic diseases such as cancer, neurological disorders and autoimmune diseases, many linked to the endocrine disrupting effect attributed to these contaminants. However, the scientific evidence is often limited. For many contaminants, regulatory institutions consider the results of ecotoxicological tests, in vitro or in vivo, since experimentation on humans raises ethical questions. Epidemiological studies on certain contaminants are very scarce, often involving small populations, have ethnic, age group, or exposure biases, and rarely consider exposure to multiple contaminants. As a result, drawing strong conclusions is sometimes premature. However, there is no doubt that many soil contaminants exist and are increasing, and we cannot rule out the harmful effects despite limited evidence (Benjamin et al., 2017).
Polycyclic aromatic hydrocarbons
Polycyclic aromatic hydrocarbons (PAHs) are ubiquitous contaminants and are classified as carcinogenic (e.g. benzo[a]pyrene) or possible carcinogenic to humans (e.g. benzo[b,k,j]fluoranthene or carbazole, among others) (IARC, 2020b). Industrial, urban, agricultural and forestry soils present concentrations of PAHs in decreasing order (WHO, 2000). Inhalation, ingestion or dermal contact with PAH-contaminated soil particles are common soil-related exposure routes (WHO, 2000). Crops can take up and concentrate PAHs from polluted soils, representing an important pathway for PAHs exposure (Wang et al., 2017), although no threshold levels have been established at the international level (JECFA, 2006a). Although the population is generally exposed to low levels of PAHs, occupational epidemiology studies demonstrate the health effects of PAHs, and exposure of vulnerable populations living in areas at higher risk of PAH soil pollution should not be ruled out (Chen et al., 2018; Tarafdar and Sinha, 2018).
PAHs are highly lipophilic and can be absorbed from the lungs, gut and skin. A higher incidence of respiratory (lung cancer), cardiovascular and immunological diseases have been observed in exposed populations (Drwal, Rak and Gregoraszczuk, 2019). Additionally, PAHs can pass over the placental barrier affecting foetal neurodevelopment. Jedrychowski and his co-workers observed a three-fold increase in the risk of a depressed verbal IQ when the infant was exposed to PAH before birth, an effect that was significantly reduced if the exposure occurred after birth (Jedrychowski et al., 2015). PAHs prenatal exposure is also related to reduced foetal development and chronic conditions in adulthood, such as heart diseases, obesity, or immunosuppression (Drwal, Rak and Gregoraszczuk, 2019).
Volatile organic compounds (VOCs)
Volatile organic compounds (VOCs) and especially benzene, toluene, ethylbenzene and xylene (BTEX) show ubiquitous distribution in the environment and there is increased concern for possible human health effects (Cheng et al., 2019). VOCs are mainly released from natural sources such as forest fires, but anthropogenic sources are becoming more relevant from activities such as the extraction and combustion of oil and natural gas, petrochemical activities and use in industrial products such as paints, lubricants, adhesives, and other oil products. These contaminants are lipophilic and are rapidly absorbed by the respiratory and digestive systems, but are easily metabolized. Thus their persistence in the human body is short (ATSDR, 2004). However, biotransformation occurs before BTEX is excreted from the body, and reactive species are produced that remain in the organs and tissues causing damage (Montero-Montoya, López-Vargas and Arellano-Aguilar, 2018).
Due to the volatile nature, humans are mainly exposed to VOCs through inhalation, in indoor air by diffusion of soil gas, and outdoors (ATSDR, 2004). Ingestion and dermal contact are also possible but normally limited to occupational exposure (Werder et al., 2019). No studies exist on dose-response exposures to complex mixtures of BTEX, and reference values are usually derived for individual contaminants (ATSDR, 2004). Hematologic effects, acute myelogenous leukaemia (AML) and myelodysplastic syndrome (MDS) are the main diseases attributed to BTEX acute exposure, supported by strong evidence (Chen et al., 2019a; Galbraith, Gross and Paustenbach, 2010; The Collaborative on Health and the Environment, 2019). Benzene is classified as carcinogenic, while ethylbenzene is considered as possible carcinogenic to humans; toluene and xylenes are non-carcinogenic (IARC, 2020a). Long-term exposure to benzene leads to decreased bone marrow cellularity, which can eventually induce aplastic anaemia and the development of leukaemia (ATSDR, 2004). Neurotoxic effects of BTEX have also been reported in experimental animals and observed in humans; however further studies are required (ATSDR, 2004; Werder et al., 2019). Some of the symptoms reported are headache, dizziness, difficulty concentrating, numbness/tingling sensations, blurred/double vision, or loss of consciousness (Krishnamurthy et al., 2019; Werder et al., 2019). There is some evidence for damage to the respiratory system: asthma, irritation, acute and chronic respiratory diseases, and damage to lung function (Hong et al., 2017; The Collaborative on Health and the Environment, 2019).
Phenols, chlorobenzenes and chlorophenols
Human-made phenol-containing compounds are priority contaminants due to ubiquitous distribution in the environment, persistence and toxicity (ATSDR, 2008, 2020; ECB-JRC, 2003, 2006). Phenols are extracted from crude oil and are widely used in the industrial synthesis and production of dyes, polymers, resins, pharmaceuticals, pesticides, fertilizers, disinfectants, and other organic preservatives (Abdollahi, Hassani and Derakhshani, 2014). The presence in the environment is mainly due to release during production, use and disposal of phenol-containing products, as well as in the generation of industrial and municipal wastewater (ECB-JRC, 2006; Zaki et al., 2015). Humans can be exposed through ingestion, inhalation and dermal contact (Meena, Band and Sharma, 2015).
Phenolic compounds are easily absorbed by the skin and respiratory and gastrointestinal track, and once in the body, are metabolically degraded in the liver, gut and kidneys, which leads to the formation of more reactive species (ECB-JRC, 2006). These metabolic products are related to DNA damage, the destruction of some proteins and the disruption of the electron transport mechanisms (Soto-Hernández, Palma-Tenango and Garcia-Mateos, 2017). Phenol is a potent neurotoxin although it is relatively mobile in soils and has a half-life of only several days. Although direct ingestion of phenol can be lethal at a concentrations of 1 g of phenol (Meena, Band and Sharma, 2015); human exposure to phenol-polluted soil is low and the major risk comes from exposure to contaminated plant shoots (ECB-JRC, 2006). Nevertheless, low-dose long-term exposure has been reported to be responsible for multiple diseases such as anorexia, diarrhoea, vertigo, salivation and dark coloration of urine (Abdollahi, Hassani and Derakhshani, 2014).
Chlorophenols are also widely used as disinfectants and in pesticide formulations due to high biocide potential (ATSDR, 1999). The main routes of exposure to chlorophenols are occupational exposure and through the ingestion of contaminated drinking water; dermal contact with wood treated by chlorophenol-based disinfectants is also a relevant route of exposure (ATSDR, 1999). Chlorophenols have been recently detected in human urine and tissues in several countries, suggesting that the exposure to these chemicals could be higher than expected (Honda and Kannan, 2018; Igbinosa et al., 2013). Environmental exposure to chlorophenols is relatively low, as they show low mobility in soils and are rapidly degraded by photolytic activity and microorganisms (ATSDR, 1999; Badanthadka and Mehendale, 2014). Chlorophenols are considered potentially carcinogenic to humans (IARC, 2020a) and endocrine disrupting activity has also been reported in animals and humans (Michałowicz et al., 2018). Haemolytic anaemia caused by the apoptosis of erythrocytes has been reported by Michałowicz and co-workers (2018) and others, specifically caused by pentachlorophenol at occupational exposure concentrations (Michałowicz et al., 2018).
Chlorobenzenes are aromatic compounds used in the production of dyes, pharmaceuticals and resins used in plastic and rubber industries (National Research Council, 2012). Chlorobenzenes reach the soil matrix in sewage sludge applications and via direct releases from industries, and as the other aromatic contaminants, they are rapidly biodegraded and moderately absorbed in soils (ATSDR, 2020). Occupational exposure is the most significant and concerning source of human exposure (ECB-JRC, 2003). Environmental exposure is limited and the main routes are inhalation and intake of contaminated drinking water and food, although the concentrations are usually low (ATSDR, 2020; ECB-JRC, 2003). Chlorobenzenes have shown certain genotoxic potential in animals in in vitro and in vivo studies, and also neurotoxicity after acute exposure to high concentrations (National Research Council, 2012). However limited or no studies are available on the effects of acute or chronic exposure to chlorobenzene in humans (ATSDR, 2020).
Explosives
Although explosives are not as widely distributed in the soil as other organic contaminants, there are still many affected areas polluted from the First and Second World Wars, from other international wars and civil wars, and from military sites scattered around the planet (see Chapters 2 and 3). Explosives are mainly found in manufacturing areas, construction and demolition sites, military areas (including training operations, open detonation, assembly and packaging operations) and war zones. The population may be exposed to these contaminants by ingestion of polluted soil or food produced in contaminated soil and neighbouring areas, as well as by accidental inhalation or direct dermal contact with the contaminant or polluted soil (Broomandi et al., 2020; Gorecki et al., 2017). Explosives are usually rapidly excreted in urine, but metabolites remain in the body causing several diseases (Ahlborg, Einistö and Sorsa, 1988; Lima et al., 2011). Explosives can also move throughout environmental compartments, from soil to groundwater and surficial water bodies and to plant and animals (Chatterjee et al., 2017; Via, 2016).
Among the commonly used explosives, 2,4,6-trinitrotoluene (TNT) is one of the most studied explosives because of its health effects. Although IARC listed TNT as non-carcinogenic to humans (IARC, 2020a), several studies with workers and exposed populations indicate that TNT affects primarily the spleen and liver, and can also have carcinogenic effects (Ahlborg, Einistö and Sorsa, 1988; ATSDR, 1995; Chatterjee et al., 2017). Unspecific effects, such as convulsions, vertigo, vomiting and unconsciousness have been reported after exposure to dinitrotoluene (DNT) and have also been observed in workers in explosive factories in Europe and the United States of America exposed to hexahydro-1,3,5-trinitro-1,3,5-triazine (RDX) (Letzel et al., 2003; Pichtel, 2012). Hepatobiliary carcinoma and urothelial cancer have been reported in persons exposed to high concentrations of DNT (Lima et al., 2011). Ecotoxicological effects have been observed in bacteria, aquatic and terrestrial organisms and crops. Thus, similar mechanisms could be expected in humans (Chatterjee et al., 2017). However, health outcomes of exposure to explosives have been scarcely studied and controversy exists regarding some of the results (Lima et al., 2011).
Dioxin and dioxin-like compounds
Dioxins and dioxin-like compounds, including polychlorinated/brominated dibenzo-p-dioxins (PCDDs/PBDDs), polychlorinated/brominated dibenzofurans (PCDFs/PBDFs) and dioxin-like polychlorinated biphenyls (dl-PCBs), are distributed in the global environment and are well known for causing toxic effects on biota and humans. These contaminants are easily absorbed in humans and accumulate in liver and body lipids, are poorly metabolized and persist for several years (Knutsen et al., 2018). dl-PCBs and other dioxins are persistent in the environment and are classified as carcinogenic to humans (IARC, 2020b). The WHO categorizes these organic contaminants as endocrine disruptors, immunosuppressors, carcinogens, and teratogens (WHO, 2016c). According to IARC, based on the available evidence, only the carcinogenicity for dl-PCBs 77, 81, 105, 114, 118, 123, 126, 156, 157, 167, 169, 189 and 2,3,7,8-Tetrachlorodibenzo-para-dioxin (TCDD) can be confirmed (IARC, 2020a).
Intake of contaminated food is the main route of exposure to dioxins and a tolerable monthly intake has been set up at 70 pg/kg b.w./month, applicable to intake of PCDDs, PCDFs and dl-PCBs (JECFA and World Health Organization, 2002). Severe cases of dl-PCB poisoning through the ingestion of contaminated rice oil occurred in Japan and Taiwan in 1968 and 1979, respectively, where thousands of people were directly affected by skin lesions and altered reproductive and immunological function. Dysfunctional developmental effects were transmitted to the next generation exposed during gestation and lactation (Loganathan and Masunaga, 2015).
Chloracne is probably the most well-known disease related to dioxin exposure but this is caused by exposure to high concentrations (serum levels > 20 000 pg/g fat) (Knutsen et al., 2018), several orders of magnitude greater than environmental background levels and food concentrations. Some notable cases worldwide have been reported, including the cases in Seveso, Italy, in 1976, after an industrial accident in which the population was exposed first through inhalation of the toxic cloud generated during the explosion, and later through environmental and contaminated food exposure, with levels of TCDD in topsoil ranging from 15.5 to 5 477 μg/m2 (Pesatori et al., 2009). Chloracne, offspring alterations, lower fertility rates, and breast and lymphatic-hematopoietic cancers were the main health effects observed in the affected population (Eskenazi et al., 2018). Another well-known case of chloracne was that of Ukrainian President Viktor Yushchenko, who was poisoned with dioxins in 2004. A short time after exposure to the dioxins, an acne-like eruption of blackheads, cysts, and pustules appeared in his body (Schecter, 2012).
Dioxins and dl-PCBs join the aryl hydrocarbon receptor (AhR), a steroid-hormone receptor, which ultimately binds to DNA and causes a wide range of cellular and metabolic alterations, and also induce activation or inactivation of multiple genes that have significant impact on metabolism and development (Bock, 2016; Carpenter, 2006). Dioxins and dl-PCBs have also been related to a higher incidence of cancer, neurological retardation and ultimately death (White and Birnbaum, 2009). Non-Hodgkin’s lymphoma and suppression of the immune system are also attributed to dioxin exposure (The Collaborative on Health and the Environment, 2019). EFSA also reported an impact on semen quality after pre- and post-natal exposure (Knutsen et al., 2018). Recently, Guo and co-workers associated autism spectrum disorder (ASD) to exposure to dioxins and dl-PCBs, although the mechanisms of action are not yet clear (Guo et al., 2018).
Polychlorinated biphenyls (PCBs)
Non dioxin-like polychlorinated biphenyls (ndl-PCBs) are also widely distributed contaminants that are highly persistent in the environment and accumulate in lipid tissues (Carpenter, 2006). Ndl-PCBs can cross the placenta and accumulate in the foetus (WHO, International Programme on Chemical Safety and Inter-Organization Programme for the Sound Management of Chemicals, 2003). PCBs were phased out of the global markets at the end of last century, and environmental concentrations have been gradually reduced, although these contaminants still persist in the environment (EFSA, 2010). It is estimated that around 200 million kg of PCBs are still circulating between the global environmental compartments (WHO, International Programme on Chemical Safety and Inter-Organization Programme for the Sound Management of Chemicals, 2003). Legacy ndl-PCBs released from PCB-containing materials as well as non-legacy PCBs produced as by-products of industrial pigments and dyes pose a significant long-term risk to human health and the environment (Hu and Hornbuckle, 2010; Klocke and Lein, 2020).
The major route of exposure for ndl-PCBs is through the intake of contaminated water and food (EFSA, 2010), principally milk, dairy products, fish, meat, poultry and game. Fruits and vegetables present lower concentrations of ndl-PCBs than food of animal origin (EFSA, 2010; Mihats et al., 2015). Several institutions consider the reference value of 10 ng/kg b.w./day for ndl-PCBs in food, but no specific agreement has been reached regarding the tolerable daily intake (TDI) of ndl-PCBs (Mihats et al., 2015).
Ndl-PCBs modulate intracellular Ca+ signalling activity (Choi et al., 2016). In addition, ndl-PCBs mimic the action of oestrogen and in the body have been related to immunotoxicity, neurotoxicity, and carcinogenesis, especially related to breast cancer (Carpenter, 2006; WHO, International Programme on Chemical Safety and Inter-Organization Programme for the Sound Management of Chemicals, 2003). With the current evidence, IARC classifies some ndl-PCBs as carcinogens to humans (IARC, 2020a). Liu and co-workers observed an increase in reactive oxygen species in in vivo experiments with breast cancer cells that led to a higher metastatic capacity (Liu, Li and Du, 2010). The estrogenic activity of ndl-PCBs has also been linked to iron metabolism, having a suppressive effect that can lead to anaemia (Qian et al., 2015).
Evidence has emerged in recent years linking exposure to environmental concentrations of ndl-PCBs to other diseases (WHO, International Programme on Chemical Safety and Inter-Organization Programme for the Sound Management of Chemicals, 2003). There is multiple evidence in animal models and in vitro and in vivo studies that demonstrate the neurotoxicity of ndl-PCBs (Ulbrich and Stahlmann, 2004; Winneke, 2011). Some studies have tried to elucidate the molecular mechanisms of action; for example, Choi and co-workers have demonstrated the molecular mechanism by which ndl-PCBs cause neurobehavioral disturbances by disrupting neuronal communication and reduce synaptic plasticity in children after prenatal exposure (Choi et al., 2016). Reduced birth- size (Kobayashi et al., 2017) and risk of gestational diabetes mellitus (Zhang et al., 2018) have also been reported. Many of these health outcomes have been reported to be gender-specific (Klocke and Lein, 2020; Zhang et al., 2018).
Polybrominated diphenyl ethers (PBDEs)
Polybrominated diphenyl ethers (PBDEs) have been widely used as flame retardants in a vast range of industrial, construction, electronic and textile products. Production has been phased out in many countries since their inclusion in the Stockholm Convention list of POPs (Stockholm Convention, 2021), and the environmental and human loads have reduced since that time. However, PBDEs are found in virtually all environmental matrices, including wild organisms and humans, due to long persistence, and current use in many products (Jiang et al., 2019b). Relatively high concentrations have been reported especially in e-waste dismantling and recycling areas and countries where their production and use has not yet been banned, such as the United States of America or China (Jiang et al., 2019b; Klinčić et al., 2020). Exposure pathways vary from inhalation, to dermal contact and ingestion of contaminated plants, soil and dust (Müller et al., 2016; Wu et al., 2020). PBDEs have been detected in multiple human samples worldwide, including umbilical cord blood, placenta, breast milk, blood, semen, and the liver (Jiang et al., 2019b; Klinčić et al., 2020; Wu et al., 2020). Children are especially vulnerable due to prenatal and postnatal exposures being higher than for adults (Fischer et al., 2006).
The number of research works trying to elucidate the role of PBDEs on human health has grown considerably in the last decade. PBDEs have been associated with neurotoxicity, and several studies have found sound evidence of the relationship between prenatal PBDE exposure and impaired motor, cognitive and behavioural ability in small children, showing lower IQ levels, or aggressive behaviour among other effects (Gibson et al., 2018; Vuong et al., 2018). These effects may be related to the impact of PBDEs on thyroid hormone production and regulation, PBDEs being endocrine disruptors (Wu et al., 2020; Yu et al., 2019). Several cancers have also been associated with the PBDEs body burden, including breast, colorectal, papillary thyroid, and ovarian and cervical cancers or endometrial carcinoma (Wu et al., 2020). Evidence of the oxidative stress posed by PBDEs on human cells have also been discussed by several authors (Poston and Saha, 2019). However, conflicting observations have been reported worldwide, and thus more research is needed to fully elucidate the mechanisms of action, identify all routes of exposure and body burdens and possible interactions with other contaminants (Choi and Kim, 2020; Wu et al., 2020).
Perfluoroalkyl and polyfluoroalkyl substances (PFASs)
Other contaminants of emerging concern are also causing alarm because of transfer from soil to crops and wide distribution in humans and animals worldwide (DeWitt, 2015). Advances in detection technologies have made possible the determination of low concentrations (ng/L blood) that have significant effects on health, even at these low concentrations (Lei et al., 2015). This is the case with PFAS, for which ingestion through consumption of contaminated food and water is a major exposure route for humans. PFASs are mainly transferred from soil to roots and tubers, while contamination of plant aerial parts is mostly due to exposure by contaminated irrigation water (Scher et al., 2018). Although concentration of legacy PFAS has reduced in human serum, newly synthetized PFAS and by-products are not yet consistently monitored (Sunderland et al., 2019).
PFAS are endocrine disruptors, and interact with thyroid hormones, altering cardiovascular system functioning and lipids metabolism, and increasing the risk of obesity (Braun, 2017; Naidu et al., 2020). Increased concentration of cholesterol and other lipids in blood, or dyslipidaemia, is one of the major health effects attributed to PFAS, associated with chronic diseases such as obesity, hypertension, diabetes and hepatotoxicity (Jiang, Gao and Zhang, 2015; Sunderland et al., 2019). In addition, a high incidence of several types of cancer (e.g., breast or prostate cancer) has been observed in populations with higher levels of PFAS in the blood, although a clear relationship has not been established due to the prevalence of other risk factors, such as heredity (Lei et al., 2015). Some evidence also relates prenatal PFAS exposure to neurodevelopmental impairment, but further research is needed in this field (Goudarzi et al., 2016; Naidu et al., 2020).
Pesticides
Studies on health effects from exposure to pesticides mainly concern occupational exposure or self-poisoning, where exposure is at relatively high concentrations that do not occur in the general population. The number of epidemiological studies linking chronic diseases to exposure to pesticide-polluted soils is very low due to wide distribution and coexistence with other contaminants. Thus, it is very complex to establish casual relationships, coupled with less support for this type of research (Bonner and Alavanja, 2017; Kim, Kabir and Jahan, 2017). However, scientific evidence points to a relationship between pesticide exposure and chronic diseases such as cancer, asthma, allergies and development impairment (Kim, Kabir and Jahan, 2017).
Pesticide-contaminated food has been often reported, although the source of pesticides is little studied in depth. However, the uptake of several pesticides by plants has been demonstrated (Ge et al., 2017; Hwang, Zimmerman and Kim, 2018). Although the most persistent pesticides have been controlled or banned after the adoption of the Stockholm Convention and many countries have strict controls and protective tolerable limits on pesticide residues in food (Carvalho, 2017), residues of legacy or in-use pesticides are still detected in foods and may cause unintentional poisoning. This is particularly important in low-income countries, where control and precautionary measures are less widely applied and pesticides are misused due to lower awareness and literacy among farmers and the illegal trade in highly toxic pesticides (Donkor et al., 2016; Özkara, Akyıl and Konuk, 2016; Victoria, Neema and Martin, 2017). Pesticide-polluted food is also an issue in higher-income countries with weak regulations (Danial et al., 2016). Wu et al., 2001 reported several cases of food-borne agrochemical poisoning in Taiwan due to the misuse of the banned pesticide methamidophos. Additionally, the potential risk from exposure to low residue levels of several pesticides in several different foods in combination could manifest in chronic effects (Machekano et al., 2019). Akoto and his collaborators noted that although the levels of a single pesticide in several vegetables were below the European Maximum Residue Levels (EC, 2016), the combined consumption of vegetables contaminated by several pesticides in Ghana had a potential health risk (Akoto et al., 2015).
4.3.3.4. Health consequences of exposure to emerging contaminants
Pharmaceuticals and personal care products (PPCPs)
The presence of pharmaceuticals (both human and veterinary) and personal care products in the environment is steadily increasing and these chemicals are already found in all environmental media on all continents in highly variable concentrations, from nanograms to micrograms per litre of water or gram of soil (Ebele, Abou-Elwafa Abdallah and Harrad, 2017; Klatte, Schaefer and Hempel, 2017; Verlicchi and Zambello, 2015). These compounds are normally used in low therapeutic concentrations and their half-lives are relatively short; however, due to continuous release in the environment through wastewater and organic residues, PPCPs are considered persistent or pseudo-persistent in the environment (Richmond et al., 2017). In addition, PPCPs are biologically active compounds and have a potentially bioaccumulative and toxic behaviour, thus are considered as PBT (persistent, bioaccumulative and toxic) contaminants (Cassani and Gramatica, 2015).
The main groups of pharmacological compounds found in soils from sewage sludge, wastewater and animal manure are: antimicrobial, anthelmintic, antiparasitic, steroid, corticoid, anti-inflammatory, pain relieving, astringent, hormonal regulators, nutritional supplements and growth promoters. This category also includes residues of other contaminants, such as surfactants used in detergents and soaps, musk compounds used as fragrances, personal insecticides, perfluorinated compounds (PFCs) used as household anti-adherents or hydrophobic textile coatings, among others.
Soil-related PPCP exposure to humans is mainly through the intake of contaminated food cultivated on polluted soils. There is solid evidence that wastewater treatment plants cannot eliminate all residues of PPCPs and their derivatives, which are released to agricultural soils with irrigation wastewater or through the application of sewage sludge as soil amendments. Once in the soil, PPCPs are taken up by plants and enter the food chain (Al-Farsi et al., 2017; Colon and Toor, 2016; Piña et al., 2020).
PPCPs intervene in specific metabolic and molecular pathways of target organs and species, although they can also cause similar effects in the same active sites of non-target species. PPCPs release to the environment also leads to microbial and bacterial resistance, causing 700 000 death each year due to drug-resistant diseases (IACG, 2019).
The accumulation of persistent pharmacological compounds may cause chronic side effects resulting from continuous exposure over long time at low doses (Lei et al., 2015; Zhao et al., 2019). Some studies have considered the impacts of these compounds on wild organisms, mainly in aquatic ecosystems (Mezzelani, Gorbi and Regoli, 2018; Richmond et al., 2017). However, knowledge about the ecotoxic effects on terrestrial organisms including humans have yet been elucidated (Richmond et al., 2017). Given the wide variety of compounds included in this class of contaminants and the multiple specific actions, the variety of effects on human health are also variable, and include endocrine disruption, inflammation, irritation, changes in fertility and gender rates in populations, and development of asthma, although relevant epidemiological studies are very limited or absent (Pereira et al., 2015; Wilkinson et al., 2016).
PPCPs have been detected in human samples, including breast milk, blood and urine. Although many of these PPCPs are considered of low risk to human health at the environmental concentrations detected and due to short half-lives, continuous, long-term and low concentration exposure may have significant impact. For example, Fisher and his collaborators (2017) studied the concentrations of parabens in the blood, urine and breast milk of pregnant women in Canada and the relationship to PPCP use (Fisher et al., 2017). These authors found a wide distribution of these compounds in virtually all samples. Their results show a potential transference of parabens to infants and a potential carcinogenic risk (Fisher et al., 2017). Triclosan, an antibacterial agent found in many soaps and other PPCPs, is not efficiently removed from wastewater and ends up in soil, sediments and water together with its by-products (Ruszkiewicz et al., 2017). Triclosan has been detected in human samples including breast milk and human tissues, indicating a potential bioaccumulation, and several negative effects have been reported, such as neurotoxicity. However, despite the alarming preliminary results, no studies have analysed long-term impact or the effects of co-existence with other PPCPs (Ruszkiewicz et al., 2017; Yueh and Tukey, 2016).
Plastics and synthetic polymers
Plastics are of growing concern due to their ubiquitous distribution in the environment. Scientists have recently detected plastic particles (micro and nanoplastics) in all environmental media and even in remote areas (Andrady, 2011; He et al., 2018; Lusher et al., 2015; de Souza Machado et al., 2018a). Recreation activities in wild areas can also contribute to the release of micro and nanoplastics to soil from sport clothing and footwear (Forster, Tighe and Wilson, 2020). The transfer of micro- and nanoplastics from soils to the food chain has been demonstrated in recent years, either by plant uptake or by being ingested by soil organisms (Huerta-Lwanga et al., 2017; Jiang et al., 2019a; Li et al., 2019a; Schwab et al., 2016). Evidence of bioaccumulation and biomagnification of plastics in the terrestrial food chain suggests that plastics also accumulate in human bodies (Figure 28), but the evidence is yet limited (Schwabl et al., 2019). New evidence is emerging that show the accumulation of micro- and nanoplastics in human tissues and being able even to cross the placenta (Ragusa et al., 2021; Vaseashta, 2015). Intake of contaminated food and water is the major route of exposure to micro and nanoplastics (Karbalaei et al., 2018).
Figure 28. Examples of microplastics accumulation in mice tissues after exposure for 28 days.
However, the risk posed by plastics to human health and the environment is not only their presence per se, which may cause oxidative stress, inflammation, severe immune responses, or alter the ability to detect exogenous materials and react, but also the capacity to adsorb and transport other contaminants and plastic additives that can be released in the organism (Ballesteros et al., 2020; Han et al., 2020; Prata et al., 2020). The preliminary evidence highlights the need to study in detail the pathways of exposure and entry of microplastics into our bodies and the possible adverse effects, so that informed risk assessments can be conducted and regulation improved to prevent these contaminants from affecting our health (Prata et al., 2020; Ragusa et al., 2021).
Phthalates and other plasticizers
Phthalates and other plasticizers are widely present in all environmental media. They are used in multiple daily items and provide plasticity, flexibility, or higher fixation. The effects of phthalates on human health have not yet been fully elucidated, and evidence has mainly focussed on animal and in vitro studies (Benjamin et al., 2017; US EPA, 2015b).
Phthalates are demonstrated endocrine disruptors and teratogens (Benjamin et al., 2017). Other evidence also points to a mutagenic action on the reproductive system and embryonic development (Radke et al., 2018; Swan, 2008). Phthalates are rapidly metabolised and excreted in urine and faeces (US FDA, 2020); however, studies with experimental animals have shown evidence of anomalies in reproductive tract (Hauser and Calafat, 2005). Diethylhexyl phthalate and dibutyl phthalate show hepatic and renal effects at high doses and cause hepatocellular carcinoma, anovulation, and decreased foetal growth (Hauser and Calafat, 2005). Some effects on respiratory function, metabolism, and thyroid function of humans are also reported with phthalate exposure (Meeker, Sathyanarayana and Swan, 2009 and references therein). Children are the most vulnerable to phthalate exposure, suffering from food allergies (Stelmach et al., 2015) and neurobehavioral disorders in prenatal and early life exposure (Braun, 2017). Ruiz and co-workers also identify that low-income populations in the United States of America are more frequently exposed to endocrine-disrupting chemicals, including phthalates and other plasticizers, increasing the risk of diabetes and other metabolic disorders (Ruiz et al., 2018).
Bisphenol A is another plasticizer widely used and found in different environmental media, including soils and food (Careghini et al., 2015). Although bisphenol A is rapidly eliminated from the body, the continuous exposure in some populations poses a significant health risk (Ruiz et al., 2018). Bisphenol A is an endocrine disruptor; due to its estrogenic activity it shows reproductive and developmental toxicity, which particularly affects the foetus in the first stages of pregnancy in rodents (FAO and WHO, 2010). Recent evidence link low-dose long-term exposure to bisphenol A with a higher incidence of breast cancer (Wang, Liu and Liu, 2017). However, insufficient data is available on the effects and mechanisms of action of Bisphenol A on human health at environmental concentrations (EFSA Panel on Food Contact Materials, 2015).
Nanomaterials
Nanotechnology emerged in the 1990s and its use and applications have greatly expanded since that time (Klaine et al., 2008). Manufactured nanomaterials (MNM) have numerous applications in medicine and technology and have enabled many advances in countless scientific fields (Pereira et al., 2015). MNM are diverse in terms of physical, chemical, electrical and magnetic properties. MNM are characterised by small size, up to several dozen nanometres and usually less than 100 nm (Saleh, 2020). Their intrinsic characteristics and small size facilitate the diffusion of nanomaterials through the cell membranes, but the interactions with the cellular components and the genetic material have not yet been fully elucidated and vary according to the size, morphology, surface charge and coating of the nanomaterial (Ganguly, Breen and Pillai, 2018; Schwab et al., 2016). The formation of a biocorona of lipids and proteins on the MNM surface when reaching the environment also influence the behaviour (Monopoli et al., 2012).
Currently, inhalation of MNM appears to be the main route of exposure, especially in occupational exposure, but ingestion may become more relevant as nanotechnologies in food and food packaging evolve (Pietroiusti et al., 2018). Dermal exposure can also be significant for consumers (Malakar et al., 2020). Studies of the impacts of MNM on environmental and human health are still at the very early stages and existing data are insufficient to understand the mechanisms of toxicity. Evidence linking MNM exposure to different diseases is still very scarce, so no robust conclusions can be drawn (Aschberger et al., 2011; Linkov et al., 2011). The effects of nanomaterials can vary from inducing oxidative stress, to the release of other toxic compounds associated with or as part of the nanomaterials, such as trace elements or ions (Klaine et al., 2008). Inflammation and development of pleural mesothelioma have been attributed to the inhalation of certain long and rigid MNM fibres, which can easily reach the alveolar region (IARC, 2020a; Pietroiusti et al., 2018). Oxidative stress and the subsequent production of reactive oxygen species that can travel from the lungs to other parts of the body through the lymphatic system and bloodstream can also cause damage to the organs and tissues (Pietroiusti et al., 2018). Genotoxic effects and impaired reproduction have also been observed in laboratory rodents, indicating that more research is needed on these possible effects in humans (Ganguly, Breen and Pillai, 2018; Pietroiusti et al., 2018).
- 6 Indicator 3.3.5. Number of people requiring interventions against neglected tropical diseases (including soil-borne helminthiasis)
- 7 Indicator 3.4.1. Mortality rate attributed to cardiovascular disease, cancer, diabetes or chronic respiratory disease
- 8 https://apps.who.int/food-additives-contaminants-jecfa-database/chemical.aspx?chemID=5294
- 9 Non-aqueous phase liquids (see Chapter 2)
- 10 DALYs = Disability Adjusted Life Years. The sum of years of potential life lost due to premature mortality and the years of productive life lost due to disability (WHO, 2020a).
- 11 Millisievert is the unit to express the total radiation dose received. The rate of accumulation is expressed as a dose rate per unit time (e.g. mSv/yr)