Soil has a profound effect on the health and well-being of humans. Depending upon the condition of the given soil and the interactions of interest, this effect can be either positive or negative and direct or indirect. Soils that affect human health include natural soil, which usually has little anthropogenic contamination, and soils in agroecosystems, urban areas, mines, oil and gas extraction areas, landfill sites and other locations where anthropogenic contamination is more likely. People in professions that work closely with soil, such as farmers, construction workers or miners are at a greater risk of health problems that involve direct contact with soil, but everyone’s health is affected by soil to some extent. This is because soil provides many of the nutrients we require and can pass on harmful substances through the food that we eat. Some dusts generated from soil can travel thousands of miles and affect people long distances from where they originated. Although recent advances in the role soil plays in human health are being made and continue to be investigated, few people probably think about soil having an effect on their health. This paper will give a brief, general overview of the topic of soil and human health. Other excellent papers on this topic have been published recently and we encourage the reader to find additional details on many of these topics in other related publications (e.g. Pepper, 2013; Brevik & Burgess, 2015; Oliver & Gregory, 2015; Cakmak & Kutman and Li et al. in this issue).
Probably the first recorded depiction of the relation between human health and soil occurs in 1400 BC in the Bible in the book of Numbers where Moses directs the people to “see what the land is like….how is the soil…fertile or poor?” (Numbers 13:18–20). In 400 BCE Hippocrates published a list of things that should be considered part of a proper medical evaluation, a list that included the nature of the ground (Hippocrates, 2010) and in 60 BCE Columella wrote about hidden diseases from marshes (Sylvia et al., 1998); in each case advancing the idea that soil is important to human health. However, it was not until the early 1900s that the idea that soil could affect human health started to gain widespread acceptance. McCarrison (1921) concluded that the fertility of a soil determines the nutrient content of food crops, and therefore the health of humans who ate the crops. In the late 1930s, the USDA Yearbook of Agriculture (USDA, 1938) included discussion on the importance of soil as the origin for many of the essential elements necessary for human health in at least three of its chapters, and in 1940 the USDA established the Plant, Soil and Nutrition Research Unit (PSNRU) at Cornell University which still continues to do research into soil and human health (PSNRU, 2008). In the 1940s, individuals such as Sir Albert Howard (1940), Lady Eve Balfour (1943) and J. I. Rodale (1945) offered opinions on the links between soil and human health, in particular the effect of soil fertility on the nutrient content of foods grown in a particular soil was a common theme. The 1950s brought about the realization that soil could supply toxic amounts of elements to the human diet (USDA, 1957). André Voisin published extensively on the potential links between soil and human health in 1959, a study that was probably the most comprehensive on the subject up to that time. From these first realizations, studies into the relation between soil and human health have continued to increase and several of the areas of investigation will be described below in summary. Brevik & Sauer (2015) recently reviewed the history of the soil–human health field and we direct readers to this review for more detail.
Routes of exposure
There are three common ways that humans are exposed to soil materials: (i) ingestion, (ii) respiration and (iii) skin absorption or penetration (Brevik, 2013). Ingestion can occur deliberately, known as geophagy, or incidentally, such as during hand to mouth contact (particularly children) or when raw fruits or vegetables are consumed without adequate washing. Ingestion of soil is especially common in children (von Lindern et al., 2016) and pregnant women. Ingested soil can potentially supply essential nutrients, but it can also lead to exposure to heavy metals, organic chemicals or pathogens and in large amounts can cause an intestinal obstruction (Henry & Cring, 2013). Respiration involves inhaling soil materials. Some serious problems are linked to inhalation, such as coccidioidomycosis (Bultman et al., 2005; Stockamp & Thompson, 2016), acute inflammation of the bronchial passages, chronic bronchitis, emphysema and fibrotic changes from breathing in soil-derived dust (Zosky et al., 2014), and mesothelioma from breathing in naturally occurring asbestos minerals from soil-derived dust (Buck et al., 2016). Absorption or penetration of the skin can expose an individual to pathogens and soil chemicals (Brevik, 2013). It can also cause podoconiosis (endemic non-filarial elephantiasis), which is a non-infectious disease found in subsistence farmers who frequently go barefoot. This is due to long-term contact with volcanically-derived clay in the soil which obstructs the lymph system (Deribe et al., 2013). Prevention is as simple as wearing shoes, and the condition has ceased to occur in countries where it was once found such as in France, Ireland and Scotland once the use of shoes became commonplace (Deribe et al., 2013).
There are many ways that soil can adversely affect human health. The soil may be contaminated either naturally or through anthropogenic activities with chemical elements and substances that are in toxic amounts when ingested or inhaled. A supply of any element may result in human toxicity, even elements that are essential for life. For any essential element there is an optimal range of concentration in humans, falling below this optimal range results in deficiency, whereas, concentrations above the optimal range create toxicity. Thus, the level of any essential element in humans can be deficient, adequate or toxic depending upon the concentrations of these elements in the soil and the degree of exposure. Both deficiency and toxicity can result in morbidity and in some cases mortality. There are many examples, reports and research publications on the risk of toxicity from substances in soil and the risk to human health, although some have been studied more than others. There are also elements that can be present in soil that have no known benefit for human health such as lead and mercury, but can cause problems with toxicity even at very small concentrations (Combs, 2005; Brevik & Burgess, 2015). Herein we briefly overview several elements of particular interest. The reader is referred to other papers on the supply of elements by soil, such as Steinnes (2011), Green et al. (2016) and Cakmak & Kutman (this issue), for additional information.
Lead is probably the single largest soil contaminant worldwide because it has been widely introduced into soil from anthropogenic sources such as leaded petrol (gasoline), lead-based paint, lead mining and smelting, and other industrial activities. The effects of lead, especially on children and adolescents, is well documented (Deckers & Steinnes, 2004; Balabanova et al., 2017) and has led to multiple public health problems and concerns. Lead in urban soil, where children are especially at risk for contact and contamination, is a particular problem (Filippelli & Laidlaw, 2010; Li et al., 2015). Mass lead poisoning was recently reported in Senegal (Haefliger et al., 2009) and Nigeria (Lo et al., 2012) in villages that participated in informal recycling of used lead-acid batteries and gold ore processing, respectively. The recycling and gold processing activities resulted in lead contaminated soil, with dust from such soil being inhaled, ingested or both, causing lead poisoning. Such studies demonstrate the challenges that many developing countries still face with regard to soil contamination by heavy metals and human health (Wu et al., 2015).
In addition to lead, arsenic poisoning remains a concern over large parts of the world. Arsenic is a naturally occurring element that can concentrate in drinking water, especially water obtained from wells (Helmke & Losco, 2013; Ayotte et al., 2015). Millions of people worldwide are exposed to potentially toxic levels of arsenic each day. Moreover, another common source of arsenic exposure is from the wood found in and around homes, especially in wood preservatives used in pressure treated timber (lumber). Arsenic can concentrate in the soil around structures made with this treated wood where it creates an exposure hazard, especially to children (Gardner et al., 2013). Another problem is the use of arsenic contaminated water to irrigate rice crops; the arsenic then accumulates in people who consume the rice (Brammer & Ravenscroft, 2009; Kwon et al., 2017). Rice is the dietary staple for about half the world’s population, and for most of these people rice also represents their primary exposure to arsenic (Zhao et al., 2010).
Cadmium contamination can be caused by industrial activities or by fertilization with sewage sludge or superphosphate (Nordberg et al., 2015). Cadmium is the most common heavy metal contaminant in the soils of China (Zhao et al., 2015). Large concentrations of cadmium in soil can lead to corresponding large concentrations in plant tissues (Hunter, 2008), which results in toxicity to humans when foods grown in such soil are consumed. The classic example of health problems caused by soil cadmium was the itai-itai disease outbreak in Japan in the first half of the 1900s (Nordberg et al., 2015). Mining in the Toyama Prefecture of Japan released large quantities of cadmium into the Jinzu River, which was used for rice irrigation. Rice absorbed cadmium from the water, and people who consumed the rice subsequently developed itai-itai disease. Itai-itai means “it hurts-it hurts” in Japanese, and the disease is characterized by weak, brittle bones, pain in the legs and spine, coughing, anaemia, and kidney failure. However, large cadmium concentrations in soil do not necessarily produce such symptoms because other soil and dietary conditions are important. Cadmium bioavailability is affected by soil aeration status (Zhao et al., 2015), soil pH and the concentrations of other elements present in a soil. The effect on humans is affected by the concentrations of nutrients such as iron and zinc present in the local diet (Brevik, 2013; Morgan, 2013). Residents of the village of Shipham, in England have large cadmium concentrations in their soil, but do not appear to suffer any adverse health effects because of low bioavailability of the cadmium in their soil and large soil zinc concentration (Chaney, 2015). More in-depth discussions of itai-itai soil interrelations are provided by Morgan (2013) and Brevik & Sauer (2015).
Soil is the primary nitrogen source for plants, and given that nitrogen is required for human health, nitrate is an essential nutrient; however, because of its importance plants can quickly diminish nitrate concentrations in soil. For production agriculture to succeed, the nitrogen consumed has to be replaced frequently, and this is usually with the use of chemical fertilizers. Properly managed, this does not endanger human health and increases crop production. However, improper use and overuse can lead to leaching of excess nitrate into groundwater or surface water (Zhang et al., 2015). Nitrate-contaminated water can cause serious toxicity when the gut microflora convert nitrate into nitrite. Nitrite then reacts with haemoglobin to form methemoglobin, which prevents oxygen from being carried throughout the body. The condition is called methemoglobinemia, and while it can occur in adults it is a bigger problem in infants (Bryan and Ivy, 2015). With the decrease in oxygen concentrations in the blood, infants can become cyanosed with a bluish colouring of the skin. Nitrate has also been identified as a risk factor in the development of stomach cancer (Nagini, 2012). Therefore, proper use of nitrogen fertilizers is vital to prevent public health concerns over nitrate (Richard, 2014).
Mercury occurs naturally in soil formed from parent materials with a large organic content; mercury has a strong affinity for organic matter. However, anthropogenic contamination through the mining of gold, burning of coal or chlorine production can cause mercury contamination of soil over large areas. Mercury can be methylated by soil organisms causing it to become mobile in the soil leading to surface water contamination or methyl-mercury can be taken up by plants (Xu et al., 2015). Subsequent human exposure occurs through consumption of contaminated water, plants, animals or both. Therefore, the general public is more likely to encounter large concentrations of mercury through ingestion of fish when the water source is contaminated with methyl-mercury, the consumption of vegetation grown in mercury contaminated soil or the improper handling and disposal of compact fluorescent light bulbs (CFLs) (Boerleider et al., 2017; Liang et al., 2015).
Soil can be contaminated with radioactive elements naturally or through anthropogenic activity. There is a wide range of radioactive elements that occur naturally and cause concern (Cygan et al., 2007); radon represents the largest natural radiation dose to humans (Appleton, 2007). Radon is a naturally occurring radioactive gas found in many parts of the world that accumulates in basements and other underground structures (Appleton, 2007). It is known to cause lung cancer in individuals (Islami et al., 2015), and because it is inherent to the soil, proper ventilation of basements to reduce the radon concentration or proper sealing to prevent the entry of radon are the only remedies (Khan & Gomes, 2017).
In addition to naturally-occurring radiation such as radon gas, the anthropogenic release of radionuclides into the environment, including soil, poses an immediate and long lasting threat to human health. Anthropogenically generated radionuclides are often the by-product of medical waste, nuclear waste, nuclear power disasters, or fallout from the testing, use or both of nuclear weapons or dirty bombs that contaminate the soil in the vicinity of or downwind from these point sources (Hu et al., 2010). These forms of radioactive pollution can occur by accident or purposefully. Probably the most publicized releases of radionuclides have been from nuclear power plant disasters, the most recent was the Fukushima Daiichi nuclear plant in Japan related to the earthquake and tsunami in 2011 (Chino et al., 2011). The Chernobyl nuclear disaster in the Ukraine (former USSR) in 1986 was another large accidental release that received considerable attention and which has several implications for human health related to radioactive fallout into soil (Brevik, 2013). The effect of radionuclides on human health can be through either direct exposure to the radioactive materials, which leads to various cancers and genetic mutations (Magill & Galy, 2005), or indirect exposure through the creation of soil nutrient imbalances because of antagonism between elemental nutrients (Brevik, 2013).
Xenobiotic organic chemicals
Xenobiotic organic chemicals are carbon based compounds that are synthesized and therefore unnatural. They are referred to as xenobiotic from the Greek term ‘xeno’ for strange. The differences between these synthesized organic compounds and their natural parent compounds are the common insertion of halogen atoms (chlorine, fluorine, bromine) or multivalent nonmetal atoms (such as sulphur or nitrogen) into the structures (Calabrese & Baldwin, 1998; Salem et al., 2017). Because these xenobiotic compounds contain types of atoms in locations that do not occur in natural compounds, organisms have not evolved adequate pathways of biotransformation to metabolize them. Therefore, the synthetic organic compounds are very resistant to biological decay and are usually markedly toxic to organisms even at extremely small doses. Soil contamination with organic chemicals is a serious problem in all nations (Aelion, 2009). A common hazard from these organic chemicals comes from the application of pesticides in both rural and urban areas, with a large percentage of the applied chemicals reaching the soil (Figure 1). For example, when pesticides were applied to a forest area about 25% reached the tree foliage, about 1% reached the target insect and about 30% reached the soil, with the remainder ending up in the atmosphere and surface or groundwater. Application of pesticides to crops increased the percentage of pesticide reaching the soil compared to application to the forest area (Calabrese & Baldwin, 1998).