Abstract
Production of rice, a major staple food crop, should be maintained both quantitatively and qualitatively to assure global food security. In recent decades, various natural (biogeochemical weathering of rocks) and anthropogenic (increased application of agrochemicals, solid and liquid waste discharges from domestic and industrial areas, vehicular pollution, etc.) activities have deteriorated soil and water resources by contributing potentially toxic elements (PTEs) to the environment. Shortage of land resources and requirements of the ever-increasing human population has led to increasing global trend of rice cultivation in contaminated soils, causing accumulation of various PTEs such as arsenic (As), mercury (Hg), cobalt (Co), cadmium (Cd), copper (Cu), lead (Pb), and nickel (Ni) in rice crop, especially in the grains. Rice plants uptake and accumulate PTEs leading to their entry into the food chain. Consumption of rice contaminated with PTEs disturbs the human metabolism as PTEs interfere with different physiological/molecular mechanisms causing various health problems such as weak bones; skin problems; respiratory, cardiovascular, endocrine, nervous, reproductive, and hepatic disorders; and cancer. Possible non-carcinogenic and carcinogenic health risks have been determined in some studies by following the guidelines provided by various governmental or non-governmental agencies. Considering these facts, the present study was conducted to give a broader perspective on rice contamination with various potentially toxic elements, their bioconcentration in rice, associated health risks in human beings, and strategies for bioremediation of soil and water resources to eliminate PTEs.
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Introduction
Food is a basic necessity for the existence of living beings. Uptake and accumulation of different potentially toxic elements (PTEs) such as metals and metalloids in edible plants, from both terrestrial and aquatic resources, have put all living beings in a food chain in a dangerous situation, where their food quality and health security have been jeopardised (Rafiq et al. 2014). The rapid increase in population in developing countries has led to food and land shortage over the years, which has been compensated by bringing the polluted or contaminated land (near industries, mining areas, and wastewater drains) under cultivation (Zhao et al. 2007; Hu and Ding 2009; Fan et al. 2017; Islam et al. 2019). The problem is further accentuated by the indiscriminate use of chemical-based pesticides and fertilisers to increase the yield of crop plants. The shortage of water resources has also encouraged the use of contaminated domestic and industrial wastewater for irrigation of fields (Chung et al. 2011; Tiwari et al. 2011). All these efforts to increase food production have ignored a major aspect of food safety and cumulatively led to the accumulation of various contaminants in food crops being cultivated in contaminated soils or being irrigated with polluted groundwater or subjected to the injudicious application of agrochemicals (Cao et al. 2010; Nagajyoti et al. 2010; Naser et al. 2012a, b).
Different potentially toxic elements such as aluminium (Al), gold (Au), thallium (Tl), antimony (Sb), tin (Sn), arsenic (As), lead (Pb), vanadium (V), barium (Ba), lithium (Li), bismuth (Bi), cadmium (Cd), mercury (Hg), nickel (Ni), and silver (Ag) may cause respiratory, endocrinal, and genetic disorders, cancer, seizures, hypotension, anaemia, osteomalacia, skin and hair problems, cardiac arrhythmias, and diseases related to stomach, kidneys, reproductive organs, nervous system, etc. (Järup 2003; Duruibe et al. 2007; Kar et al. 2008; Ali et al. 2013; Prashanth et al. 2015; NORD 2019). However, various trace elements such as copper (Cu), chromium (Cr), cobalt (Co), iron (Fe), manganese (Mn), selenium (Se), and zinc (Zn) are important components of biological molecules and play important role in various metabolic and physiological processes essential for normal functioning of the human body, but when present in excess amount, become harmful to human health (Tables 1 and 2) (Prashanth et al. 2015; Al-Fartusie and Mohssan 2017; NORD 2019). Table 1 gives a summary of the literature on some elements explaining their biological role in human beings which become potentially toxic at higher concentrations. Table 2 presents a summary of the literature on various human health hazards posed by different potentially toxic elements.
Food crops from contaminated sites are detrimental at every trophic level of the food chain because of microbial contamination of plants, higher bioaccumulation or bioconcentration of different elements, pesticides, and toxins in different parts of the plants (Khan et al. 2008; Ahmad et al. 2013; Wang et al. 2013). Rice (Oryza sativa L.) is an important staple food crop consumed worldwide (Fu et al. 2008). Among different continents, about 90% of land area under rice cultivation lies in Asia (Rafiq et al. 2014). The International Rice Research Institute (IRRI) compiled data on global production of paddy; production and consumption of milled rice (in Tonnes) from the year 2014 to 2018 (IRRI 2019), which are graphically presented in Fig. 1. Production of paddy and milled rice showed a slight increase from the year 2014 to 2018. However, the production of paddy rice was significantly higher than the milled rice every year. It was observed that in each year, there was very little difference between annual production and total consumption of milled rice, indicating high consumption of rice.
Consumption of milled rice (tonnes) in various countries in the year 2018 was recorded by IRRI (2019) (Fig. 2) and it was found that China is the major consumer of rice followed by India and Indonesia (Rafiq et al. 2014; IRRI 2019). It became evident from Fig. 2 that Asian countries are major consumers of milled rice, where rice is consumed in various forms such as steamed rice, fried rice, rice flour, rice cakes, congee, rice crackers, and puffed rice. According to Zeng et al. (2015a), in rice-consuming nations, contaminated rice is the main source of exposure to PTEs in the human population. The present work is an attempt to summarise recent literature on different sources of soil and water pollution and bioaccumulation of PTEs in rice crop followed by the discussion on possible human health risk posed due to consumption of rice grown in contaminated areas. Few studies regarding remediation strategies to control pollution of soils and irrigation water have also been discussed. During the preparation of this manuscript, the main focus was on literature from 2010 to 2019 and reports from Asia as rice is widely consumed in Asia. However, some reports earlier than 2010 and few from other continents are also included.
Sources of soil and water pollution
Soil is both sink and source of different PTEs (Wuana and Okieimen 2011; Brevik and Burgess 2012). Similarly, groundwater, an essential component of life, also contains different contaminant to varying degrees. All PTEs exist naturally in soil and water but due to anthropogenic activities, elements present in deeper layers of the earth get excavated and dispersed in the atmosphere at concentrations higher than the normal background concentrations (Singh et al. 2018). Different contaminants, i.e. metalloids and metals, e.g. As, Cd, Co, C, Cu, Pb, and Ni, in soil and water are toxic and may harm living beings by invading the food chain. Some of the sources of PTE in soil and water are discussed below:
Geogenic sources
Metals and metalloids exist naturally and are released on the earth crust and introduced into groundwater via geothermal processes, volcanic activities, reductive dissolution of ores and minerals, weathering and erosion of soils, sediments and parent bed rock, etc. (Smith et al. 1998; IARC 2004; Ravenscroft et al. 2009; Patil et al. 2012; Owa 2014; Singh et al. 2018)
Anthropogenic sources
Industrialisation and urbanisation on global scale have led to contamination of different environmental components with various PTEs over the last few decades (Cai et al. 2015). The major anthropogenic sources of contamination in soils and groundwater are sewage discharge, untreated industrial wastewaters, nuclear power plants, mining activities, excessive application and leaching of agrochemicals (pesticides, fertilisers, and insecticides), urban storms, landfill leachates, oil seeping, deposition of atmospheric pollutants, such as coal fly ash released from industries and vehicular pollutants, on soil and surface water, etc. (Hutton 1983; Mehra et al. 1998; Smith et al. 1998; Gulz et al. 2005; Lee et al. 2008; Baba et al. 2010; Mulligan et al. 2001; Irfan et al. 2013; Lim and McBride 2015; Saleem et al. 2018; Chonokhuu et al. 2019; Yadav et al. 2019). As per the European Environment Agency (EEA 2009), the relative contribution of major anthropogenic sources to soil pollution is presented in Fig. 3. It was observed that industrial production and commercial services provided a maximum contribution to soil pollution (36%), followed by the oil industry (17%), municipal waste treatment, and disposal (15%), etc.
Accumulation of potentially toxic elements (PTEs) in rice
Plants, during their life cycle, act as miners of different elements from earth (Peralta-Videa et al. 2009). Transport and accumulation of various PTEs in edible parts of a plant from the soil are a major entry point for their incorporation into the food chain, posing a high health risk to human beings (Fu et al. 2008; Naser et al. 2012a, b; Liao et al. 2013). Accumulation of PTEs in plants from soil is dependent on physico-chemical properties of soil, contents of PTEs in soil, microbial activity in the soil, plant physiology, mechanism of PTE uptake and transport, plant’s mineral requirements, etc. (Tangahu et al. 2011; Sahoo and Kim 2013; Chibuike and Obiora 2014). Plants growing in polluted soils uptake various environmental contaminants, such as metals/metalloids, and accumulate them in different tissues of the plants at varying degrees (Baker 1981). Bioconcentration factor (BCF) is an indicator of the fate of contaminants in the plants. It is a ratio of the concentration of a potentially toxic element (PTE) (metal/metalloid) in a plant (CP) to the concentration of the same PTE in the soil (CS). BCF can be determined as (Huang et al. 2008; Yang et al. 2009):
According to Baker (1981) and Chibuike and Obiora (2014), if a plant is capable of accumulating high content of contaminant (element/metal/metalloid) from the soil, then the value of BCF will be greater than 1, it is called as an accumulator of that specific contaminant. BCF has been addressed as a bioaccumulation factor (BAF) or transfer factor (TF) in some studies (Cao et al. 2010; Šmuc et al. 2012; Kong et al. 2018).
Kong et al. (2018) conducted a study to estimate the bioaccumulation of various heavy metals in rice from a high geological background (HGB) area in Guizhou Province, China. BAF values calculated for different PTEs such as As, Cd, Cu, Pb, and Zn in rice were > 1. BAF values of all metals were higher in the HGB zone of alluvial plain type in comparison to metallogenic belt type except Cd. In another study conducted by Gaurav et al. (2018), BCF values for Cd, Cr, Ni, Cu, Pb, and Zn were > 1 in rice collected from industrial areas (Paper industry, distillery, and sugar mill) in uppermost Ganga-Yamuna Doab region of Saharanpur district. Another study was carried out by Juen et al. (2014) to determine the bioconcentration factor of metals in root, stem, and grains of paddy. Mean BCFs for As (38.40), Co (1.02), Pb (1.81), and Cd (7.10) in roots are > 1. In stems, BCF for only Cd (1.53) is > 1. In grains, none of the metals had BCF > 1. Results indicated that the highest amount of metals (especially As) was accumulated in roots than other plant parts. Transfer of various metals (Zn, Pb, Cd, and Cu) in different organs and tissues (roots, stalk, leaf, and husk) of rice was studied by Wang et al. (2013) in an area near a coal gangue pile in China. BAFs for Zn (1.32), Cd (4.22), and Cu (1.66) in roots were found to be > 1. In the case of stalk tissue, BAF for only Cd (1.02) was > 1. BAFs for none of the metals was > 1 in leaves and husk of rice plants. Liu et al. (2007) studied the accumulation of heavy metals in roots, straw, and grains of rice plants in agricultural soils near Zhengzhou City, People’s Republic of China. It was observed that upper limits of BCFs for Cd (44.13), As (3.76), and Hg (3.90) in roots and for Cd (8.05) and Hg (1.53) in straw tissues of the rice plants were > 1, whereas in case of grains, BCFs for none of the heavy metals exceeded the value of 1. This suggested that aerial parts of the plant absorbed but did not accumulate heavy metals in comparison to roots.
Chen et al. (2018) also estimated BCFs for Cd, Zn, Cu, Ni, Pb, and Cr in rice and wheat grains collected from Lihe River Watershed of the Taihu Region, China. BCFs for different contaminants in rice varied as follows: Cd (0.577) > Zn (0.459) > Cu (0.259) > Ni (0.059) > Pb (0.015) > Cr (0.11), whereas for wheat grains, order of variation was as follows: Zn (0.651) > Cu (0.271) > Cd (0.254) > Ni (0.038) > Pb (0.014) > Cr (0.006). It was observed that BCFs for Cd, Cr, and Ni were relatively higher in rice in comparison to wheat, indicating a higher accumulation capacity of rice for these elements. Lee et al. (2017) estimated BCFs for different elements in rice from abandoned sites in Kyungpook Province, Korea. Mean BCFs were found to follow the order: Cr (0.688) > Hg (0.459) > Cu (0.287) > Mn (0.222) > Cd (0.171) > Zn (0.107) > As (0.042) > Pb (0.029) > Al (0.019). High BCF for Cr indicated a high affinity of rice for Cr (Mohanty et al. 2011; Sharma et al. 2018). Rahimi et al. (2017) determined BAF for Cd, Ni, Pb, and Zn in rice grains from four locations, i.e. Chamgordan, Varnamkhast, Zarrinshahr, and Sede, Iran. It was observed that BAFs for all heavy metals in all locations were < 1 except Cd, which had BCF > 1 in all locations except Sede, Iran. These results also suggested a relatively higher accumulation of Cd in rice in the study area in comparison to other heavy metals analysed. Yadav et al. (2016) estimated BCFs for metals such as Co, Cu, Zn, Ni, Cd, Ni, Cr, and Fe in rice grains from alluvial plain–type area in Fatehabad district, Haryana, India. The mean BCF for different metals in rice grains varied as: Zn (0.11) > Co (0.10) > Cu (0.08) > Cr (0.08) > Ni (0.02) > Pb (0.011) > Cd (0.009) > Fe (0.003). Zeng et al. (2015a) analysed the transfer and accumulation of heavy metals in brown rice from Shimen, Fenghuang, and Xiangtan counties of Hunan Province, China. It was observed that Cd (0.551) had the highest TF, followed by Hg (0.0853), suggesting that Cd had higher mobility than Hg from soil to rice plant.
Šmuc et al. (2012) determined TF in rice crop in Kočani field plant system in the Republic of Macedonia. Order of mean TFs for different elements in rice crop varied as follows: Mo (0.7) > Zn (0.03) > Cd (0.15) > Cu (0.10) > As (0.03) > Pb (0.01). Singh et al. (2011) investigated the accumulation of various heavy metals in paddy irrigated with water from Ramgarh Lake, Gorakhpur, UP, India (experimental site). It was found that contents of Cr, Pb, Cd, As, Mn, Zn, and Hg in roots, straw, and grains of plants from the experimental site were higher than the same in the control site (irrigated with bore well water). Contents of As, Hg, Cd, and Pb were higher in roots in comparison to the other plant parts. Order of BAFs of different contaminants in paddy plants from experimental site was observed as follows: Hg (0.308) > Mn (0.032) Pb (0.028) > Cd (0.017) > As (0.016) > Zn (0.008) > Cu (0.002) > Cr (0.001), whereas for control site, order was as follows: Hg (0.272) > Mn (0.038) > Pb (0.03) > Cd (0.016) > As (0.014) > Zn (0.007) > Cu (0.002) > Cr (0.002). It was evident from the results that BAFs were slightly higher for the experimental site. Order of different contaminants on the basis of TFs in rice grains from an area in the vicinity of an industrial zone in Jiangsu, China, has been reported in a study to be as follows: Zn (0.11) > Cu (0.081) ≥ Cd (0.080) > Hg (0.027) > Cr (0.0084) > Pb (0.0017) where mean contents (mg/kg) of Zn, Cu, Cd, Hg, Cr, and Pb in soils from the area under investigation were 102.70, 31.80, 0.169, 0.235, 97.40, and 29.60, respectively (Cao et al. 2010). The study concluded that Zn, Cu, and Cd were more easily transferred from soil to rice in comparison to other metals. It was revealed from a review of various studies that different PTEs were accumulated to different extents in rice grains depending on different factors such as the physiology of rice plant, its mineral requirements, physico-chemical properties of soil, and bioavailability of different PTEs in soil. Furthermore, it was observed that studies on rice contamination with PTEs were mainly from Asia, where rice is a staple crop and also it is mostly being cultivated either on contaminated soils or irrigated with waste water from industries or untreated/partially treated sewage to meet the needs of the ever-growing population there (Akinbile and Haque 2012; Satpathy et al. 2014; Chakraborti et al. 2018).
Health risks
Contamination of soil and irrigation water with different organic and inorganic pollutants may lead to uptake and accumulation of pollutants in rice (Satpathy et al. 2014). Long-term consumption of contaminated rice may cause various human health problems (Jiang et al. 2017). PTEs such as metals and metalloids are persistent environmental contaminants, which are toxic at varied concentrations (Kar et al. 2008; Reza and Singh 2010; Assubaie 2015; Faisal et al. 2014). Elements such as As, Cd, and Pb have no known biological role and are toxic even at low concentrations (Duruibe et al. 2007; Haloi and Sarma 2012). On the other hand, few elements such as Cr, Co, Cu, Fe, Mn, and Zn are essential for the normal functioning of living beings having a biological role in different metabolic processes and required in minute quantities. However, these essential elements when consumed over long durations or even in small quantities may accumulate in different tissues of the body causing various irregularities such as skeletomuscular, respiratory, gastrointestinal, reproductive, renal, endocrinal, cardiovascular, neurological, hepatic, and genetic disorders, and cancer (Järup 2003; Duruibe et al. 2007; Kar et al. 2008; Ali et al. 2013). The summary of some studies indicating human health hazards posed by exposure to different potentially toxic elements has been presented in Table 2.
Estimation of the potential health risk posed to consumers eating contaminated rice over long durations has been reported in various reports from all over the globe signifying the impact of rice contamination with different PTEs on human health (Table 3). During the literature survey, various reports from different counties such as China, India, Bangladesh, Iran, South Korea, Nigeria, and Thailand were noticed. It was observed that in most of the studies, contents of different PTEs in rice were compared with food safety standards given by different government agencies such as the Joint FAO/WHO Expert Committee on Food Additives (JECFA 2005, 2014), the Ministry of Health of the People’s Republic of China (MHPRC 2005, 2012, 2017), and the Food and Agriculture Organization and World Health Organization (FAO/WHO 2001). In these studies, health risks posed to the human population due to daily intake of rice grains contaminated with PTEs such as Cd, As, Pb, Cr, Fe, Zn, Hg, Cu, Mn, Co, and Ni were calculated and risks were categorised into two categories: non-carcinogenic and carcinogenic. In the case of non-carcinogenic risk, hazard quotient (HQ) and hazard index (HI) were analysed. HQ is an index used to estimate non-carcinogenic health risk whereas HI is the sum of HQs estimated for different PTEs and used for assessment of overall non-carcinogenic health risk posed to consumers. Similarly, to analyse the possibility of cancer occurrence in the population, another index, i.e. cancer risk (CR), is being used. If CR was estimated for more than one PTE, then CR posed by individual PTEs were added to estimate total cancer risk (TCR). Results were compared with the safe limits given by USEPA (2010). HQ or HI > 1.00 and CR or TCR > 1.00E−06 indicated a high possibility of occurrence of non-cancerous health problems and cancer, respectively. In many reports, abbreviations used for risk assessment were different as some used abbreviations, NHQ (non-carcinogenic hazard quotient), THQ (target hazard quotient), and HRI (health risk index) instead of HQ. In some reports, HI was replaced with the following abbreviations: THI (total hazard index), THQ (total hazard quotient), TTHQ (total target hazard quotient), and AR (accumulative risk). In place of CR, other abbreviations such as TCR (target carcinogenic risk) and “Risk” have been used. Similarly, in some reports, TCR has been replaced with Risktotal. It was observed that in most of the studies given in Table 3, PTEs such as As, Pb, Cd, Co, and Cr exceeded the corresponding food safety limits prescribed by different agencies as mentioned earlier and were reported to pose health risks to the human population such as paralysis, depression, encephalopathy, seizures, oedema, dermatitis, anaemia, cardiomyopathy, osteoporosis, proteinuria, renal tubular dysfunction, emphysema, reproductive disorders, and cancer as described in Table 2.
Remediation strategies
Removal of PTEs from soil and water is necessary to alleviate the problem of uptake and accumulation of these contaminants by plants from soil and irrigation water. Bioremediation is a method which utilises living organisms, i.e. microorganisms or plants or both for the removal of PTEs from the environment, i.e. soil and water (Chibuike and Obiora 2014). Phytoremediation, an eco-friendly method, is a bioremediation technique which uses hyperaccumulating plants, such as Jatropha curcas L., Lactuca sativa L., and Brassica juncea L., for removal of PTEs from the environment (Cioica et al. 2019). There are different mechanisms of phytoremediation: phytoextraction (extraction of contaminants from soil/water and transport to other plant parts), rhizofiltration (uptake of contaminants from wetlands or wastewater streams), phytostabilisation (immobilisation of contaminants in plant tissue and conversion in less toxic form by complexation or metal precipitation or reduction of contaminants), and phytovolatisation (uptake of contaminants by plants and release in the environment in form of less toxic volatile forms via transpiration) (Mahajan and Kaushal 2018). Bioremediation, using microorganisms, is a highly efficient and low-cost technique for degrading different contaminants into less harmless forms for decontaminating soils, waste water, and sediments (Mejáre and Bülow 2001). Microbes such as Pseudomonas putida, Bacillus subtilis, Ralstonia eutropha, and Enterobacter cloacae have been used to sequester or reduce heavy metals in harmless forms (Chibuike and Obiora 2014).
Addition of soil amendments in the form of organic wastes after composting or vermicomposting add organic matter to the soil which retains heavy metals in soil decreasing their mobility and also increases soil fertility (Huang et al. 2016a). The addition of inorganic amendments such as lime to soils for reduction of metal uptake by plants is applied globally (Khan and Jones 2009). Treatment of waste waters before irrigation, rainwater harvesting to collect rain water for irrigation, and treatment of solid and liquid wastes before dumping them in land resources are some other techniques that can be used for avoiding the problem of soil contamination (McLaughlin et al. 1999). Few studies using different remediation techniques for reduction of contents of different PTEs in soil by using hyperaccumulator plants or reduction of uptake of PTEs by plants via their stabilisation in soil have been summarised in Table 4.
Conclusion
The quality of rice crop has deteriorated globally due to both geogenic and anthropogenic contamination of soil and irrigation water with PTEs after the advent of the industrialisation era. Rice being a staple food in majority of countries in the world has led to transfer of contaminants to human bodies through food chain. Consequently, the occurrence of various health problems (both carcinogenic and non-carcinogenic) in rice consumers has increased over the years. It was evident from the literature survey that in most of the studies, contents of As, Cd, and Pb in rice plants exceeded the safe limits provided by different agencies. These contaminants also posed health risks to rice consumers. Therefore, it is important to avoid accumulation of PTEs in rice crop by different remediation techniques such as phytoremediation and bioremediation of soil, and irrigation of water by using plants and/or microorganisms. Moreover, treatments of solid and liquid wastes from domestic sectors and industries before their disposal, rain water harvesting, and soil amendments are also few strategies to control rice contamination.
Data availability
None
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The authors would like to thank the Guru Nanak Dev University and DAV College, Amritsar, for providing internet and library facilities for the collection and review of the literature.
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Sharma, S., Kaur, I. & Nagpal, A.K. Contamination of rice crop with potentially toxic elements and associated human health risks—a review. Environ Sci Pollut Res 28, 12282–12299 (2021). https://doi.org/10.1007/s11356-020-11696-x
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DOI: https://doi.org/10.1007/s11356-020-11696-x