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Review

A Review of Environmental Contamination and Health Risk Assessment of Wastewater Use for Crop Irrigation with a Focus on Low and High-Income Countries

1
Department of Environmental Sciences, COMSATS Institute of Information Technology, 61100 Vehari, Pakistan
2
Institute of Soil and Environmental Sciences, University of Agriculture Faisalabad, Faisalabad 38040, Pakistan
3
MARUM and Department of Geosciences, University of Bremen, D-28359 Bremen, Germany
4
Southern Cross GeoScience, Southern Cross University, Lismore, NSW 2480, Australia
*
Authors to whom correspondence should be addressed.
Int. J. Environ. Res. Public Health 2018, 15(5), 895; https://0-doi-org.brum.beds.ac.uk/10.3390/ijerph15050895
Submission received: 27 March 2018 / Revised: 22 April 2018 / Accepted: 24 April 2018 / Published: 1 May 2018
(This article belongs to the Special Issue Studies on Heavy Metals and Health)

Abstract

:
Population densities and freshwater resources are not evenly distributed worldwide. This has forced farmers to use wastewater for the irrigation of food crops. This practice presents both positive and negative effects with respect to agricultural use, as well as in the context of environmental contamination and toxicology. Although wastewater is an important source of essential nutrients for plants, many environmental, sanitary, and health risks are also associated with the use of wastewater for crop irrigation due to the presence of toxic contaminants and microbes. This review highlights the harmful and beneficial impacts of wastewater irrigation on the physical, biological, and chemical properties of soil (pH, cations and anions, organic matter, microbial activity). We delineate the potentially toxic element (PTEs) build up in the soil and, as such, their transfer into plants and humans. The possible human health risks associated with the use of untreated wastewater for crop irrigation are also predicted and discussed. We compare the current condition of wastewater reuse in agriculture and the associated environmental and health issues between developing and developed countries. In addition, some integrated sustainable solutions and future perspectives are also proposed, keeping in view the regional and global context, as well as the grounded reality of wastewater use for crop production, sanitary and planning issues, remedial techniques, awareness among civil society, and the role of the government and the relevant stakeholders.

Graphical Abstract

1. Introduction

Water is an essential component of life, but it is a susceptible and finite resource that has qualitative vulnerability and quantitative limitations. It is expected that 60% of the total world’s population may face the problem of a water shortage by the year of 2025 [1]. In the areas where fresh water is in short supply, wastewater is frequently used for crop irrigation. Although not legally permitted in most countries, the use of untreated wastewater for crop irrigation has been practiced in many countries worldwide due to the shortage of good quality water [2,3,4].
Wastewater production sources include different human activities, such as industrial, commercial, and domestic activities. Municipal wastewater is also sometimes distinguished into urban, rural, and agricultural areas/sources. With the rapid expansion of the population, cities, industries, and the domestic water supply, the quantity of wastewater production is increasing at the same proportion [5]. The average volume of wastewater generated daily by human activities depends on the availability of the water quantity in the house, the cultural level/type, the cost of the water, and the economic conditions [6].
Agriculture is the most common area in which untreated wastewater is reused. According to an estimate in 2004, approximately 20 million ha is irrigated with wastewater in fifty countries worldwide [7,8]. The use of wastewater for crop irrigation has further increased in recent years. The municipal wastewater demand corresponds to 11% of the water withdrawal, globally [9]. About 3% of the municipal wastewater demand is consumed and the remaining 8% is being discharged as wastewater; that is, 330 km3 of wastewater per year [9], which is potentially irrigating almost 40 million ha (approximately 8000 m3 per ha) [9] or 15% of all irrigated lands.
Wastewater usage for crop irrigation has certain advantages such as providing the essential nutrients and organic matter, saving water and nutrients, and reducing water contamination [2,10]. It has been reported that quite sufficient quantities of macronutrients (N, P, and K) are supplied to soil and plants via wastewater application [10]. Therefore, it is a great temptation for poor farmers to irrigate crops with wastewater as it can reduce the crop production cost [11], with the cost of crop production decreasing by 10%–20% when irrigated using wastewater.
Besides these benefits, a number of drawbacks are associated with the use of wastewater for crop irrigation [4,10,12]. Wastewater contains potentially toxic elements (PTEs) such as zinc, chromium, copper, cadmium, nickel, lead, mercury, and parasitic worms, which can induce severe risks to the human health and the environment [13,14,15]. The use of untreated wastewater for crop irrigation can also cause soil hardening and shallow groundwater contamination [16,17]. However, the main problem of wastewater crop irrigation is the presence of potentially toxic elements (PTEs) [4,18,19] (Figure 1). The build-up of PTEs in the soil and crops by wastewater irrigation results in soil contamination, and in turn, affects food safety [4,20,21].
The contamination of agricultural soils by wastewater application poses health risks due to the presence of PTEs which have long-term implications for the environmental and health [22,23]. Soil contamination with PTEs is the main route of their exposure to humans via food crop consumption, which could cause various health issues in humans if the PTE concentration exceeded the safe limit [24,25,26,27]. The long-term use of PTE-contaminated vegetables can cause the continuous build-up of toxic metals in the kidney and liver of humans, causing disorders in the physic-biochemical processes [28,29,30]. Studies regarding the health risk assessment after the consumption of PTE contaminated food/vegetables are being performed in developed countries. However, very little is explored in less developed countries [20,28,31].
However, there exists a considerable difference in the collection, treatment, and reuse of wastewater for crop irrigation between low and high-income countries [10]. This variation among the two groups can be due to several factors such as the availability of fresh water for crop irrigation, the availability of resources to treat wastewater, the awareness among the farming community about environmental and human health issues related to wastewater crop irrigation, and the implementation of laws of wastewater use in the agriculture sector [4,10,12]. Moreover, there are social, economic, and corporate issues that are also affecting the wastewater treatment and reuse for crop irrigation between low and high-income countries.
There exists abundant data regarding the generation of wastewater, its use for crop irrigation, and the associated environmental and health risks at the national and global level. However, there are contrasting opinions about the value of wastewater for the irrigation of crops. Some studies valued it as a source of essential crop nutrients and a management practice, while opponents claimed it an act of criminal negligence owing to its environmental and health issues [20,28,31]. A comprehensive review highlighting all these aspects at a national and international scenario can be of great use for researchers, scientists, and policymakers. Therefore, in this review, we highlight and compare the current scenario of wastewater production and use for crop irrigation and the associated environmental and health risks at the national and global level. Moreover, the review traces the history of wastewater use for crop irrigation and proposes some future perspectives and management strategies to minimize the risks associated with the use of wastewater for crop irrigation.

2. The Current Global Scenario of Wastewater Use for Crop Irrigation

Nowadays, under freshwater scarce conditions, it becomes almost mandatory for farmers to consider and use any sources of water, especially in many arid and semi-arid regions [12]. Consequently, crop irrigation using wastewater becomes a valid option, urged by the lack of feasible alternatives [10]. The agricultural sector uses a major portion of the total municipal water reuse [32], which accounts almost 70% of the total agricultural water consumption [33]. It has been reported that untreated or partially treated municipal/industrial wastewater is used for the irrigation of about >20 million ha of crop worldwide [2].
Nowadays, the use of wastewater for crop irrigation has gained considerable attention. With the rapid advancement, development, and wide acceptance/application of wastewater treatment technologies, the use of treated wastewater has increased in developed countries [34,35]. Globally, the use of wastewater for crop irrigation has increased about 10–29% per year in Europe, the United States, and China, and by up to 41% in Australia [35]. Table 1 presents the data about the total wastewater produced, collected, treated, and used for crop irrigation in different countries around the globe [9].
The global wastewater discharge reaches 400 billion m3/year, contaminating ~5500 billion m3 of water per year [2]. The nature and the quality of the wastewater used vary within and between the countries. It has been stated that 15 million m3/day of reclaimed water is reusing by approximately 44 countries for irrigation purposes [36]. Globally, the use of untreated wastewater for urban and peri-urban agriculture accounts for about 11% of all the irrigated croplands [37]. It is estimated that 10% of the global population consumes food produced from wastewater irrigation [38].
The practice of crop irrigation with wastewater is not well-regulated in low-income countries, and the environmental and economic issues are poorly understood [10,12]. Some poor countries use raw sewage for irrigation purpose, although its use is considered illegal [39]. In less developed and low-income countries such as Asia, Latin America, and Africa, wastewater is used for irrigation without any treatment [5,40]. However, on the other hand, in middle-income countries, wastewater is used after treatment [9].
Wastewater use for crop irrigation is practiced in several countries globally [41]. According to the estimation in fifty countries, wastewater is used to irrigate 20 million ha [42]. China is ranked the number 1 country in the world based on the total population and is also the top-ranked country by the volume of wastewater generated. About 68.5 billion tons of wastewater was discharged from municipal and industrial sources in 2012, which is comparable to the annual flow volume of the Yellow River [43]. Furthermore, the 1st National Pollutant Source Census Bulletin [44] estimated that about 108.16 billion cubic meters of wastewater (34.33 billion cubic meters from domestic sources and 73.83 billion cubic meters from industrial sources) were being generated per year in China.
It has been reported that the wastewater produced in China annually is used for irrigating an area of about 1.33 × 106 ha [45]. Although China has adopted urban wastewater reuse programs, its development at the national level is slow. In India, about 38,354 million liters of wastewater is produced per day in major cities, while the treatment capacity is only 11,786 million liters per day. In India, approximately 2600 million m3 of untreated wastewater is used for crop production [19]. It has been estimated that about 73% of urban wastewater generated in India remains untreated (Development Finance Corporation) [46]. In Mexico, about 70,000 ha are irrigated with processed wastewater, while about 260,000 ha is irrigated with untreated wastewater [47]. Informal irrigation in Ghana involving wastewater diluted from streams and rivers occurs on 11,500 ha of an area larger than the reported extent of the formal irrigation in the country [48].

3. The Wastewater Use and Treatment in Low and High Income Countries

Globally, about 330 km3/year of municipal wastewater is generated, which can theoretically irrigate and fertilize crops grown on millions of hectares. However, the fate of this wastewater is very different in low and high-income countries. In the literature, the data on the fate (collection, treatment, and reuse) is scarce and scattered globally. Only a small portion of waste is currently treated and the share of the treated wastewater that is used for crop irrigation is significantly low. According to the Food and Agriculture Organization (FAO) [9], globally, about 60% of the total municipal wastewater generated is treated before its reuse. The data on the percent of untreated wastewater discharged into the environment is presented in Figure 2 [49]. It is evident from Figure 2 that the wastewater released into the environment, in the treated or untreated form, greatly varies between low and high-income countries. Currently, 92% and 30% of untreated wastewater is discharged into the environment, respectively, in low and high-income countries [9].
High-income countries have established wastewater treatment facilities. It has been reported that, globally, more than 80% of the facilities of wastewater treatment have been identified in developed countries such as the USA, Japan, and Europe. For example, in France, there are over 17,000 wastewater treatment plants and 15,000 water treatment plants. The sewerage network in France is nearly 800,000 km long. China has 3272 urban sewage treatment plants, which can treat about 140 million cubic meters of sewage per day (Ministry of Housing and Urban-Rural Development of the People’s Republic of China) [50]. The USA had 15,591 treatment facilities in 2000. In California, more than 75% of the processed wastewater is used for crop irrigation.
Low-income countries have very low or limited wastewater treatment facilities. For example, in east India, wastewater treatment plants neither exist nor function adequately [51]. In low-income countries, the wastewater released from industrial and municipal sources is used for crop irrigation directly, with no or very little dilution. In some cases, the wastewater is first released into water bodies where it undergoes dilution prior to its use for crop irrigation. In this way, the effect of wastewater irrigation on the soil, plants, and human health may vary when used with or without prior dilution.
In many low-income countries, the absence of technical and financial resources makes it very difficult to efficiently collect and treat wastewater. For example, approximately 30% of the total wastewater produced is directly used for the irrigation of 32,500 ha of crops in Pakistan [52], while 64% of the wastewater is directly discharged into water bodies without any pretreatment [4]. In India, only 24% of wastewater from the industrial and municipal sectors are treated [53].
The situation of wastewater collection and treatment is even worse in West African countries, where usually <10% of the wastewater produced is collected in sewage systems [54]. Firstly, the wastewater treatment facilities are totally missing in developing countries. In the cases where the wastewater treatment facilities are available, the sustainability of these facilities is a big issue in developing countries. In many cities in Asia and Africa, large centralized wastewater collection and treatment plants/systems have failed to be sustained and are not functional.
Consequently, the decentralized wastewater collection and treatment systems have been promoted in low-income countries as they are more flexible for long-term operation and financial sustainability [55]. For example, in Ghana, only 7 out of 44 smaller treatment plants are operational and, generally, none of them meet the designed effluent standards [54].
There exists limited data in the published literature about water disposal and treatment, as well as its use in the agricultural sector of developing countries compared to developed countries. In fact, in developing countries, there are no proper university-industry research linkages, which is one of the main reasons for the lack of problem-oriented research in these countries. The lack of scientific/research data and university-industry research linkages in these countries makes it difficult to establish policies, planning, and laws for environmentally friendly practices, especially in the agricultural sector.
Moreover, the economic and social factors, as well as the lack of awareness and knowledge of the environmental and health risks among the people of developing countries also hinder the adaptation and implementation of these environmentally friendly practices. Although there is a significant improvement regarding the problem-oriented research in the last decade, especially in the Indo-Pak sub-continent, many key steps are needed for the proper implementation of environmentally friendly practices in developing countries. The role of research institutes/universities and funding agencies, as well as government organizations, could play a key role in this regard. Poverty is also considered an important factor behind the use of wastewater for crop irrigation, especially in less-developed countries. Farmers with small agricultural land holdings prefer to use wastewater for irrigation despite the availability of fresh water. This is due to the low-cost of crop production by adopting this irrigation practice.
In some developing countries, the limited public awareness, the less commercial development of wastewater recycle/reuse, and the social setup are some of the other key challenges faced in the realm of wastewater use for the agricultural sector. Wastewater recycling/reuse seminars, commercial operation mechanisms, and fiscal support from the government can be highly effective in mitigating the environmental and health issues related to the use of wastewater in the agricultural sector.
The above-mentioned facts clearly show an alarming gap of environmentally-friendly practices and environmentally sustainable approaches regarding water treatment among the developed and developing countries, especially in the highly populated (and continual growing) areas of South and Southeast Asia. There is a need at the global level to do more and shrink down this lacuna. In this regard, the role of the environmental and health organizations working at the national and international level is critically important.

4. Potential Impacts of Wastewater Irrigation on Crops

The use of wastewater for crop irrigation in the agricultural sector has the potential for both negative and positive effects (Table 2) on the soil quality/productivity, crop production, and human health [4,12] (Figure 3). Wastewater may contain unwanted pathogens and chemical constituents that pose health and environmental risks. The negative effects of crop irrigation with wastewater are primarily due to the presence of high total suspended and dissolved solids, high nutrient contents, and PTEs [3,4,16,56]. Wastewater may contain high concentrations of salts which can affect the soil quality and productivity by accumulating in the root zone. The prolonged use of saline and sodium-rich wastewater can deteriorate the soil structure and affect the soil productivity [4]. Soil salinization due to wastewater irrigation has been extensively reported during the recent years [57]. The major effect of wastewater on crop productivity is due to the presence of heavy metals, which are well-known to negatively affect crop productivity [58].
Wastewater may also carry viruses, bacteria, nematodes, and protozoa, which can cause different diseases [59]. Wastewater application may also affect the physic-chemical properties of soil, which, in turn, modifies the soil quality and fertility. Mireles et al. [60] reported that the agricultural sites (Mixquiahuala, Hidalgo and Tláhuac, D.F) previously irrigated with wastewater for more than 50 years in Mexico City show deterioration of the soil and now only certain plant species can be cultivated at these sites.

5. The Effect of Wastewater on the Physico-Chemical Properties of Soil

Wastewater application changes some physicochemical properties of the irrigated soil. Several previous studies have shown that the application of wastewater significantly changes the soil’s physical, chemical, and biological properties [80], which can, in turn, alter the biogeochemical behavior (mobility and bioavailability) of metals and other nutrients. Therefore, the variation in soil properties as a result of wastewater application can have a significant impact (both positive and negative) on the soil quality and crop productivity (Figure 1).

5.1. The Effect of Wastewater on Soil pH

The soil pH is the master variable that controls the partitioning of metals between the solid and solution phases of soil. The soil pH affects the adsorption/desorption of PTEs in soils [81], and, in turn, their biogeochemical behavior in the soil-plant system [82]. There exists a negative correlation between the soil pH and the PTE bioavailability to plants for several PTEs [83]. Most vegetables grow at their best in soils having a pH between 6.0 and 7.5 due to the increased availability of most of the nutrients. There exists a complex variation regarding the effect of wastewater irrigation on soil pH [84]. Wastewater is a source of acidic substances and irrigation using wastewater decreases the soil pH due to the decomposition of organic matter and the formation of organic acids in the soils [85,86]. In the majority of studies, the soil pH significantly increased after long-term irrigation with wastewater from different sources [87,88]. In some studies, however, soil pH was unaffected by long-term wastewater irrigation [89] while others reported decreased soil pH [19,89].
An increase in the soil pH as a result of the wastewater application might be due to the sulfate contents in the wastewater [90]. In general, the effect of wastewater irrigation on the soil pH depends on the pH of the wastewater source and the pH buffering capacity of the soil. Generally, the change in the equilibrium of the complex dynamic reactions taking place simultaneously in the soil may affect the soil pH after wastewater application. Previous studies [4,91,92,93] reported increased pH of soil under wastewater irrigation.
On the contrary, other studies reported decreases in the pH by wastewater irrigation [94,95,96,97,98]. The decrease in the soil pH after wastewater irrigation is due to the production of H+ ions produced during the oxidation reactions, while the decrease in soil pH is due to neutralization of the H+ ions by calcium carbonate in wastewater/sludge. Therefore, the overall effect of wastewater application on the soil pH depends on the initial soil pH as well as the cation/anion ratio and chemistry of the wastewater.

5.2. The Effect of Wastewater on Soil Organic Matter

Soil organic matter (SOM) is the second most important parameter determining soil quality, after pH. SOM governs the biogeochemical behavior (mobility/bioavailability) of metals and nutrients in the soil-plant system [81,99]. The processes controlling the metal behavior in soil mainly depend on the nature/type of organic matter. SOM is reported to exist in either a suspended or dissolved form in an aqueous medium [100]. When presented in the dissolved form, SOM can form metal-OM complexes with metals, while in the solid phase, SOM can adsorb metals from the aqueous medium [81]. Therefore, SOM can greatly affect (increase or decrease) the mobility of PTEs in soils and their availability to plants [101,102]. Organic matter (OM) also acts as a sink of essential nutrients which are important for plant growth [103]. The SOM content is also important for controlling the microbial activity in soil [104,105]. Large OM inputs enhance the microbial organism’s growth and block soil pores that cause decreases in soil infiltration and favor the anaerobic microbiological growth due to aeration problems in the soil [104,105,106,107].
Organic matter accumulation in the surface soil as a result of wastewater irrigation has been reported previously [4]. The application of wastewater will increase the OM contents in the soil which is considered a beneficial effect for soil [3]. The addition of organic matter into the soil through wastewater application improves the soil structure and the moisture content’s increased cation exchange capacity and helps to retain the metals and reduce their bioavailability and mobility and adds nutrients into the soils [108,109,110].
However, higher organic matter concentrations through wastewater application can have an adverse effect on the soil porosity and create anaerobic conditions in the root zone [111]. In addition, if an agricultural runoff having a higher OM concentration reaches the surface water, it may cause the dissolved oxygen depletion in the water, resulting in hypoxic conditions and thus, increasing the aquatic species mortality [108]. Continuous wastewater usage for irrigation significantly altered the water infiltration into soil due to the blockage of water transmission holes by organic matter [112]. The reduced soil water efficiency and lower water retention, as well as increased surface runoff and altered water infiltration, will have significant implications for the crop water use and the soil water balance.

5.3. The Effect of Wastewater on Soil Cations and Anions

Irrigation water comprises of inorganic constituents; primarily, the dissolved nutrients (Table 2) and salts, however, these salts vary greatly in both composition and concentration. The major constituents of dissolved salts are cations which include magnesium (Mg2+), sodium (Na+), and calcium (Ca2+) and anions which include sulfate (SO42−), bicarbonate (HCO3), and chloride (Cl) [113]. Soil irrigation with wastewater generally adds significant quantities of cations, as well as their salts such as sulfates, phosphates, bicarbonates, and chlorides [113,114]. It is well known that the application of wastewater modifies the cation concentration in soil, which, in turns, affects the metal/nutrient balance between solid and aqueous phase soil [4,10]. However, the effect depends on the concentration of these cations in the applied wastewater.
Moreover, the concentration of these cations in the soil also varies with the type of vegetable cultivated because the nutrient uptake and accumulation varies with the vegetable type [4,115]. Vegetables are reported to be a rich source of nutrients and are capable of up-taking cations (Na, K, Ca, and Ba) in high quantities compared to crops and plants. Several studies [4,91] reported the increase in the concentrations of Ca, K, and Mg in the soil and in vegetables due to the wastewater application in irrigation.
In some studies, the application of wastewater provides the N, P, and K contents up to 4, 8, and 10 times more than needed by forage plants [116]. Thapliyal et al. [91] also reported total N contents values that are several times higher in soil irrigated with wastewater. Christen et al. [117] reported that long-term winery wastewater application on pastures resulted in the increased availability of K contents and had the potential of groundwater leaching and other water sources. Although the higher K ion content effects applied in the soil have not been studied extensively, its long-term application could cause the alteration of the soil physicochemical properties [118]. The excess concentration of Na is detrimental to the soil structure and reduces the soil’s capacity significantly to transmit water [4]. Wastewater application enhances the Cl concentration in the soil which exceeds the crop tolerance and the crops develop injury symptoms [119].
Overall, the worth of wastewater as a source of crop nutrients depends on the soil fertility level, the type and species of the crop grown, and the concentrations of the nutrients in the wastewater. The efficiency nutrient use for wastewater is nearly 100%. This is because the nutrients present in wastewater are commonly found in a dissolved form and, therefore, they are easily available for plant uptake. Moreover, the wastewater-induced nutrient supply matches the demand of crops because nutrients are supplied in patches with each irrigation, compared to synthetic fertilizers which are usually applied to crops in two to three splits [4,120].
The use of wastewater has been reported to save up to 94% and 45% of fertilizer required, respectively, for alfalfa and wheat [121]. It is reported that wastewater containing an average concentration of 35 mg/L of N, 10 mg/L of P, and 30 mg/L of K, largely fulfills the requirements of most vegetables and crops [6]. Usually, farmers benefit not only in terms of fertilizer savings but also in terms of improving the fertility of the soil. This also has an additional benefit for society by reducing the greenhouse gases produced during fertilizers, especially the nitrogenous manufacturing and supplying [122,123,124].
The effect of wastewater application on the soil nutrient status and the nutrient use efficiency is also reported in terms of crop production. It was observed that in comparison with the groundwater, the yield of marketable fruit was higher with wastewater [125,126]. Some other studies [4,127,128,129] also showed that wastewater irrigation significantly increased the dry and fresh forage yield of crops and vegetables in comparison with the well-water irrigation.

6. The Effect of Wastewater on Soil Microbial Community

The soil is a heterogeneous environment in both space and time and the microbial activity is focused at the localized sites on and around the organic residues. Decomposer communities undergo succession as inorganic and organic residues are changed.
The application of wastewater has been reported to affect soil microbial activity and community establishment (Table 3).
The effect of wastewater application on soil microbial activity can be direct or indirect via the changing of the soil physic-chemical properties [139,140]. In many low-income and developing countries, the use of wastewater for crop irrigation is one of several sources of pathogens [12]. Consequently, the quality of food and hygienic conditions remain critical even in areas where the irrigation water (wastewater) appears safe.
In metal contaminated soils, the change in the soil microbial diversity or shift from bacterial to fungal population has been reported [141]. The long-term municipal wastewater application has been revealed to reduce the diversity of the arbuscular mycorrhizal fungi [142] and some types of wastewater such as olive mill wastewater have been reported to have an impact on the microbial community structure [143,144]. Wastewater irrigation in soil altered the ammonia-oxidizing bacterial population and the Nitrosomonas and Nitrosospira species became dominant [144].
Wastewater use for irrigation may be the source of the beneficial bacteria for soils [145]. Wastewater and soil both have quite different characteristics, but are inhabited by a wide diversity of the bacteria. For example, in N cycling, the bacteria involved with the ability to remediate soil contaminants (for example, PTEs, antibiotics, or pesticides) may contribute to the improvement of the soil quality [146,147].
The increase in the activity of some enzymes (for example, laccases, hydrolytic, cellulases, phosphatase, proteolytic) has been reported in the soils irrigated with the treated wastewater [148,149,150,151,152]. This effect may be due to the provision of the organic carbon as suggested by the simultaneous increase in the activity of dehydrogenase, generally a parameter indicative of the biological oxidation of the organic compounds [152].
The irrigation of soil with wastewater is expected to stimulate different metabolic pathways and organisms through the supply of nutrients and organic matter. It is, thus, suggested that the irrigation of wastewater may stimulate microorganism activity involved in the biochemical balance of the elements such as N, P, and C [146,147]. However, the stimulation of the soil microbial activity and the abundance may have negative effects on the soil properties.

7. The Effect of Wastewater on Potentially Toxic Elements in the Soil-Plant System

7.1. The Effect of Wastewater on the Concentration of Potentially Toxic Elements in the Soil

Wastewater irrigation leads to the PTE accumulation in soil. In some countries, the groundwater contains high concentrations of PTEs [153,154,155,156,157,158], which also results in high levels of these elements in wastewater. Sewage water has been implicated as the potential source of PTEs such as Cd, Cu, Ni, Cr, Pb, and Zn in the soil, plants, and food items (Table 4). These PTEs have high environmental persistence due to their non-degradable nature and are readily accumulated in the soil to toxic levels [27,102,159,160]. Wastewater irrigation is well-reported to cause the disproportionate accretion of PTEs in soils [161,162]. A linear relationship of the wastewater irrigation period with the buildup of PTEs in the soil has been found [163,164]. As a matter of fact, the long-term soil irrigation with wastewater can be responsible for the soil contamination by PTEs [22,108,116].
Nowadays, the presence of PTEs in wastewater is abundant due to the excessive use of these elements in industrial activities and household articles [165,166,167,168]. Many studies worldwide have emphasized the risk of PTE accumulation in wastewater irrigated topsoil [169,170,171,172]. The levels of these PTEs in wastewater vary between regions and depend on the volume, source composition, and treatment of wastewater.
Several past studies from developing and developed countries reported PTE accumulations in the soil as a result of wastewater application. Compared to groundwater irrigated soils, high PTE contents in soils have been reported in different regions around the globe (Table 2) such as Fe, Cr, Co, Mn, Ni, Cu, Zn, and Pb in Mixquiahuala, Hidalgo, and Tláhuac, D.F. of Mexico City [60]; Cr, Pb, Ni, and Zn in Tongliao, China [186]; Cd, Cu, Zn, Pb, Cr, Mn, and Ni in suburban areas of Varanasi-India [187]; Cd, Cr, Cu, Pb, and Zn in the Bani–Malik wastewater treatment plant of Jeddah, Saudi-Arabia [132]; Cd, Cu, Cr, Ni, Pb, and Zn in Pakistan [188]; Cd, Ni, Cr, Zn, Cu, and Pb in Hanoi, Vietnam [189]; Zn, Cu, Mn, Cd, Pb, Ni, Fe, and Cr in Harare [190]; and Cd, Cu, Pb, and Zn near Nhue River, Vietnam [191]. Abdu et al. [176] reported soil concentrations of Pb (0.6–46 mg/kg), Cd (2.3–4.8 mg/kg), Ni (0–17 mg/kg), Cu (0.8–18 mg/kg), Zn (13–285 mg/kg), and Cr (1.8–72 mg/kg) in seven vegetable gardens from the three West African countries of Nigeria, Burkina, and Mali under 30 years of wastewater application. Khan et al. [76] reported increases in the PTE concentrations (Cr, Ni, Pb, Mn, and Cd) in soil irrigated with wastewater. Similarly, Khan et al. [20] reported a substantial buildup of Pb and other PTEs in the wastewater-irrigated soils compared to the control soil. Several other studies also reported PTE build-ups in the soil in different areas around the globe.
Despite the low levels of PTEs in most wastewaters, the soil may accumulate high levels of PTEs due to the continuous and long-term soil irrigation with untreated wastewater [4]. The long-term application of untreated and treated wastewater has resulted in significant increases of PTEs in the soil [19,92,142] as well as groundwater leachate through dumpsites [192].
Many studies conducted in Southeast Asian countries such as India, China, and Pakistan, where industrial effluent with sewage water (untreated or diluted) is widely used for irrigation found that Cd, followed by Pb, were the major metals which caused a risk to human health [4,21,188,193]. In most of these studies, the concentration of Pb and Cd exceeded the permissible limits for the PTEs in irrigation water; that is, the WHO/FAO standards of 5.0 and 0.01 mg/L for Pb and Cd, respectively [4,76,194]. Generally, due to higher mobility, Cd is a major relevant PTEs presenting a risk to human health; additionally, because it is bioavailable to plants at very lower concentrations that are not phototoxic but cause health risks to humans [167].
In peri-urban regions of Pakistan, vegetables and crops are frequently irrigated by wastewater without any primary treatment due to the non-availability of fresh water [195,196,197,198,199]. In different areas of Lahore-Pakistan, the continuous use of wastewater for irrigation in the agricultural areas has caused a buildup of highly toxic metals compared to the soil irrigated by groundwater [173]. Amin et al. [200] reported that the Pb concentration in the soil irrigated by wastewater was four times higher than the soil irrigated by tube-well water in Mardan-Pakistan.
Generally, irrigation with wastewater elevates the total and available PTE concentrations in soils. Heavy metals introduced into the soil via wastewater irrigation accumulate primarily in the surface layer and are generally more mobile and bioavailable than those released from the parent rocks [201]. Therefore, PTE addition to the soil by wastewater application may represent more threats to plant contamination than natural sources of PTE contaminations. The soil physico-chemical properties (electrical conductivity, pH, soil mineralogy, cation exchange capacity, and biological and microbial conditions) and the presence of soil organic and inorganic ligands greatly influence the mobile and bioavailable portion of PTEs in the soil [166,202]. In fact, all these soil properties and constituents control the basic physical, chemical, and biological processes that determine the fate and behavior of PTEs in soils [203,204].

7.2. The Effect of Wastewater on Potentially Toxic Element Accumulation in Plants

The soil is the direct pathway for the contamination of plants by PTEs via root uptake. Vegetables and crops irrigated by wastewater take up high concentrations of PTEs which may cause health risks to the users (Table 4 and Table 5). Several studies have demonstrated that wastewater irrigated plants may absorb and accumulate PTEs in concentrations greater than the maximum permissible limits (MPLs) with serious public health implications [4,73,164,205].
Several previous studies have also reported the high accumulation (above the toxic limit) of PTEs in different edible parts of crops/vegetables around the globe (Table 4): for example Pb, Cu, Zn, Ni, Cd, and Cr in Beta vulgaris, Phaseolus vulgaris, Spinacea oleracea, and Brassica oleracea [206]; Cr, Pb, Ni, and Zn in maize [186]; Cd, Cu, Cr, Ni, Pb, and Zn in vegetables [188]; Pb and Ni in Beta vulgaris [187]; Cd, Cr, Cu, Ni, Pb, and Zn in the vegetables [189]; and Zn, Cu, Mn, Cd, Pb, Ni, Fe, and Cr in Zea mays [190]. Kiziloglu et al. [207] reported that wastewater irrigation increased the Cu, Fe, Mn, Zn, Pb, Cd, and Ni contents of red cabbage and cauliflower plants. Similarly, the level of Cr, Pb, Ni, and Cd in the edible parts of okra were higher than the safe limit, with levels at 63%, 28%, 90%, and 83% in the samples, respectively [132]. They reported that the irrigation of okra with PTE enriched wastewater is not safe for human use. High concentrations of Cr, Cd, Co, Pb, Cu, Zn, and Ni were reported in spinach, cabbage, radish, and forage grasses when grown on sewage sludge-amended soils [208,209]. Similarly, the wastewater-induced increased accumulation of PTEs by vegetables than the allowable level by EU standards has been reported in Harare-Zimbabwe [205], Bejing-China [20], the industrial zone of Faisalabad-Pakistan [210], Varanasi-India [187], and Peshawar-Pakistan [70].
The soil-plant transfer of PTEs after the irrigation with wastewater depends on several factors relating to the soil, plant, and wastewater. Heavy metals may exist in soil in different forms such as free metal ion or complexed with various organic, inorganic, or soil constituents [204,211]. The soil-plant transfer of PTEs mainly depends on their chemical speciation [212,213,214]. Generally, the PTEs added to soil via wastewater application (anthropogenically) accumulate mainly in the topsoil and are usually have higher mobility and bioavailability compared to those deposited from their parent material [201,215].
The partition of PTEs in the soil and solid phases, as well as their soil-plant transfer after their introduction via wastewater irrigation, depend on soil’s physico-chemical properties (soil mineralogy, cation exchange capacity, pH, and microbial and biological conditions) and the presence of inorganic and organic ligands in the soil [18,27,216,217]. In fact, different soil physico-chemical properties control various soil physico-biochemical processes that govern the fate and behavior of the PTEs in the soils after being introduced by wastewater. For example, Mireles et al. [60] reported a low PTE accumulation in plants, probably due to the physico-chemical properties of the soils that prevent their translocation to plants in the agricultural soils of Mixquiahuala, Hidalgo, and Tláhuac irrigated with wastewater from Mexico City for more than 50 years.
Plant species have a diverse capacity for the accumulation and removal of PTEs from soil [218,219,220]. Certain plant species generally termed as hyper-accumulators can accumulate high levels of PTEs after wastewater irrigation [221,222,223,224]. Overall, hyper-accumulator plant species have the potential to accumulate PTE contents that are 100–1000 times higher compared to non-hyper-accumulating plants [204,218,225,226,227,228]. The edible parts of leafy vegetables grown under wastewater irrigation practice accumulate higher concentrations of PTEs than other vegetables [4]. Therefore, the soil-plant transfer of PTEs in wastewater irrigated soils also depends on the plant type being cultivated in that soil.
After metal uptake, the compartmentation of PTEs in different plant parts (root versus shoot or edible versus non-edible) also varies with the plant and the metal type. Generally, the majority of absorbed metals are stored in the plant root (>90%), with a small portion transferred to the plant shoot [166]. This sequestration of PTEs in the plant roots is due to the presence of endodermis or immobilization by negatively charged pectins within the cell wall (Pourrut et al., 2011). The heavy metal uptake and accumulation in different plant parts play an important role in their health effects [24,26,229,230,231,232]. Depending on the type of the edible part of the vegetable, the increased metal accumulation in the roots and shoots can be useful or toxic. For example, for leafy vegetables, the metal accumulation in the roots is useful, however, for tuber vegetables, a high translocation to its shoots is desired. The degree of the metal contamination also varies with the type of edible plant portion and its presence above or below ground. Generally, the risk of PTE contamination is higher for vegetables having consumable plant parts below the ground than those above the grounds.
Inside the plants, the compartmentation of PTEs in different plant parts is generally controlled by different transporter proteins [233,234,235]. Recent advancements in research at the cellular and genetic level have revealed numerous carrier proteins responsible for the root-shoot translocation of PTEs. These transporter proteins include HMA (heavy metal ATPase) [236,237,238], IRTP (iron-regulated transporter Proteins) [239], ZIP (zinc-regulated transporter Proteins) [240,241], CDF (cation diffusion facilitator) [242,243], and Nramp (natural resistance and macrophage protein) [244]. The expression of these metal carrier proteins is cell and metal specific and they may carry out different roles in different plant species.
Potentially toxic elements may accumulate at high levels in plants after wastewater irrigation. The excessive concentration of PTEs in plant tissue is capable of inducing various physiologically, morphologically, and biochemically toxic effects [18]. The heavy metals induce plant toxicity by disrupting the nutrient and water uptake and transport, altering the nitrogen metabolism, disrupting the activity of ATPase, reducing photosynthesis, interfering with plant growth, dysfunctioning the plant photosynthetic machinery in chloroplasts, and causing stomatal closure [245,246,247,248]. Heavy metals may also cause invisible symptoms of plant injury such as the browning of roots, necrosis, chlorosis, and leaf rolling [249,250,251]. At the cellular level, excessive PTE exposure can cause the enhanced production of reactive oxygen species (ROS), the alteration of cell cycles, and division and chromosomal aberrations [18,159,168,252]. Heavy metals have also been reported to causes protein oxidation, lipid peroxidation, and genotoxicity, most probably via ROS overproduction [216,253].

7.3. The Effect of Wastewater Irrigation on Food Chain Contamination and Human Health

Besides PTEs toxicity to plants, nowadays, food safety has become the most important public concern worldwide. The exposure of urban wastewater is multifaceted. Human health risks due to wastewater crop irrigation include the exposure of consumers and farmers to pathogens including the helminthes infections and inorganic and organic trace elements [4]. Direct exposure happens through the accidental inhalation, ingestion, or dermal contact in different ways: while using wastewater for domestic activities (for example, for dish cleaning or washing clothes), during working processes (for example, while managing the wastewater treatment and emptying the onsite sanitation facilities or reusing the wastewater for irrigation purposes), during flooding actions caused by heavy rains; and due to recreational activities (for example, bathing or swimming in lakes or rivers fed by the wastewater) [254,255,256,257].
Wastewater is discharged commonly into water bodies with little and no treatment due to the limited availability of treatment facilities in many low-income countries [4,10,12]. The release of untreated municipal and industrial wastewater into water bodies (oceans and seas) is a reason for the rapidly growing deoxygenated dead zones. It is estimated that wastewater disposal of water bodies affects about 245,000 km2 of marine ecosystems, as well as fisheries, livelihoods, and food chains [258].
Recent international data indicate that wastewater- and sanitation-related diseases are pervasive and growing alarmingly in countries where untreated wastewater is commonly used for crop irrigation. About 842,000 deaths in 2012 in middle- and low-income countries were linked with sanitation services, contaminated drinking water, and inadequate hand-washing facilities (WHO, 2014b). These diseases were mainly reported among children under 5 years of age [259,260].
Indirect exposure occurs through the use of contaminated drinking water or wastewater-fed fish and crops [261]. In the case of PTEs, humans can be exposed to these toxic compounds via several pathways such as dust inhalation, drinking contaminated water, or via atmospheric inhalation. However, the consumption of food contaminated with PTEs is considered to be the major pathway (>90%) of human exposure to PTEs [20,28,76,195]. Due to increasing the unchecked use of untreated wastewater for crop irrigation in many regions of the world, there is an increased risk of public exposure to the PTEs because of the consumption of food cultivated in sewage wastewater [21,60]. There are numerous studies in the literature supporting this assertion [4,20,21,28,76,186,188,195,196,255].
Clinical studies have revealed that serious systemic health issues can develop as a result of extreme dietary PTE accumulation and are linked with the etiology of a number of diseases, especially nervous system, cardiovascular, blood, and kidney, as well as the bone diseases [25,31,262]. The consumption of PTE contaminated vegetables can cause the depletion of nutrients in the human body that cause many problems in humans such as intrauterine growth retardation, disabilities with malnutrition, impaired psycho-social faculties, upper gastrointestinal cancer, and immunological defenses (Iyengar and Nair, 2000; Wang et al., 2012; Raja et al., 2015). These PTEs (for example, Pb and Cd) are capable of inducing carcinogenesis, teratogenesis, and mutagenesis; high Pb and Cd concentrations in edible plant parts were attributed to the occurrence of upper gastrointestinal cancer [29]. Moreover, Pb is also reported to cause improper hemoglobin synthesis, renal and tumor infection, elevated blood pressure, and the dysfunctioning of the reproductive system [166,245].
PTEs are even capable of inducing toxic effects to living organisms, including human beings, at very low levels due to the absence of proper defense mechanisms to mitigate the toxic effects of these metals and to remove them from the body. Therefore, much attention is given worldwide to food safety and risk assessment. Children and infants, in particular, are more vulnerable to wastewater contaminants [263] and their exposure to these contaminants was referenced in several articles [264].
Legislation regarding the use of wastewater for crop irrigation and associated health risks started in the early 19th century. During that period, wastewater use for crop irrigation in peri-urban fields induced catastrophic epidemics of numerous waterborne syndromes [265,266,267]. These health issues resulted in the establishment of some legislation at the national and international levels such as Great Britain’s Public Health Act, about the “discharge of rainwater in the river and of wastewater on the soil” [3,268].
In order to perform sanitary controls along the borders, the International Office of Public Hygiene was established [269]. The issue of wastewater-borne diseases also led to the development of underground sewage systems in many cities around the globe in the early 1950s [270]. Moreover, the international health and environmental/sanitary movement, generally backed and endorsed by European countries, resulted in a series of sanitary conferences/workshops/seminars on environmentally sustainable development.
Keeping in view the environmental and health risks associated with the use of wastewater disposal/use in the agricultural sector, WHO drafted the guidelines in 1973 on the “Reuse of effluents: methods of wastewater treatment and health safeguards”. These guidelines were later further updated in 1989 and 2006, keeping in view with epidemiological studies [38,271]. The parameters such as health risk assessments have now been included in these updated guidelines.

8. Health Risk Assessment after Food Chain Contamination by Wastewater Irrigation

Estimating the level of exposure of PTEs and tracing their routes of contamination to the target organisms are critical for understanding the health risks involved [25,272]. This is especially important in less developed countries, where the literacy and health risk awareness rates are very low. In low-income countries, many farm workers using wastewater for crop irrigation have been routinely exposed to poor hygiene conditions for most of their lives. Indeed, most of these farmers are either unaware of the risks or may accept these health risks for the benefits of their occupation with no other alternative/resources available as income.
Keeping in view the high volume use of untreated wastewater for crop irrigation and the low literacy rate in low-income countries, there exists a serious health risk of public exposure to PTEs due to the ingestion of vegetables/crops grown in wastewater (Table 5). Several literature studies, especially in low-income countries, support this assertion [21,28,76,195,273]. In order to trace the route and level of exposure to PTEs, a systematic risk assessment is necessary to avoid the possible health hazards and to make timely decisions/policies.
Nowadays, there is an increasing trend in estimating the health risk using soil contamination indices, soil-plant transfer factors, and metal contents in edible plant parts [25,31,274,275]. The most commonly used risk assessment parameters have been summarized in Table 6, which include the degree of contamination (Cdeg), the enrichment factor (EF), bioaccumulation potential (BAP), the uptake/transfer factor, translocation factor (TrF), hazard quotient (HQ), the health risk index (HRI), estimated daily intake (EDI), and lifetime cancer risk (ILTCR) [26,274,276].

9. Future Perspectives

The above-mentioned data show that wastewater crop irrigation has both positive and negative effects. However, by adopting and implementing some precautionary measures and practices, these negative effects of wastewater use can be minimized, making it a safe and reliable source of irrigation.
  • The environmental protection laws and their proper implementation totally differ in developing and developed countries. Generally, the cities in developed countries have well-established and adopted environmentally friendly practices and environmentally sustainable approaches regarding wastewater disposal, treatment, and reuse in the agricultural sector. However, the scenario is very much alarming in developing countries, especially in highly populated areas of the Indo-Pak Sub-continent. In future, more wastewater will be produced/disposed and more environmental and health risks will appear due to the rapid urbanization, industrialization, increase in the world’s population, food demand, economic development, and increase in living standards. Therefore, there will be a need for more systematic approaches in industrial and agricultural sectors to tackle this environmental and health dilemma. At the industrial level, the use of environmental-friendly processes and techniques with minimal use/production of waste material can be highly effective.
  • Similarly, the treatment of industrial wastewater before its discharge is also a key prerequisite to effectively alleviate its negative environmental effects. The proper establishment of wastewater treatment techniques can address the growing demands both in terms of quantity and quality. In the agricultural sector, the development of suitable irrigation approaches can be highly effective for its safe use. It is well-established that environmental contamination can be greatly controlled using a proper irrigation method. For example, drip irrigation has been regarded as the most environmentally friendly approach, which can mitigate up to 70% of environmental risks and leaching rates.
  • Climate change has recently emerged as a key environmental challenge. The uncertainty of this anthropogenic-assisted natural phenomena and irregularity of the environment has to be faced and tacked properly. The scattered pattern of droughts and rainfall over the temporal scale will aggravate water shortages in some areas while flooding other areas. Under such conditions, there will be a need for appropriate techniques and wastewater disposal infrastructure to collect, recycle, and distribute wastewater, protect the soil, and optimize the management.
  • In areas (arid, semi-arid) where fresh water supply is short, the mixing of wastewater with ground or surface water can greatly dilute the PTE concentrations in the applied (mixed) irrigation water. In this way, the risk of PTEs accumulating in soil and crops, as well as the associated health hazards, can be minimized. Similarly, the choice of vegetables/crops (low metal-accumulating species) cultivated using wastewater irrigation can also be a management strategy in areas where farmers have no choice but to use untreated wastewater for crop irrigation.
  • In order to effectively manage this environmental and health issue, there is need to properly implement laws and regulations on wastewater discharge and use in the agricultural sector, especially in less developed countries. The reports show that farmers in less developed countries do not pay enough attention to such laws and regulations, which results in environmental and health issue. Therefore, there is a need for strict regulatory systems, at the local, national, and international level, for effectively managing wastewater irrigation in the agricultural sector. Although abutment data are available regarding the wastewater use for crop irrigation, its effect (both positive and negative) on the soil, on plants, and on humans, there is limited data available with respect to the chemical speciation of the different contaminants (especially PTEs) in wastewater generated from different sectors at different time periods. Similarly, the plant physiological responses (overproduction of reactive oxygen species, lipid peroxidation) and tolerance mechanisms (activation of antioxidative enzymes, production of phytochelatins, glutathione, and so forth) remain unexplored under the wastewater crop irrigation scenario. It is possible that wastewater composition and chemical speciation of a contaminant may greatly vary in different municipal/industrial wastewaters during different seasons (summer and winter). Consequently, the environmental and health risk of that contaminant can vary under these circumstances. Further research work is needed in this regard.

10. Conclusions

Wastewater is used for crop irrigation as an alternative to freshwater. Wastewater collection, disposal, and use in agriculture have a long history. Nowadays, it has become a common practice in many countries around the globe to use wastewater for irrigation. Wastewater crop irrigation represents both opportunities and challenges with respect to its uses and its environmental/health effects. It appears beneficial in terms of a strategy to reuse and manage municipal/industrial water, conserve fertilizer and water, and to achieve certain environmental and social goals. This practice of wastewater crop irrigation has mitigated water deficit crises, to a large extent, especially in arid and semi-arid areas of the world. The nutritional value of wastewater has also been an attraction of its widespread use for crop irrigation. Simultaneously, untreated wastewater irrigation can provoke numerous environmental and human health issues. One of the main issues related to this practice is the build-up of heavy metals in soil, plants, food chains, and ultimately in human beings.
When the environmental and human health issues related to wastewater crop irrigation are assessed globally, there exists a considerable difference between the developed and developing countries. The collection, recycling, and reuse of wastewater in the agricultural sector is better adapted and operated in developed countries compared to the developing world. Social, economic, corporate, and legislative issues are hindering its proper use in the developing world.
Keeping in view the rapid population growth and economic development as well as the uncertainty over climate change, the wastewater use in the agricultural sector may face many challenges. Therefore, the wastewater collection, recycling, and reuse have good prospects in the future, especially in rapidly growing and heavily populated cities, arid and semi-arid areas, and in developing countries. Thus, strategies and techniques for water saving should be methodized on priority. Finally, further scientific research regarding the use of wastewater irrigation is needed for the more effective and sustainable development and adaptation of wastewater irrigation systems, especially in less developed areas.

Author Contributions

M.S. and N.K.N. conceived the idea for this review article; S.K., N., T.S., and A.H.S. prepared draft of paper with N.K.N. and M.S.; I.B. reviewed and edited manuscript; N.K.N. and M.S. reviewed and finalized paper.

Acknowledgments

The authors are highly thankful to the Higher Education Commission (HEC) of Pakistan for funding a research project (Project No. 20-4423/R&D/HEC/14/980). Nabeel Khan Niazi is thankful to the International Foundation for Science (IFS Grant No. W/5698-1) and HEC (Project No. 6425/Punjab/NRPU/R&D/HEC/2016), Pakistan for financial support. Thanks are extended by Irshad Bibi to the Alexander von Humboldt Foundation (Ref 3.5-AK-1164117-GFHERMES-P) for a Postdoctoral Research Fellowship at the University of Bremen, Germany, as well as to HEC, Pakistan (Project No. 6396/Punjab/NRPU/R&D/HEC/2016) for providing financial assistance.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Rijsberman, F.R. Water scarcity: Fact or fiction? Agric. Water Manag. 2006, 80, 5–22. [Google Scholar] [CrossRef]
  2. Zhang, Y.; Shen, Y. Wastewater irrigation: Past, present, and future. Wiley Interdiscip. Rev. Water 2017. [Google Scholar] [CrossRef]
  3. Jaramillo, M.F.; Restrepo, I. Wastewater Reuse in Agriculture: A Review about Its Limitations and Benefits. Sustainability 2017, 9, 1734. [Google Scholar] [CrossRef]
  4. Khalid, S.; Shahid, M.; Dumat, C.; Niazi, N.K.; Bibi, I.; Gul Bakhat, H.F.S.; Abbas, G.; Murtaza, B.; Javeed, H.M.R. Influence of groundwater and wastewater irrigation on lead accumulation in soil and vegetables: Implications for health risk assessment and phytoremediation. Int. J. Phytoremed. 2017, 19, 1037–1046. [Google Scholar] [CrossRef] [PubMed]
  5. Alobaidy, A.H.M.J.; Abid, H.S.; Maulood, B.K. Application of water quality index for assessment of Dokan lake ecosystem, Kurdistan region, Iraq. J. Water Resour. Prot. 2010, 2, 792. [Google Scholar] [CrossRef]
  6. Kalavrouziotis, I. The reuse of Municipal Wastewater in soils. Glob. Nest J. 2015, 17, 474–486. [Google Scholar]
  7. Abaidoo, R.C.; Keraita, B.; Drechsel, P.; Dissanayake, P.; Maxwell, A.S. Soil and crop contamination through wastewater irrigation and options for risk reduction in developing countries. In Soil Biology and Agriculture in the Tropics; Springer: Berlin, Germany, 2010; pp. 275–297. [Google Scholar]
  8. Jiménez, B. Irrigation in developing countries using wastewater. Int. Rev. Environ. Strateg. 2006, 6, 229–250. [Google Scholar]
  9. FAO. AquaStat, Food and Agriculture Organization of the United Nations. 2017. Available online: http://www.fao.org/nr/water/aquastat/data/query/results.html (accessed on 22 January 2018).
  10. Murtaza, G.; Ghafoor, A.; Qadir, M.; Owens, G.; Aziz, M.; Zia, M. Disposal and use of sewage on agricultural lands in Pakistan: A review. Pedosphere 2010, 20, 23–34. [Google Scholar] [CrossRef]
  11. Scott, C.A.; Drechsel, P.; Raschid-Sally, L.; Bahri, A.; Mara, D.; Redwood, M.; Jiménez, B. Wastewater irrigation and health: Challenges and outlook for mitigating risks in low-income countries. In Wastewater Irrigation and Health: Assessing and Mitigating Risk in Low-Income Countries; Earthscan: London, UK, 2010; pp. 381–394. [Google Scholar]
  12. Qadir, M.; Wichelns, D.; Raschid-Sally, L.; McCornick, P.G.; Drechsel, P.; Bahri, A.; Minhas, P. The challenges of wastewater irrigation in developing countries. Agric. Water Manag. 2010, 97, 561–568. [Google Scholar] [CrossRef]
  13. Mark, Y.-A.; Philip, A.; Nelson, A.W.; Muspratt, A.; Aikins, S. Safety assessment on microbial and heavy metal concentration in Clarias gariepinus (African catfish) cultured in treated wastewater pond in Kumasi, Ghana. Environ. Technol. 2017, 1–10. [Google Scholar] [CrossRef] [PubMed]
  14. Azimi, A.; Azari, A.; Rezakazemi, M.; Ansarpour, M. Removal of Heavy Metals from Industrial Wastewaters: A Review. ChemBioEng Rev. 2016, 4, 37–59. [Google Scholar] [CrossRef]
  15. Shahid, M. Biogeochemical Behavior of Heavy Metals in Soil-Plant System; Higher Education Commssion: Islamabad, Pakistan, 2017; pp. 1–196. [Google Scholar]
  16. Li, Q.; Tang, J.; Wang, T.; Wu, D.; Jiao, R.; Ren, X. Impacts of Sewage Irrigation on Soil Properties of Farmland in China: A Review. Yellow River 2017, 4, 5. [Google Scholar] [CrossRef]
  17. Muamar, A.; Zouahri, A.; Tijane, M.; El Housni, A.; Mennane, Z.; Yachou, H.; Bouksaim, M. Evaluation of heavy metals pollution in groundwater, soil and some vegetables irrigated with wastewater in the Skhirat region “Morocco”. J. Mater. Environ. Sci. 2014, 5, 961–966. [Google Scholar]
  18. Shahid, M.; Sabir, M.; Arif Ali, M.; Ghafoor, A. Effect of organic amendments on phytoavailability of nickel and growth of berseem (Trifolium alexandrinum) under nickel contaminated soil conditions. Chem. Speciat. Bioavailab. 2014, 26, 37–42. [Google Scholar] [CrossRef]
  19. Rattan, R.; Datta, S.; Chhonkar, P.; Suribabu, K.; Singh, A. Long-term impact of irrigation with sewage effluents on heavy metal content in soils, crops and groundwater—A case study. Agric. Ecosyst. Environ. 2005, 109, 310–322. [Google Scholar] [CrossRef]
  20. Khan, S.; Cao, Q.; Zheng, Y.; Huang, Y.; Zhu, Y. Health risks of heavy metals in contaminated soils and food crops irrigated with wastewater in Beijing, China. Environ. Pollut. 2008, 152, 686–692. [Google Scholar] [CrossRef] [PubMed]
  21. Singh, A.; Sharma, R.K.; Agrawal, M.; Marshall, F.M. Health risk assessment of heavy metals via dietary intake of foodstuffs from the wastewater irrigated site of a dry tropical area of India. Food Chem. Toxicol. 2010, 48, 611–619. [Google Scholar] [CrossRef] [PubMed]
  22. Khan, S.; Aijun, L.; Zhang, S.; Hu, Q.; Zhu, Y.-G. Accumulation of polycyclic aromatic hydrocarbons and heavy metals in lettuce grown in the soils contaminated with long-term wastewater irrigation. J. Hazard. Mater. 2008, 152, 506–515. [Google Scholar] [CrossRef] [PubMed]
  23. Mapanda, F.; Mangwayana, E.; Nyamangara, J.; Giller, K. The effect of long-term irrigation using wastewater on heavy metal contents of soils under vegetables in Harare, Zimbabwe. Agric. Ecosyst. Environ. 2005, 107, 151–165. [Google Scholar] [CrossRef]
  24. Mombo, S.; Foucault, Y.; Deola, F.; Gaillard, I.; Goix, S.; Shahid, M.; Schreck, E.; Pierart, A.; Dumat, C. Management of human health risk in the context of kitchen gardens polluted by lead and cadmium near a lead recycling company. J. Soils Sediment. 2016, 16, 1214–1224. [Google Scholar] [CrossRef]
  25. Shahid, M.; Khalid, M.; Dumat, C.; Khalid, S.; Niazi, N.K.; Imran, M.; Bibi, I.; Ahmad, I.; Hammad, M.; Tabassum, R.A. Arsenic level and risk assessment of groundwater in Vehari, Punjab Province, Pakistan. Exposure Health 2017. [Google Scholar] [CrossRef]
  26. Xiong, T.; Dumat, C.; Pierart, A.; Shahid, M.; Kang, Y.; Li, N.; Bertoni, G.; Laplanche, C. Measurement of metal bioaccessibility in vegetables to improve human exposure assessments: Field study of soil–plant–atmosphere transfers in urban areas, South China. Environ. Geochem. Health 2016, 38, 1283–1301. [Google Scholar] [CrossRef] [PubMed]
  27. Xiong, T.; Leveque, T.; Shahid, M.; Foucault, Y.; Mombo, S.; Dumat, C. Lead and cadmium phytoavailability and human bioaccessibility for vegetables exposed to soil or atmospheric pollution by process ultrafine particles. J. Environ. Qual. 2014, 43, 1593–1600. [Google Scholar] [CrossRef] [PubMed]
  28. Mahmood, A.; Malik, R.N. Human health risk assessment of heavy metals via consumption of contaminated vegetables collected from different irrigation sources in Lahore, Pakistan. Arab. J. Chem. 2014, 7, 91–99. [Google Scholar] [CrossRef]
  29. Järup, L. Hazards of heavy metal contamination. Br. Med. Bull. 2003, 68, 167–182. [Google Scholar] [CrossRef] [PubMed]
  30. Dumat, C.; Xiong, T.; Shahid, M. Agriculture Urbaine Durable: Opportunité Pour la Transition Écologique; Presses Universitaires Européennes: Saarbrücken, Germany, 2016; pp. 1–88. [Google Scholar]
  31. Shahid, M.; Rafiq, M.; Niazi, N.K.; Dumat, C.; Shamshad, S.; Khalid, S.; Bibi, I. Arsenic accumulation and physiological attributes of spinach in the presence of amendments: An implication to reduce health risk. Environ. Sci. Pollut. Res. 2017, 24, 16097–16106. [Google Scholar] [CrossRef] [PubMed]
  32. Miller-Robbie, L.; Ramaswami, A.; Amerasinghe, P. Wastewater treatment and reuse in urban agriculture: Exploring the food, energy, water, and health nexus in Hyderabad, India. Environ. Res. Lett. 2017, 12, 075005. [Google Scholar] [CrossRef]
  33. Ecosse, D. Techniques Alternatives en vue de Subvenir à la Pénurie D’eau Dans le Monde; Sciences: Amiens, Germany, 2001. [Google Scholar]
  34. Chen, Z.; Ngo, H.H.; Guo, W. A critical review on the end uses of recycled water. Crit. Rev. Environ. Sci. Technol. 2013, 43, 1446–1516. [Google Scholar] [CrossRef]
  35. Aziz, F.; Farissi, M. Reuse of Treated Wastewater in Agriculture: Solving Water Deficit Problems in Arid Areas. Ann. West Univ. Timisoara Ser. Biol. 2014, 17, 95. [Google Scholar]
  36. Winpenny, J.; Heinz, I.; Koo-Oshima, S.; Salgot, M.; Collado, J.; Hernandez, F. The Wealth of Waste; Food and Agriculture Organization of the United Nations (FAO): Roma, Italy, 2010. [Google Scholar]
  37. Thebo, A.L.; Drechsel, P.; Lambin, E.; Nelson, K. A global, spatially-explicit assessment of irrigated croplands influenced by urban wastewater flows. Environ. Res. Lett. 2017, 12, 074008. [Google Scholar] [CrossRef]
  38. World Health Organization. Guidelines for the Safe Use of Wastewater, Excreta and Greywater; World Health Organization: Geneva, Switzerland, 2006; Volume 1. [Google Scholar]
  39. Huibers, F.P.; Moscoso, O.; Durán, A.; van Lier, J.B. Use of wastewate rin agriculture: The water chain approach. Irrig. Drain. 2005, 54, S3–S9. [Google Scholar] [CrossRef]
  40. Martin, P.; Nishida, J.; Afzal, J.; Akbar, S.; Damania, R.; Hanrahan, D. Pakistan Strategic Country Environmental Assessment; World Bank: South Asia Region, 2006; Volume 1. [Google Scholar]
  41. Valipour, M.; Singh, V.P. Global experiences on wastewater irrigation: Challenges and prospects. In Balanced Urban Development: Options and Strategies for Liveable Cities; Springer: Gewerbestrasse, Switzerland, 2016; pp. 289–327. [Google Scholar]
  42. Drechsel, P.; Evans, A.E. Wastewater use in irrigated agriculture. Irrig. Drain. Syst. 2010, 24, 1–3. [Google Scholar] [CrossRef]
  43. Feng, H.; Tan, D.; Lazareva, I. 8 Facts on China’s Wastewater. Available online: http://chinawaterrisk.org/resources/analysis-reviews/8-facts-on-china-wastewater/ (accessed on 30 April 2018).
  44. NPSCB. 1st National Pollutant Source Census Bulletin; China Press: Kuala Lumpur, Malaysia, 2010. [Google Scholar]
  45. Wang, H. A study of the permissible toxicant level in agricultural utilization of sludge. Chin. Environ. Sci. 1983, 3, 56–59. [Google Scholar]
  46. Scott, C.A.; Faruqui, N.I.; Raschid-Sally, L. Wastewater Use in Irrigated Agriculture: Management Challenges in Developing Countries. In Wastewater Use in Irrigated Agriculture: Confronting the Livelihood and Environmental Realities; CABI Publishing: Oxfordshire, UK, 2004. [Google Scholar]
  47. Villalobos, G.; Gamez, G.; Herrera, F. Program for the reuse of wastewater in Mexico. In Municipal Wastewater in Agriculture; Academic Press: New York, NY, USA, 1981; pp. 105–144. [Google Scholar]
  48. Keraita, B.; Drechsel, P. Agricultural use of untreated urban wastewater in Ghana. In Wastewater Use in Irrigated Agriculture: Confrontin the Livelihood and Environmental Realities; CABI Publishing: Oxfordshire, UK, 2004; pp. 101–112. [Google Scholar]
  49. FAO. The United Nations World Water Development Report 2017. Wastewater, The Untapped Resource. Available online: www.unwater.org/publications/world-water-development-report-2017/ (accessed on 30 April 2018).
  50. MOHURD, Ministry of Housing and Urban-Rural Development of the People’s Republic of China. 2017. Available online: https://translate.google.com.pk/translate?hl=en&sl=zh-CN&u=http://www.mohurd.gov.cn/&prev=search (accessed on 30 April 2018).
  51. Kaur, R.; Wani, S.; Singh, A.; Lal, K. Wastewater Production, Treatment and Use in India. Presented at the 2nd Regional workshop on Safe Use of Wastewater in Agriculture, New Delhi, India, 16–18 May 2012. [Google Scholar]
  52. Ensink, J.H.; Mahmood, T.; van der Hoek, W.; Raschid-Sally, L.; Amerasinghe, F.P. A nationwide assessment of wastewater use in Pakistan: An obscure activity or a vitally important one? Water Policy 2004, 6, 197–206. [Google Scholar]
  53. Minhas, P.; Samra, J. Quality Assessment of Water Resources in the Indo-Gangetic Basin Part in India; Central Soil Salinity Research Inst.: Karnal, India, 2003. [Google Scholar]
  54. Drechsel, P.; Graefe, S.; Sonou, M.; Cofie, O.O. Informal Irrigation in Urban West Africa: An Overview; International Water Management Institute (IWMI): Colombo, Sri Lanka, 2006; Volume 102. [Google Scholar]
  55. Bokhari, S.H.; Mahmood-ul-Hassan, M.; Riaz, Y.; Munir, A.; Ali, Z. Baseline water quality of municipal ponds and metal removal ability of Typha latifolia L. from sewage and industrial wastewaters. Int. J. Phytoremediat. 2017, 19, 1077–1084. [Google Scholar] [CrossRef] [PubMed]
  56. Ensink, J.H.; Simmons, R.; van der Hoek, W. Wastewater use in Pakistan: The cases of Haroonabad and Faisalabad. In Wastewater use in Irrigated Agriculture: Confronting the Livelihood and Environmental Realities; CABI Publishing: Oxfordshire, UK, 2004; pp. 91–99. [Google Scholar]
  57. Morugán-Coronado, A.; García-Orenes, F.; Mataix-Solera, J.; Arcenegui, V.; Mataix-Beneyto, J. Short-term effects of treated wastewater irrigation on Mediterranean calcareous soil. Soil Tillage Res. 2011, 112, 18–26. [Google Scholar] [CrossRef]
  58. Shahid, M.; Khalid, S.; Abbas, G.; Shahid, N.; Nadeem, M.; Sabir, M.; Aslam, M.; Dumat, C. Heavy metal stress and crop productivity. In Crop Production and Global Environmental Issues; Springer: Berlin, Germany, 2015; pp. 1–25. [Google Scholar]
  59. Uyttendaele, M.; Jaykus, L.A.; Amoah, P.; Chiodini, A.; Cunliffe, D.; Jacxsens, L.; Holvoet, K.; Korsten, L.; Lau, M.; McClure, P. Microbial hazards in irrigation water: Standards, norms, and testing to manage use of water in fresh produce primary production. Compr. Rev. Food Sci. Food Saf. 2015, 14, 336–356. [Google Scholar] [CrossRef]
  60. Mireles, A.; Solís, C.; Andrade, E.; Lagunas-Solar, M.; Piña, C.; Flocchini, R.G. Heavy metal accumulation in plants and soil irrigated with wastewater from Mexico city. Nucl. Instrum. Methods Phys. Res. Sect. B Beam Interact. Mater. Atoms 2004, 219–220, 187–190. [Google Scholar] [CrossRef]
  61. Urbano, V.R.; Mendonça, T.G.; Bastos, R.G.; Souza, C.F. Effects of treated wastewater irrigation on soil properties and lettuce yield. Agric. Water Manag. 2017, 181, 108–115. [Google Scholar] [CrossRef]
  62. Alghobar, M.A.; Suresha, S. Effect of wastewater irrigation on growth and yield of rice crop and uptake and accumulation of nutrient and heavy metals in soil. Appl. Ecol. Environ. Sci. 2016, 4, 53–60. [Google Scholar]
  63. Lal, K.; Kaur, R.; Rosin, K.; Patel, N. Low-Cost Remediation and On-Farm Management Approaches for Safe Use of Wastewater in Agriculture. In Innovative Saline Agriculture; Springer: Berlin, Germany, 2016; pp. 265–275. [Google Scholar]
  64. Nafchi, R.A. Evaluation of Wastewater Quality Compared to Well Water in Irrigation. Ecology 2017, 7, 271–278. [Google Scholar] [CrossRef]
  65. Gassama, U.M.; Puteh, A.B.; Abd-Halim, M.R.; Kargbo, B. Influence of municipal wastewater on rice seed germination, seedling performance, nutrient uptake, and chlorophyll content. J. Crop Sci. Biotechnol. 2015, 18, 9–19. [Google Scholar] [CrossRef]
  66. Galal, T.M.; Shehata, H.S. Impact of nutrients and heavy metals capture by weeds on the growth and production of rice (Oryza sativa L.) irrigated with different water sources. Ecol. Indic. 2015, 54, 108–115. [Google Scholar] [CrossRef]
  67. Begum, R.; Zaman, M.; Mondol, A.; Islam, M.; Hossain, M. Effects of textile industrial waste water and uptake of nutrients on the yield of rice. Bangladesh J. Agric. Res. 2011, 36, 319–331. [Google Scholar] [CrossRef]
  68. Khan, M.J.; Jan, M.T.; Farhatullah, N.; Khan, M.A.; Perveen, S.; Alam, S.; Jan, A.U. The effect of using waste water for tomato. Pak. J. Bot. 2011, 43, 1033–1044. [Google Scholar]
  69. Abdoulkader, B.A.; Mohamed, B.; Nabil, M.; Alaoui-Sossé, B.; Eric, C.; Aleya, L. Wastewater use in agriculture in Djibouti: Effectiveness of sand filtration treatments and impact of wastewater irrigation on growth and yield of Panicum maximum. Ecol. Eng. 2015, 84, 607–614. [Google Scholar] [CrossRef]
  70. Amin, N.-U.; Ahmad, T. Contamination of soil with heavy metals from industrial effluent and their translocation in green vegetables of Peshawar, Pakistan. RSC Adv. 2015, 5, 14322–14329. [Google Scholar] [CrossRef]
  71. Khan, A.; Khan, S.; Khan, M.A.; Qamar, Z.; Waqas, M. The uptake and bioaccumulation of heavy metals by food plants, their effects on plants nutrients, and associated health risk: A review. Environ. Sci. Pollut. Res. 2015, 22, 13772–13799. [Google Scholar] [CrossRef] [PubMed]
  72. Farahat, E.; Linderholm, H.W. The effect of long-term wastewater irrigation on accumulation and transfer of heavy metals in Cupressus sempervirens leaves and adjacent soils. Sci. Total Environ. 2015, 512, 1–7. [Google Scholar] [CrossRef] [PubMed]
  73. Hussain, A.; Alamzeb, S.; Begum, S. Accumulation of heavy metals in edible parts of vegetables irrigated with waste water and their daily intake to adults and children, District Mardan, Pakistan. Food Chem. 2013, 136, 1515–1523. [Google Scholar]
  74. Shilpi, S.; Seshadri, B.; Sarkar, B.; Bolan, N.; Lamb, D.; Naidu, R. Comparative values of various wastewater streams as a soil nutrient source. Chemosphere 2018, 192, 272–281. [Google Scholar] [CrossRef] [PubMed]
  75. Gupta, N.; Khan, D.; Santra, S. Heavy metal accumulation in vegetables grown in a long-term wastewater-irrigated agricultural land of tropical India. Environ. Monit. Assess. 2012, 184, 6673–6682. [Google Scholar] [CrossRef] [PubMed]
  76. Khan, M.U.; Malik, R.N.; Muhammad, S. Human health risk from heavy metal via food crops consumption with wastewater irrigation practices in Pakistan. Chemosphere 2013, 93, 2230–2238. [Google Scholar] [CrossRef] [PubMed]
  77. El-Nahhal, Y.; Tubail, K.; Safi, M.; Safi, J. Effect of treated waste water irrigation on plant growth and soil properties in Gaza Strip, Palestine. Am. J. Plant Sci. 2013, 4, 1736–1743. [Google Scholar] [CrossRef]
  78. Zavadil, J. The effect of municipal wastewater irrigation on the yield and quality of vegetables and crops. Soil Water Res. 2009, 4, 91–103. [Google Scholar] [CrossRef]
  79. Tiwari, K.; Singh, N.; Patel, M.; Tiwari, M.; Rai, U. Metal contamination of soil and translocation in vegetables growing under industrial wastewater irrigated agricultural field of Vadodara, Gujarat, India. Ecotoxicol. Environ. Saf. 2011, 74, 1670–1677. [Google Scholar] [CrossRef] [PubMed]
  80. Becerra-Castro, C.; Lopes, A.R.; Vaz-Moreira, I.; Silva, E.F.; Manaia, C.M.; Nunes, O.C. Wastewater reuse in irrigation: A microbiological perspective on implications in soil fertility and human and environmental health. Environ. Int. 2015, 75, 117–135. [Google Scholar] [CrossRef] [PubMed]
  81. Shahid, M.; Pinelli, E.; Dumat, C. Review of Pb availability and toxicity to plants in relation with metal speciation; role of synthetic and natural organic ligands. J. Hazard. Mater. 2012, 219, 1–12. [Google Scholar] [CrossRef] [PubMed]
  82. Shahid, M.; Pinelli, E.; Dumat, C. Tracing trends in plant physiology and biochemistry: Need of databases from genetic to kingdom level. Plant Physiol. Biochem. 2018. [Google Scholar] [CrossRef]
  83. Shahid, M.; Niazi, N.K.; Khalid, S.; Murtaza, B.; Bibi, I.; Rashid, M.I. A critical review of selenium biogeochemical behavior in soil-plant system with an inference to human health. Environ. Pollut. 2018, 234, 915–934. [Google Scholar]
  84. Kunhikrishnan, A.; Bolan, N.S.; Müller, K.; Laurenson, S.; Naidu, R.; Kim, W.-I. The influence of wastewater irrigation on the transformation and bioavailability of heavy metal (loid) s in soil. Adv. Agron. 2012, 115, 215. [Google Scholar]
  85. Vaseghi, S.; Afyouni, M.; Shariat Madari, H.; Mobli, M. Effect of sewage sludge on same macronutrients concentration and soil chemical properties. J. Water Wastewater 2005, 53, 18–25. [Google Scholar]
  86. Khai, N.M.; Öborn, I.; Hillier, S.; Gustafsson, J.P. Modeling of metal binding in tropical Fluvisols and Acrisols treated with biosolids and wastewater. Chemosphere 2008, 70, 1338–1346. [Google Scholar] [CrossRef] [PubMed]
  87. Hassanli, A.M.; Javan, M.; Saadat, Y. Reuse of municipal effluent with drip irrigation and evaluation the effect on soil properties in a semi-arid area. Environ. Monit. Assess. 2008, 144, 151–158. [Google Scholar] [CrossRef] [PubMed]
  88. Walker, C.; Lin, H. Soil property changes after four decades of wastewater irrigation: A landscape perspective. Catena 2008, 73, 63–74. [Google Scholar] [CrossRef]
  89. Christou, A.; Eliadou, E.; Michael, C.; Hapeshi, E.; Fatta-Kassinos, D. Assessment of long-term wastewater irrigation impacts on the soil geochemical properties and the bioaccumulation of heavy metals to the agricultural products. Environ. Monit. Assess. 2014, 186, 4857–4870. [Google Scholar] [CrossRef] [PubMed]
  90. Rabie Ahmed Usman, A.; Ghallab, A. Heavy-metal fractionation and distribution in soil profiles short-term-irrigated with sewage wastewater. Chem. Ecol. 2006, 22, 267–278. [Google Scholar] [CrossRef]
  91. Thapliyal, A.; Vasudevan, P.; Dastidar, M.; Tandon, M.; Mishra, S. Irrigation with domestic wastewater: Responses on growth and yield of ladyfinger Abelmoschus esculentus and on soil nutrients. J. Environ. Biol. 2011, 32, 645. [Google Scholar] [PubMed]
  92. Galal, H.A. Long-term Effect of Mixed Wastewater Irrigation on Soil Properties, Fruit Quality and Heavy Metal Contamination of Citrus. Am. J. Environ. Prot. 2015, 3, 100–105. [Google Scholar]
  93. Mulidzi, A.R. The Effect of Winery Wastewater Irrigation on the Properties of Selected Soils from the South African Wine Region. Ph.D. Thesis, Stellenbosch University, Stellenbosch, South Africa, 2016. [Google Scholar]
  94. Abegunrin, T.; Awe, G.; Idowu, D.; Onigbogi, O.; Onofua, O. Effect of kitchen wastewater irrigation on soil properties and growth of cucumber (Cucumis sativus). J. Soil Sci. Environ. Manag. 2013, 4, 139–145. [Google Scholar] [CrossRef]
  95. De Oliveira, P.C.P.; Gloaguen, T.V.; Gonçalves, R.A.B.; Santos, D.L.; Couto, C.F. Soil Chemistry after Irrigation with Treated Wastewater in Semiarid Climate. Rev. Bras. Ciênc. Solo 2016, 40. [Google Scholar] [CrossRef]
  96. Muamar, A.-J.; Tijane, M.H.; Shawqi, E.-A.; El Housni, A.; Zouahri, A.; Bouksaim, M. Assessment of the Impact of Wastewater Use on Soil Properties. J. Mater. Environ. Sci. 2014, 5, 747–752. [Google Scholar]
  97. Xue, Y.; Yang, P.; Ren, S.; Li, Y.; Su, Y. Effects of Municipal Reclaimed Wastewater Irrigation on Soil Biochemical Properties. In Proceedings of the 2010 4th International Conference on Bioinformatics and Biomedical Engineering (iCBBE), Chengdu, China, 18–20 June 2010; pp. 1–4. [Google Scholar]
  98. Mojiri, A. Effects of municipal wastewater on physical and chemical properties of saline soil. J. Biol. Environ. Sci. 2011, 5, 71–76. [Google Scholar]
  99. Shahid, M.; Dumat, C.; Silvestre, J.; Pinelli, E. Effect of fulvic acids on lead-induced oxidative stress to metal sensitive Vicia faba L. plant. Biol. Fertil. Soils 2012, 48, 689–697. [Google Scholar] [CrossRef] [Green Version]
  100. Mehmood, T.; Bibi, I.; Shahid, M.; Niazi, N.K.; Murtaza, B.; Wang, H.; Ok, Y.S.; Sarkar, B.; Javed, M.T.; Murtaza, G. Effect of compost addition on arsenic uptake, morphological and physiological attributes of maize plants grown in contrasting soils. J. Geochem. Explor. 2017, 178, 83–91. [Google Scholar] [CrossRef]
  101. Huang, Z.; Lu, Q.; Wang, J.; Chen, X.; Mao, X.; He, Z. Inhibition of the bioavailability of heavy metals in sewage sludge biochar by adding two stabilizers. PLoS ONE 2017, 12, e0183617. [Google Scholar] [CrossRef] [PubMed]
  102. Shahid, M.; Shamshad, S.; Rafiq, M.; Khalid, S.; Bibi, I.; Niazi, N.K.; Dumat, C.; Rashid, M.I. Chromium speciation, bioavailability, uptake, toxicity and detoxification in soil-plant system: A review. Chemosphere 2017, 178, 513–533. [Google Scholar] [CrossRef] [PubMed]
  103. Linkhorst, A.; Dittmar, T.; Waska, H. Molecular Fractionation of Dissolved Organic Matter in a Shallow Subterranean Estuary: The Role of the Iron Curtain. Environ. Sci. Technol. 2017, 51, 1312–1320. [Google Scholar] [CrossRef] [PubMed]
  104. Lori, M.; Symnaczik, S.; Mäder, P.; De Deyn, G.; Gattinger, A. Organic farming enhances soil microbial abundance and activity—A meta-analysis and meta-regression. PLoS ONE 2017, 12, e0180442. [Google Scholar] [CrossRef] [PubMed]
  105. Błońska, E.; Lasota, J.; Gruba, P. Enzymatic activity and stabilization of organic matter in soil with different detritus inputs. Soil Sci. Plant Nutr. 2017, 63, 242–247. [Google Scholar]
  106. Chahal, S.S.; Choudhary, O.P.; Mavi, M.S. Organic amendments decomposability influences microbial activity in saline soils. Arch. Agron. Soil Sci. 2017, 63, 1875–1888. [Google Scholar] [CrossRef]
  107. Bedbabis, S.; Rouina, B.B.; Boukhris, M.; Ferrara, G. Effect of irrigation with treated wastewater on soil chemical properties and infiltration rate. J. Environ. Manag. 2014, 133, 45–50. [Google Scholar] [CrossRef] [PubMed]
  108. Qadir, M.; Scott, C.A. Non-pathogenic trade-offs of wastewater irrigation. In Wastewater Irrigation and Health Assessing and Mitigating Risk in Low-Income Countries; IWMI: Colombo, SriLanka, 2010; pp. 101–126. [Google Scholar]
  109. Sou, M.Y.; Mermoud, A.; Yacouba, H.; Boivin, P. Impacts of irrigation with industrial treated wastewater on soil properties. Geoderma 2013, 200, 31–39. [Google Scholar]
  110. Almeida, I.C.C.; Fernandes, R.B.A.; Neves, J.C.L.; Ruiz, H.A.; Lima, T.L.B.D.; Hoogmoed, W. Soil Quality after Six Years of Paper Mill Industrial Wastewater Application. Rev. Bras. Ciênc. Solo 2017, 41. [Google Scholar] [CrossRef]
  111. Silva, L.V.; de Lima, V.L.; Pearson, H.W.; Silva, T.T.; Maciel, C.L.; Sofiatti, V. Chemical properties of a Haplustalf soil under irrigation with treated wastewater and nitrogen fertilization. Rev. Bras. Eng. Agrícola Ambient. 2016, 20, 308–315. [Google Scholar] [CrossRef]
  112. Tabatabaei, S.H.; Najafi, P.; Amini, H. Assessment of change in soil water content properties irrigated with industrial sugar beet wastewater. Pak. J. Biol. Sci. PJBS 2007, 10, 1649–1654. [Google Scholar] [PubMed]
  113. Connor, R.; Renata, A.; Ortigara, C.; Koncagül, E.; Uhlenbrook, S.; Lamizana-Diallo, B.M.; Zadeh, S.M.; Qadir, M.; Kjellén, M.; Sjödin, J. The United Nations World Water Development Report 2017; The Untapped Resource: Paris, France, 2017. [Google Scholar]
  114. Alghobar, M.A.; Suresha, S. Evaluation of Nutrients and Trace Metals and Their Enrichment Factors in Soil and Sugarcane Crop Irrigated with Wastewater. J. Geosci. Environ. Prot. 2015, 3, 46. [Google Scholar] [CrossRef]
  115. Blok, C.; Jackson, B.E.; Guo, X.; De Visser, P.H.; Marcelis, L.F. Maximum Plant Uptakes for Water, Nutrients, and Oxygen Are Not Always Met by Irrigation Rate and Distribution in Water-based Cultivation Systems. Front. Plant Sci. 2017, 8, 562. [Google Scholar] [CrossRef] [PubMed]
  116. Rusan, M.J.M.; Hinnawi, S.; Rousan, L. Long term effect of wastewater irrigation of forage crops on soil and plant quality parameters. Desalination 2007, 215, 143–152. [Google Scholar] [CrossRef]
  117. Christen, E.; Quayle, W.; Marcoux, M.; Arienzo, M.; Jayawardane, N. Winery wastewater treatment using the land filter technique. J. Environ. Manag. 2010, 91, 1665–1673. [Google Scholar] [CrossRef] [PubMed]
  118. Mosse, K.; Patti, A.; Christen, E.; Cavagnaro, T. Winery wastewater quality and treatment options in Australia. Aust. J. Grape Wine Res. 2011, 17, 111–122. [Google Scholar] [CrossRef]
  119. Reich, M.; Aghajanzadeh, T.; Helm, J.; Parmar, S.; Hawkesford, M.J.; De Kok, L.J. Chloride and sulfate salinity differently affect biomass, mineral nutrient composition and expression of sulfate transport and assimilation genes in Brassica rapa. Plant Soil 2017, 411, 319–332. [Google Scholar] [CrossRef]
  120. Sadaf, J.; Shah, G.A.; Shahzad, K.; Ali, N.; Shahid, M.; Ali, S.; Hussain, R.A.; Ahmed, Z.I.; Traore, B.; Ismail, I.M. Improvements in wheat productivity and soil quality can accomplish by co-application of biochars and chemical fertilizers. Sci. Total Environ. 2017, 607, 715–724. [Google Scholar] [CrossRef] [PubMed]
  121. Balkhair, K.S.; El-Nakhlawi, F.S.; Ismail, S.M.; Al-Solimani, S.G. Treated wastewater use and its effect on water conservation, vegetative yeild, yield components and water use efficiency of some vegetable crops grown under two different irrigation systems in western region, Saudi Arabia. Eur. Sci. J. ESJ 2013, 9. [Google Scholar]
  122. Davidson, E.A. The contribution of manure and fertilizer nitrogen to atmospheric nitrous oxide since 1860. Nat. Geosci. 2009, 2, 659–662. [Google Scholar] [CrossRef]
  123. Tubiello, F.N.; Salvatore, M.; Rossi, S.; Ferrara, A.; Fitton, N.; Smith, P. The FAOSTAT database of greenhouse gas emissions from agriculture. Environ. Res. Lett. 2013, 8, 015009. [Google Scholar] [CrossRef]
  124. Vergé, X.; Dyer, J.; Desjardins, R.; Worth, D. Greenhouse gas emissions from the Canadian dairy industry in 2001. Agric. Syst. 2007, 94, 683–693. [Google Scholar] [CrossRef]
  125. Gatta, G.; Libutti, A.; Gagliardi, A.; Beneduce, L.; Brusetti, L.; Borruso, L.; Disciglio, G.; Tarantino, E. Treated agro-industrial wastewater irrigation of tomato crop: Effects on qualitative/quantitative characteristics of production and microbiological properties of the soil. Agric. Water Manag. 2015, 149, 33–43. [Google Scholar] [CrossRef]
  126. Gatta, G.; Libutti, A.; Gagliardi, A.; Disciglio, G.; Beneduce, L.; d’Antuono, M.; Rendina, M.; Tarantino, E. Effects of treated agro-industrial wastewater irrigation on tomato processing quality. Ital. J. Agron. 2015, 10, 97–100. [Google Scholar] [CrossRef]
  127. Aghtape, A.A.; Ghanbari, A.; Sirousmehr, A.; Siahsar, B.; Asgharipour, M.; Tavssoli, A. Effect of irrigation with wastewater and foliar fertilizer application on some forage characteristics of foxtail millet (Setaria italica). Int. J. Plant Physiol. Biochem. 2011, 3, 34–42. [Google Scholar]
  128. Li, W.; Li, Z. In situ nutrient removal from aquaculture wastewater by aquatic vegetable Ipomoea aquatica on floating beds. Water Sci. Technol. 2009, 59, 1937–1943. [Google Scholar] [CrossRef] [PubMed]
  129. Cirelli, G.; Consoli, S.; Licciardello, F.; Aiello, R.; Giuffrida, F.; Leonardi, C. Treated municipal wastewater reuse in vegetable production. Agric. Water Manag. 2012, 104, 163–170. [Google Scholar] [CrossRef]
  130. Al-Rashidi, R.; Rusan, M.; Obaid, K. Changes in plant nutrients, and microbial biomass in different soil depths after long-term surface application of secondary treated wastewater. Sci. J. Riga Tech. Univ. Environ. Clim. Technol. 2013, 11, 28–33. [Google Scholar] [CrossRef]
  131. Najafi, P.; Shams, J.; Shams, A. The effects of irrigation methods on some of soil and plant microbial indices using treated municipal wastewater. Int. J. Recycl. Organ. Waste Agric. 2015, 4, 63–65. [Google Scholar] [CrossRef]
  132. Balkhair, K.S.; Ashraf, M.A. Field accumulation risks of heavy metals in soil and vegetable crop irrigated with sewage water in western region of Saudi Arabia. Saudi J. Biol. Sci. 2016, 23, S32–S44. [Google Scholar] [CrossRef] [PubMed]
  133. Williams, J.; Dimbu, P. Research Article Effect of Abbatoir Waste Water on Soil Microbial Communities. Sch. Acad. J. Biosci. 2015, 5, 452–455. [Google Scholar]
  134. Adesemoye, A.; Opere, B.; Makinde, S. Microbial content of abattoir wastewater and its contaminated soil in Lagos, Nigeria. African J. Biotechnol. 2006, 5, 1963–1968. [Google Scholar]
  135. Disciglio, G.; Gatta, G.; Libutti, A.; Gagliardi, A.; Carlucci, A.; Lops, F.; Cibelli, F.; Tarantino, A. Effects of irrigation with treated agro-industrial wastewater on soil chemical characteristics and fungal populations during processing tomato crop cycle. J. Soil Sci. Plant Nutr. 2015, 15, 765–780. [Google Scholar]
  136. Ahemad, M.; Malik, A. Bioaccumulation of heavy metals by zinc resistant bacteria isolated from agricultural soils irrigated with wastewater. Bacteriol. J. 2011, 2, 12–21. [Google Scholar] [CrossRef]
  137. De-lan, X.; Cui-ying, Z.; Shu-ming, Q.; Xu, M.; Ming-xia, G. Characterization of microorganisms in the soils with sewage irrigations. African J. Microbiol. Res. 2013, 6, 7168–7175. [Google Scholar]
  138. Malkawi, H.I.; Mohammad, M.J. Survival and accumulation of microorganisms in soils irrigated with secondary treated wastewater. J. Basic Microbiol. 2003, 43, 47–55. [Google Scholar] [CrossRef] [PubMed]
  139. Ibekwe, A.; Gonzalez-Rubio, A.; Suarez, D. Impact of treated wastewater for irrigation on soil microbial communities. Sci. Total Environ. 2017, 622–623, 1603–1610. [Google Scholar] [CrossRef] [PubMed]
  140. Oliveira, A.; Pampulha, M.E. Effects of long-term heavy metal contamination on soil microbial characteristics. J. Biosci. Bioeng. 2006, 102, 157–161. [Google Scholar] [CrossRef] [PubMed]
  141. Saadi, I.; Laor, Y.; Raviv, M.; Medina, S. Land spreading of olive mill wastewater: Effects on soil microbial activity and potential phytotoxicity. Chemosphere 2007, 66, 75–83. [Google Scholar] [CrossRef] [PubMed]
  142. Del Mar Alguacil, M.; Torrecillas, E.; Torres, P.; García-Orenes, F.; Roldán, A. Long-term effects of irrigation with waste water on soil AM fungi diversity and microbial activities: The implications for agro-ecosystem resilience. PLoS ONE 2012, 7, e47680. [Google Scholar] [CrossRef] [PubMed]
  143. Mechri, B.; Mariem, F.B.; Baham, M.; Elhadj, S.B.; Hammami, M. Change in soil properties and the soil microbial community following land spreading of olive mill wastewater affects olive trees key physiological parameters and the abundance of arbuscular mycorrhizal fungi. Soil Biol. Biochem. 2008, 40, 152–161. [Google Scholar] [CrossRef]
  144. Mechri, B.; Chehab, H.; Attia, F.; Mariem, F.; Braham, M.; Hammami, M. Olive mill wastewater effects on the microbial communities as studied in the field of olive trees by analysis of fatty acid signatures. Eur. J. Soil Biol. 2010, 46, 312–318. [Google Scholar] [CrossRef]
  145. Covarrubias, S.A.; de-Bashan, L.E.; Moreno, M.; Bashan, Y. Alginate beads provide a beneficial physical barrier against native microorganisms in wastewater treated with immobilized bacteria and microalgae. Appl. Microbiol. Biotechnol. 2012, 93, 2669–2680. [Google Scholar] [CrossRef] [PubMed]
  146. Daims, H.; Nielsen, J.L.; Nielsen, P.H.; Schleifer, K.-H.; Wagner, M. In Situ Characterization ofNitrospira-Like Nitrite-Oxidizing Bacteria Active in Wastewater Treatment Plants. Appl. Environ. Microbiol. 2001, 67, 5273–5284. [Google Scholar] [CrossRef] [PubMed]
  147. Hanjra, M.A.; Blackwell, J.; Carr, G.; Zhang, F.; Jackson, T.M. Wastewater irrigation and environmental health: Implications for water governance and public policy. Int. J. Hyg. Environ. Health 2012, 215, 255–269. [Google Scholar] [CrossRef] [PubMed]
  148. Duran, N.; Esposito, E. Potential applications of oxidative enzymes and phenoloxidase-like compounds in wastewater and soil treatment: A review. Appl. Catal. B Environ. 2000, 28, 83–99. [Google Scholar] [CrossRef]
  149. Chen, W.; Wu, L.; Frankenberger, W.T.; Chang, A.C. Soil enzyme activities of long-term reclaimed wastewater-irrigated soils. J. Environ. Qual. 2008, 37 (Suppl. S5), S36–S42. [Google Scholar] [CrossRef] [PubMed]
  150. Meli, S.; Porto, M.; Belligno, A.; Bufo, S.A.; Mazzatura, A.; Scopa, A. Influence of irrigation with lagooned urban wastewater on chemical and microbiological soil parameters in a citrus orchard under Mediterranean condition. Sci. Total Environ. 2002, 285, 69–77. [Google Scholar] [CrossRef]
  151. Ma, S.-C.; Zhang, H.-B.; Ma, S.-T.; Wang, R.; Wang, G.-X.; Shao, Y.; Li, C.-X. Effects of mine wastewater irrigation on activities of soil enzymes and physiological properties, heavy metal uptake and grain yield in winter wheat. Ecotoxicol. Environ. Saf. 2015, 113, 483–490. [Google Scholar] [CrossRef] [PubMed]
  152. Frenk, S.; Hadar, Y.; Minz, D. Resilience of soil bacterial community to irrigation with water of different qualities under Mediterranean climate. Environ. Microbiol. 2014, 16, 559–569. [Google Scholar] [CrossRef] [PubMed]
  153. Niazi, N.K.; Bibi, I.; Shahid, M.; Ok, Y.S.; Burton, E.D.; Wang, H.; Shaheen, S.M.; Rinklebe, J.; Lüttge, A. Arsenic removal by perilla leaf biochar in aqueous solutions and groundwater: An integrated spectroscopic and microscopic examination. Environ. Pollut. 2018, 232, 31–41. [Google Scholar] [CrossRef] [PubMed]
  154. Niazi, N.K.; Bibi, I.; Shahid, M.; Ok, Y.S.; Shaheen, S.M.; Rinklebe, J.; Wang, H.; Murtaza, B.; Islam, E.; Nawaz, M.F. Arsenic removal by Japanese oak wood biochar in aqueous solutions and well water: Investigating arsenic fate using integrated spectroscopic and microscopic techniques. Sci. Total Environ. 2017, 621, 1642–1651. [Google Scholar] [CrossRef] [PubMed]
  155. Shakoor, M.B.; Bibi, I.; Niazi, N.K.; Shahid, M.; Nawaz, M.F.; Farooqi, A.; Naidu, R.; Rahman, M.M.; Murtaza, G.; Lüttge, A. The evaluation of arsenic contamination potential, speciation and hydrogeochemical behaviour in aquifers of Punjab, Pakistan. Chemosphere 2018, 199, 737–746. [Google Scholar] [CrossRef] [PubMed]
  156. Shakoor, M.B.; Niazi, N.K.; Bibi, I.; Murtaza, G.; Kunhikrishnan, A.; Seshadri, B.; Shahid, M.; Ali, S.; Bolan, N.S.; Ok, Y.S. Remediation of arsenic-contaminated water using agricultural wastes as biosorbents. Crit. Rev. Environ. Sci. Technol. 2016, 46, 467–499. [Google Scholar] [CrossRef]
  157. Tabassum, R.A.; Shahid, M.; Dumat, C.; Niazi, N.K.; Khalid, S.; Shah, N.S.; Imran, M.; Khalid, S. Health risk assessment of drinking arsenic-containing groundwater in Hasilpur, Pakistan: Effect of sampling area, depth, and source. Environ. Sci. Pollut. Res. 2018. [Google Scholar] [CrossRef] [PubMed]
  158. Shahid, N.; Zia, Z.; Shahid, M.; Faiq Bakhat, H.; Anwar, S.; Mustafa Shah, G.; Rizwan Ashraf, M. Assessing Drinking Water Quality in Punjab, Pakistan. Pol. J. Environ. Stud. 2015, 24, 2597–2606. [Google Scholar] [CrossRef]
  159. Shahid, M.; Pourrut, B.; Dumat, C.; Nadeem, M.; Aslam, M.; Pinelli, E. Heavy-metal-induced reactive oxygen species: Phytotoxicity and physicochemical changes in plants. In Reviews of Environmental Contamination and Toxicology; Springer: Berlin, Germany, 2014; Volume 232, pp. 1–44. [Google Scholar]
  160. Zia, Z.; Bakhat, H.F.; Saqib, Z.A.; Shah, G.M.; Fahad, S.; Ashraf, M.R.; Hammad, H.M.; Naseem, W.; Shahid, M. Effect of water management and silicon on germination, growth, phosphorus and arsenic uptake in rice. Ecotoxicol. Environ. Saf. 2017, 144, 11–18. [Google Scholar] [CrossRef] [PubMed]
  161. Woldetsadik, D.; Drechsel, P.; Keraita, B.; Itanna, F.; Gebrekidan, H. Heavy metal accumulation and health risk assessment in wastewater-irrigated urban vegetable farming sites of Addis Ababa, Ethiopia. Int. J. Food Contam. 2017, 4, 9. [Google Scholar] [CrossRef]
  162. Mekki, A.; Sayadi, S. Study of heavy metal accumulation and residual toxicity in soil saturated with phosphate processing wastewater. Water Air Soil Pollut. 2017, 228, 215. [Google Scholar] [CrossRef] [PubMed]
  163. Xu, J.; Wu, L.; Chang, A.C.; Zhang, Y. Impact of long-term reclaimed wastewater irrigation on agricultural soils: A preliminary assessment. J. Hazard. Mater. 2010, 183, 780–786. [Google Scholar] [CrossRef] [PubMed]
  164. Silveira, M.L.A.; Alleoni, L.R.F.; Guilherme, L.R.G. Biosolids and heavy metals in soils. Sci. Agri. 2003, 60, 793–806. [Google Scholar] [CrossRef]
  165. Pierart, A.; Shahid, M.; Séjalon-Delmas, N.; Dumat, C. Antimony bioavailability: Knowledge and research perspectives for sustainable agricultures. J. Hazard. Mater. 2015, 289, 219–234. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  166. Pourrut, B.; Shahid, M.; Dumat, C.; Winterton, P.; Pinelli, E. Lead uptake, toxicity, and detoxification in plants. In Reviews of Environmental Contamination and Toxicology; Springer: Berlin, Germany, 2011; Volume 213, pp. 113–136. [Google Scholar]
  167. Shahid, M.; Dumat, C.; Khalid, S.; Niazi, N.K.; Antunes, P.M. Cadmium bioavailability, uptake, toxicity and detoxification in soil-plant system. Rev. Environ. Contam. Toxicol. 2017, 241, 73–137. [Google Scholar] [PubMed]
  168. Shahid, M.; Dumat, C.; Khalid, S.; Schreck, E.; Xiong, T.; Niazi, N.K. Foliar heavy metal uptake, toxicity and detoxification in plants: A comparison of foliar and root metal uptake. J. Hazard. Mater. 2017, 325, 36–58. [Google Scholar] [CrossRef] [PubMed]
  169. Li, Z.; Ma, Z.; van der Kuijp, T.J.; Yuan, Z.; Huang, L. A review of soil heavy metal pollution from mines in China: Pollution and health risk assessment. Sci. Total Environ. 2014, 468, 843–853. [Google Scholar] [CrossRef] [PubMed]
  170. Yi, Y.; Yang, Z.; Zhang, S. Ecological risk assessment of heavy metals in sediment and human health risk assessment of heavy metals in fishes in the middle and lower reaches of the Yangtze River basin. Environ. Pollut. 2011, 159, 2575–2585. [Google Scholar] [CrossRef] [PubMed]
  171. Lim, H.-S.; Lee, J.-S.; Chon, H.-T.; Sager, M. Heavy metal contamination and health risk assessment in the vicinity of the abandoned Songcheon Au–Ag mine in Korea. J. Geochem. Explor. 2008, 96, 223–230. [Google Scholar] [CrossRef]
  172. Luo, X.-S.; Ding, J.; Xu, B.; Wang, Y.-J.; Li, H.-B.; Yu, S. Incorporating bioaccessibility into human health risk assessments of heavy metals in urban park soils. Sci. Total Environ. 2012, 424, 88–96. [Google Scholar] [CrossRef] [PubMed]
  173. Khan, A.; Javid, S.; Muhmood, A.; Mjeed, T.; Niaz, A.; Majeed, A. Heavy metal status of soil and vegetables grown on peri-urban area of Lahore district. Soil Environ. 2013, 32, 49–54. [Google Scholar]
  174. Hu, H.; Jin, Q.; Kavan, P. A study of heavy metal pollution in China: Current status, pollution-control policies and countermeasures. Sustainability 2014, 6, 5820–5838. [Google Scholar] [CrossRef]
  175. Abedi-Koupai, J.; Mollaei, R.; Eslamian, S.S. The effect of pumice on reduction of cadmium uptake by spinach irrigated with wastewater. Ecohydrol. Hydrobiol. 2015, 15, 208–214. [Google Scholar] [CrossRef]
  176. Abdu, N.; Abdulkadir, A.; Agbenin, J.O.; Buerkert, A. Vertical distribution of heavy metals in wastewater-irrigated vegetable garden soils of three West African cities. Nutr. Cycl. Agroecosyst. 2011, 89, 387–397. [Google Scholar] [CrossRef]
  177. Meng, W.; Wang, Z.; Hu, B.; Wang, Z.; Li, H.; Goodman, R.C. Heavy metals in soil and plants after long-term sewage irrigation at Tianjin China: A case study assessment. Agric. Water Manag. 2016, 171, 153–161. [Google Scholar] [CrossRef]
  178. Qishlaqi, A.; Moore, F.; Forghani, G. Impact of untreated wastewater irrigation on soils and crops in Shiraz suburban area, SW Iran. Environ. Monit. Assess. 2008, 141, 257–273. [Google Scholar] [CrossRef] [PubMed]
  179. Abbasi, A.M.; Iqbal, J.; Khan, M.A.; Shah, M.H. Health risk assessment and multivariate apportionment of trace metals in wild leafy vegetables from Lesser Himalayas, Pakistan. Ecotoxicol. Environ. Saf. 2013, 92, 237–244. [Google Scholar] [CrossRef] [PubMed]
  180. Chung, B.; Song, C.; Park, B.; Cho, J. Heavy metals in brown rice (Oryza sativa L.) and soil after long-term irrigation of wastewater discharged from domestic sewage treatment plants. Pedosphere 2011, 21, 621–627. [Google Scholar] [CrossRef]
  181. Qureshi, A.S.; Hussain, M.I.; Ismail, S.; Khan, Q.M. Evaluating heavy metal accumulation and potential health risks in vegetables irrigated with treated wastewater. Chemosphere 2016, 163, 54–61. [Google Scholar] [CrossRef] [PubMed]
  182. Rodda, N.; Salukazana, L.; Jackson, S.; Smith, M. Use of domestic greywater for small-scale irrigation of food crops: Effects on plants and soil. Phys. Chem. Earth Parts A/B/C 2011, 36, 1051–1062. [Google Scholar] [CrossRef]
  183. De Melo, W.J.; de Stefani Aguiar, P.; de Melo, G.M.P.; de Melo, V.P. Nickel in a tropical soil treated with sewage sludge and cropped with maize in a long-term field study. Soil Biol. Biochem. 2007, 39, 1341–1347. [Google Scholar] [CrossRef]
  184. Akoto, O.; Addo, D.; Baidoo, E.; Agyapong, E.A.; Apau, J.; Fei-Baffoe, B. Heavy metal accumulation in untreated wastewater-irrigated soil and lettuce (Lactuca sativa). Environ. Earth Sci. 2015, 74, 6193–6198. [Google Scholar] [CrossRef]
  185. Nazir, R.; Khan, M.; Masab, M.; Rehman, H.U.; Rauf, N.U.; Shahab, S.; Ameer, N.; Sajed, M.; Ullah, M.; Rafeeq, M. Accumulation of heavy metals (Ni, Cu, Cd, Cr, Pb, Zn, Fe) in the soil, water and plants and analysis of physico-chemical parameters of soil and water collected from Tanda Dam Kohat. J. Pharm. Sci. Res. 2015, 7, 89–97. [Google Scholar]
  186. Lu, Y.; Yao, H.; Shan, D.; Jiang, Y.; Zhang, S.; Yang, J. Heavy metal residues in soil and accumulation in maize at long-term wastewater irrigation area in Tongliao, China. J. Chem. 2015, 2015, 628280. [Google Scholar] [CrossRef]
  187. Sharma, R.K.; Agrawal, M.; Marshall, F. Heavy metal contamination of soil and vegetables in suburban areas of Varanasi, India. Ecotoxicol. Environ. Saf. 2007, 66, 258–266. [Google Scholar] [CrossRef] [PubMed]
  188. Jamali, M.; Kazi, T.; Arain, M.; Afridi, H.; Jalbani, N.; Memon, A. Heavy metal contents of vegetables grown in soil, irrigated with mixtures of wastewater and sewage sludge in Pakistan, using ultrasonic-assisted pseudo-digestion. J. Agron. Crop Sci. 2007, 193, 218–228. [Google Scholar] [CrossRef]
  189. Huong, N.T.L.; Ohtsubo, M.; Li, L.; Higashi, T.; Kanayama, M. Heavy-Metal Contamination of Soil and Vegetables in Wastewater-Irrigated Agricultural Soil in a Suburban Area of Hanoi, Vietnam. Commun. Soil Sci. Plant Anal. 2010, 41, 390–407. [Google Scholar] [CrossRef]
  190. Masona, C.; Mapfaire, L.; Mapurazi, S.; Makanda, R. Assessment of heavy metal accumulation in wastewater irrigated soil and uptake by maize plants (Zea mays L.) at Firle Farm in Harare. J. Sustain. Dev. 2011, 4, 132. [Google Scholar] [CrossRef]
  191. Nguyen, T.L.H.; Kanayama, M.; Higashi, T.; Le, V.C.; Doan, T.H.; Daochu, A. Heavy Metal of Soil in Wastewater–Irrigated Agricultural Soil in a Surrounding Area of the Nhue River, Vietnam. J. Fac. Agric. Kyushu Univ. 2014, 59, 149–154. [Google Scholar]
  192. Oyeku, O.; Eludoyin, A. Heavy metal contamination of groundwater resources in a Nigerian urban settlement. Afr. J. Environ. Sci. Technol. 2010, 4, 201–214. [Google Scholar]
  193. Alia, N.; Sardar, K.; Said, M.; Salma, K.; Sadia, A.; Sadaf, S.; Toqeer, A.; Miklas, S. Toxicity and bioaccumulation of heavy metals in spinach (Spinacia oleracea) grown in a controlled environment. Int. J. Environ. Res. Public Health 2015, 12, 7400–7416. [Google Scholar] [CrossRef] [PubMed]
  194. Verma, R.; Suthar, S. Lead and cadmium removal from water using duckweed–Lemna gibba L.: Impact of pH and initial metal load. Alex. Eng. J. 2015, 54, 1297–1304. [Google Scholar] [CrossRef]
  195. Zia, M.H.; Watts, M.J.; Niaz, A.; Middleton, D.R.; Kim, A.W. Health risk assessment of potentially harmful elements and dietary minerals from vegetables irrigated with untreated wastewater, Pakistan. Environ. Geochem. Health 2017, 39, 707–728. [Google Scholar] [CrossRef] [PubMed]
  196. Feenstra, S.; Hussain, R.; van der Hoek, W. Health Risks of Irrigation with Untreated Urban Wastewater in the Southern Punjab, Pakistan; International Water Management Institute: Lahore, Pakistan, 2000. [Google Scholar]
  197. Aslam, M.M.; Malik, M.; Baig, M.; Qazi, I.; Iqbal, J. Treatment performances of compost-based and gravel-based vertical flow wetlands operated identically for refinery wastewater treatment in Pakistan. Ecol. Eng. 2007, 30, 34–42. [Google Scholar] [CrossRef]
  198. Ensink, J.H.; Van der Hoek, W. Implementation of the WHO guidelines for the safe use of wastewater in Pakistan: Balancing risks and benefits. J. Water Health 2009, 7, 464–468. [Google Scholar] [CrossRef] [PubMed]
  199. Sheikh, K.H.; Irshad, M. Wastewater effluents from a tannery: Their effects on soil and vegetation in Pakistan. Environ. Conserv. 1980, 7, 319–324. [Google Scholar] [CrossRef]
  200. Amin, N.; Ibrar, D.; Alam, S. Heavy metals accumulation in soil irrigated with industrial effluents of Gadoon Industrial Estate, Pakistan and its comparison with fresh water irrigated soil. J. Agric. Chem. Environ. 2014, 3, 80. [Google Scholar] [CrossRef]
  201. Cecchi, M.; Dumat, C.; Alric, A.; Felix-Faure, B.; Pradère, P.; Guiresse, M. Multi-metal contamination of a calcic cambisol by fallout from a lead-recycling plant. Geoderma 2008, 144, 287–298. [Google Scholar] [CrossRef] [Green Version]
  202. Rafique, R.; Zahra, Z.; Virk, N.; Shahid, M.; Pinelli, E.; Park, T.J.; Kallerhoff, J.; Arshad, M. Dose-dependent physiological responses of Triticum aestivum L. to soil applied TiO2 nanoparticles: Alterations in chlorophyll content, H2O2 production, and genotoxicity. Agric. Ecosyst. Environ. 2018, 255, 95–101. [Google Scholar] [CrossRef]
  203. Khalid, S.; Shahid, M.; Niazi, N.K.; Rafiq, M.; Bakhat, H.F.; Imran, M.; Abbas, T.; Bibi, I.; Dumat, C. Arsenic behaviour in soil-plant system: Biogeochemical reactions and chemical speciation influences. In Enhancing Cleanup of Environmental Pollutants; Springer: Berlin, Germany, 2017; pp. 97–140. [Google Scholar]
  204. Saifullah; Shahid, M.; Zia-Ur-Rehman, M.; Sabir, M.; Ahmad, H.R. Chapter 14—Phytoremediation of Pb-Contaminated Soils Using Synthetic Chelates. In Soil Remediation and Plants; Mermut, K.R.H.S.Ö.R., Ed.; Academic Press: San Diego, CA, USA, 2015; pp. 397–414. [Google Scholar]
  205. Muchuweti, M.; Birkett, J.; Chinyanga, E.; Zvauya, R.; Scrimshaw, M.D.; Lester, J. Heavy metal content of vegetables irrigated with mixtures of wastewater and sewage sludge in Zimbabwe: Implications for human health. Agric. Ecosyst. Environ. 2006, 112, 41–48. [Google Scholar] [CrossRef]
  206. Chopra, A.; Pathak, C. Accumulation of heavy metals in the vegetables grown in wastewater irrigated areas of Dehradun, India with reference to human health risk. Environ. Monit. Assess. 2015, 187, 445. [Google Scholar] [CrossRef] [PubMed]
  207. Kiziloglu, F.; Turan, M.; Sahin, U.; Kuslu, Y.; Dursun, A. Effects of untreated and treated wastewater irrigation on some chemical properties of cauliflower (Brassica olerecea L. var. botrytis) and red cabbage (Brassica olerecea L. var. rubra) grown on calcareous soil in Turkey. Agric. Water Manag. 2008, 95, 716–724. [Google Scholar] [CrossRef]
  208. Singh, R.; Agrawal, M. Potential benefits and risks of land application of sewage sludge. Waste Manag. 2008, 28, 347–358. [Google Scholar] [CrossRef] [PubMed]
  209. Singh, R.; Agrawal, M. Variations in heavy metal accumulation, growth and yield of rice plants grown at different sewage sludge amendment rates. Ecotoxicol. Environ. Saf. 2010, 73, 632–641. [Google Scholar] [CrossRef] [PubMed]
  210. Farooq, M.; Anwar, F.; Rashid, U. Appraisal of heavy metal contents in different vegetables grown in the vicinity of an industrial area. Pak. J. Bot. 2008, 40, 2099–2106. [Google Scholar]
  211. Shahid, M.; Ferrand, E.; Schreck, E.; Dumat, C. Behavior and impact of zirconium in the soil–plant system: Plant uptake and phytotoxicity. In Reviews of Environmental Contamination and Toxicology; Springer: Berlin, Germany, 2013; Volume 221, pp. 107–127. [Google Scholar]
  212. Shahid, M.; Dumat, C.; Pourrut, B.; Sabir, M.; Pinelli, E. Assessing the effect of metal speciation on lead toxicity to Vicia faba pigment contents. J. Geochem. Explor. 2014, 144, 290–297. [Google Scholar] [CrossRef]
  213. Rafiq, M.; Shahid, M.; Abbas, G.; Shamshad, S.; Khalid, S.; Niazi, N.K.; Dumat, C. Comparative effect of calcium and EDTA on arsenic uptake and physiological attributes of Pisum sativum. Int. J. Phytoremed. 2017, 19, 662–669. [Google Scholar] [CrossRef] [PubMed]
  214. Rafiq, M.; Shahid, M.; Shamshad, S.; Khalid, S.; Niazi, N.K.; Abbas, G.; Saeed, M.F.; Ali, M.; Murtaza, B. A comparative study to evaluate efficiency of EDTA and calcium in alleviating arsenic toxicity to germinating and young Vicia faba L. seedlings. J. Soils Sedim. 2017, 1–11. [Google Scholar] [CrossRef]
  215. Shahid, M.; Arshad, M.; Kaemmerer, M.; Pinelli, E.; Probst, A.; Baque, D.; Pradere, P.; Dumat, C. Long-term field metal extraction by Pelargonium: Phytoextraction efficiency in relation to plant maturity. Int. J. Phytoremed. 2012, 14, 493–505. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  216. Shahid, M.; Pinelli, E.; Pourrut, B.; Dumat, C. Effect of organic ligands on lead-induced oxidative damage and enhanced antioxidant defense in the leaves of Vicia faba plants. J. Geochem. Explor. 2014, 144, 282–289. [Google Scholar] [CrossRef]
  217. Shahid, M.; Dumat, C.; Aslam, M.; Pinelli, E. Assessment of lead speciation by organic ligands using speciation models. Chem. Speciat. Bioavailab. 2012, 24, 248–252. [Google Scholar] [CrossRef]
  218. Foucault, Y.; Lévêque, T.; Xiong, T.; Schreck, E.; Austruy, A.; Shahid, M.; Dumat, C. Green manure plants for remediation of soils polluted by metals and metalloids: Ecotoxicity and human bioavailability assessment. Chemosphere 2013, 93, 1430–1435. [Google Scholar] [CrossRef] [PubMed]
  219. Austruy, A.; Shahid, M.; Xiong, T.; Castrec, M.; Payre, V.; Niazi, N.K.; Sabir, M.; Dumat, C. Mechanisms of metal-phosphates formation in the rhizosphere soils of pea and tomato: Environmental and sanitary consequences. J. Soils Sedim. 2014, 14, 666–678. [Google Scholar] [CrossRef]
  220. Niazi, N.K.; Bibi, I.; Fatimah, A.; Shahid, M.; Javed, M.T.; Wang, H.; Ok, Y.S.; Bashir, S.; Murtaza, B.; Saqib, Z.A. Phosphate-assisted phytoremediation of arsenic by Brassica napus and Brassica juncea: Morphological and physiological response. Int. J. Phytoremed. 2017, 19, 670–678. [Google Scholar] [CrossRef] [PubMed]
  221. Sun, Y.-B.; Zhou, Q.-X.; An, J.; Liu, W.-T.; Liu, R. Chelator-enhanced phytoextraction of heavy metals from contaminated soil irrigated by industrial wastewater with the hyperaccumulator plant (Sedum alfredii Hance). Geoderma 2009, 150, 106–112. [Google Scholar] [CrossRef]
  222. Dhir, B.; Srivastava, S. Heavy metal removal from a multi-metal solution and wastewater by Salvinia Natans. Ecol. Eng. 2011, 37, 893–896. [Google Scholar] [CrossRef]
  223. Bennicelli, R.; Stępniewska, Z.; Banach, A.; Szajnocha, K.; Ostrowski, J. The ability of Azolla caroliniana to remove heavy metals (Hg (II), Cr (III), Cr (VI)) from municipal waste water. Chemosphere 2004, 55, 141–146. [Google Scholar] [CrossRef] [PubMed]
  224. Niazi, N.K.; Singh, B.; Van Zwieten, L.; Kachenko, A.G. Phytoremediation potential of Pityrogramma calomelanos var. austroamericana and Pteris vittata L. grown at a highly variable arsenic contaminated site. Int. J. Phytoremed. 2011, 13, 912–932. [Google Scholar] [CrossRef] [PubMed]
  225. Arshad, M.; Silvestre, J.; Pinelli, E.; Kallerhoff, J.; Kaemmerer, M.; Tarigo, A.; Shahid, M.; Guiresse, M.; Pradère, P.; Dumat, C. A field study of lead phytoextraction by various scented Pelargonium cultivars. Chemosphere 2008, 71, 2187–2192. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  226. Niazi, N.K.; Bashir, S.; Bibi, I.; Murtaza, B.; Shahid, M.; Javed, M.T.; Shakoor, M.B.; Saqib, Z.A.; Nawaz, M.F.; Aslam, Z. Phytoremediation of Arsenic-Contaminated Soils Using Arsenic Hyperaccumulating Ferns. In Phytoremediation; Springer: Berlin, Germany, 2016; pp. 521–545. [Google Scholar]
  227. Niazi, N.K.; Singh, B.; Van Zwieten, L.; Kachenko, A.G. Phytoremediation of an arsenic-contaminated site using Pteris vittata L. and Pityrogramma calomelanos var. austroamericana: A long-term study. Environ. Sci. Pollut. Res. 2012, 19, 3506–3515. [Google Scholar] [CrossRef] [PubMed]
  228. Sabir, M.; Waraich, E.A.; Hakeem, K.R.; Öztürk, M.; Ahmad, H.R.; Shahid, M. Phytoremediation: Mechanisms and adaptations. Soil Remediat. Plants Prospects Chall. 2014, 85, 85–105. [Google Scholar]
  229. Mombo, S.; Dumat, C.; Shahid, M.; Schreck, E. A socio-scientific analysis of the environmental and health benefits as well as potential risks of cassava production and consumption. Environ. Sci. Pollut. Res. 2016, 24, 5207–5221. [Google Scholar] [CrossRef] [PubMed]
  230. Xiong, T.; Austruy, A.; Pierart, A.; Shahid, M.; Schreck, E.; Mombo, S.; Dumat, C. Kinetic study of phytotoxicity induced by foliar lead uptake for vegetables exposed to fine particles and implications for sustainable urban agriculture. J. Environ. Sci. 2016, 46, 16–27. [Google Scholar] [CrossRef] [PubMed]
  231. Ashraf, A.; Bibi, I.; Niazi, N.K.; Ok, Y.S.; Murtaza, G.; Shahid, M.; Kunhikrishnan, A.; Li, D.; Mahmood, T. Chromium (VI) sorption efficiency of acid-activated banana peel over organo-montmorillonite in aqueous solutions. Int. J. Phytoremed. 2017, 19, 605–613. [Google Scholar] [CrossRef] [PubMed]
  232. Abbas, G.; Murtaza, B.; Bibi, I.; Shahid, M.; Niazi, N.; Khan, M.; Amjad, M.; Hussain, M. Arsenic Uptake, Toxicity, Detoxification, and Speciation in Plants: Physiological, Biochemical, and Molecular Aspects. Int. J. Environ. Res. Public Health 2018, 15, 59. [Google Scholar] [CrossRef] [PubMed]
  233. Hasan, M.; Cheng, Y.; Kanwar, M.K.; Chu, X.-Y.; Ahammed, G.J.; Qi, Z.-Y. Responses of Plant Proteins to Heavy Metal Stress—A Review. Front. Plant Sci. 2017, 8, 1492. [Google Scholar] [CrossRef] [PubMed]
  234. Zhang, M.; Liu, B. Identification of a rice metal tolerance protein OsMTP11 as a manganese transporter. PLoS ONE 2017, 12, e0174987. [Google Scholar] [CrossRef] [PubMed]
  235. Liu, G.; Chai, T.; Sun, T. Heavy metal absorption, transportation and accumulation mechanisms in hyperaccumulator Thlaspi caerulescens. Sheng wu Gong Cheng Xue Bao Chin. J. Biotechnol. 2010, 26, 561–568. [Google Scholar]
  236. Satoh-Nagasawa, N.; Mori, M.; Nakazawa, N.; Kawamoto, T.; Nagato, Y.; Sakurai, K.; Takahashi, H.; Watanabe, A.; Akagi, H. Mutations in rice (Oryza sativa) heavy metal ATPase 2 (OsHMA2) restrict the translocation of zinc and cadmium. Plant Cell Physiol. 2011, 53, 213–224. [Google Scholar] [CrossRef] [PubMed]
  237. Papoyan, A.; Kochian, L.V. Identification of Thlaspi caerulescens genes that may be involved in heavy metal hyperaccumulation and tolerance. Characterization of a novel heavy metal transporting ATPase. Plant Physiol. 2004, 136, 3814–3823. [Google Scholar] [CrossRef] [PubMed]
  238. Lee, S.; Kim, Y.-Y.; Lee, Y.; An, G. Rice P1B-type heavy-metal ATPase, OsHMA9, is a metal efflux protein. Plant Physiol. 2007, 145, 831–842. [Google Scholar] [CrossRef] [PubMed]
  239. Khalid, S.; Shahid, M.; Niazi, N.K.; Murtaza, B.; Bibi, I.; Dumat, C. A comparison of technologies for remediation of heavy metal contaminated soils. J. Geochem. Explor. 2017, 182, 247–268. [Google Scholar] [CrossRef]
  240. Guerinot, M.L. The ZIP family of metal transporters. Biochim. Biophys. Acta (BBA) Biomembranes 2000, 1465, 190–198. [Google Scholar] [CrossRef]
  241. Krämer, U.; Talke, I.N.; Hanikenne, M. Transition metal transport. FEBS Lett. 2007, 581, 2263–2272. [Google Scholar] [CrossRef] [PubMed]
  242. Montanini, B.; Blaudez, D.; Jeandroz, S.; Sanders, D.; Chalot, M. Phylogenetic and functional analysis of the Cation Diffusion Facilitator (CDF) family: Improved signature and prediction of substrate specificity. BMC Genom. 2007, 8, 107. [Google Scholar] [CrossRef] [PubMed]
  243. Guffanti, A.A.; Wei, Y.; Rood, S.V.; Krulwich, T.A. An antiport mechanism for a member of the cation diffusion facilitator family: Divalent cations efflux in exchange for K+ and H+. Mol. Microbiol. 2002, 45, 145–153. [Google Scholar] [CrossRef] [PubMed]
  244. Pottier, M.; Oomen, R.; Picco, C.; Giraudat, J.; Scholz-Starke, J.; Richaud, P.; Carpaneto, A.; Thomine, S. Identification of mutations allowing Natural Resistance Associated Macrophage Proteins (NRAMP) to discriminate against cadmium. Plant J. 2015, 83, 625–637. [Google Scholar] [CrossRef] [PubMed]
  245. Pourrut, B.; Shahid, M.; Douay, F.; Dumat, C.; Pinelli, E. Molecular mechanisms involved in lead uptake, toxicity and detoxification in higher plants. In Heavy Metal Stress in Plants; Springer: Berlin, Germany, 2013; pp. 121–147. [Google Scholar]
  246. Shahid, M.; Xiong, T.; Masood, N.; Leveque, T.; Quenea, K.; Austruy, A.; Foucault, Y.; Dumat, C. Influence of plant species and phosphorus amendments on metal speciation and bioavailability in a smelter impacted soil: A case study of food-chain contamination. J. Soils Sedim. 2014, 14, 655–665. [Google Scholar] [CrossRef]
  247. Shahid, M.; Dumat, C.; Pourrut, B.; Silvestre, J.; Laplanche, C.; Pinelli, E. Influence of EDTA and citric acid on lead-induced oxidative stress to Vicia faba roots. J. Soils Sedim. 2014, 14, 835–843. [Google Scholar] [CrossRef]
  248. Shahid, M.; Xiong, T.; Castrec-Rouelle, M.; Leveque, T.; Dumat, C. Water extraction kinetics of metals, arsenic and dissolved organic carbon from industrial contaminated poplar leaves. J. Environ. Sci. 2013, 25, 2451–2459. [Google Scholar] [CrossRef]
  249. Emamverdian, A.; Ding, Y.; Mokhberdoran, F.; Xie, Y. Heavy metal stress and some mechanisms of plant defense response. Sci. World J. 2015, 2015, 756120. [Google Scholar] [CrossRef] [PubMed]
  250. Shahid, M.; Dumat, C.; Pourrut, B.; Abbas, G.; Shahid, N.; Pinelli, E. Role of metal speciation in lead-induced oxidative stress to Vicia faba roots. Rus. J. Plant Physiol. 2015, 62, 448–454. [Google Scholar] [CrossRef]
  251. Shahid, M.; Austruy, A.; Echevarria, G.; Arshad, M.; Sanaullah, M.; Aslam, M.; Nadeem, M.; Nasim, W.; Dumat, C. EDTA-enhanced phytoremediation of heavy metals: A review. Soil Sedim. Contam. Int. J. 2014, 23, 389–416. [Google Scholar] [CrossRef]
  252. Shamshad, S.; Shahid, M.; Rafiq, M.; Khalid, S.; Dumat, C.; Sabir, M.; Murtaza, B.; Farooq, A.B.U.; Shah, N.S. Effect of organic amendments on cadmium stress to pea: A multivariate comparison of germinating vs young seedlings and younger vs older leaves. Ecotoxicol. Environ. Saf. 2018, 151, 91–97. [Google Scholar] [CrossRef] [PubMed]
  253. Shahid, M.; Pinelli, E.; Pourrut, B.; Silvestre, J.; Dumat, C. Lead-induced genotoxicity to Vicia faba L. roots in relation with metal cell uptake and initial speciation. Ecotoxicol. Environ. Saf. 2011, 74, 78–84. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  254. Fuhrimann, S.; Winkler, M.S.; Kabatereine, N.B.; Tukahebwa, E.M.; Halage, A.A.; Rutebemberwa, E.; Medlicott, K.; Schindler, C.; Utzinger, J.; Cissé, G. Risk of intestinal parasitic infections in people with different exposures to wastewater and fecal sludge in Kampala, Uganda: A cross-sectional study. PLoS Negl. Trop. Dis. 2016, 10, e0004469. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  255. Fuhrimann, S.; Winkler, M.S.; Schneeberger, P.H.; Niwagaba, C.B.; Buwule, J.; Babu, M.; Medlicott, K.; Utzinger, J.; Cissé, G. Health risk assessment along the wastewater and faecal sludge management and reuse chain of Kampala, Uganda: A visualization. Geospat. Health 2014, 9, 251–255. [Google Scholar] [CrossRef] [PubMed]
  256. Yapo, R.; Koné, B.; Bonfoh, B.; Cissé, G.; Zinsstag, J.; Nguyen-Viet, H. Quantitative microbial risk assessment related to urban wastewater and lagoon water reuse in Abidjan, Côte d’Ivoire. J. Water Health 2014, 12, 301–309. [Google Scholar] [CrossRef] [PubMed]
  257. Fuhrimann, S.; Winkler, M.S.; Stalder, M.; Niwagaba, C.B.; Babu, M.; Kabatereine, N.B.; Halage, A.A.; Utzinger, J.; Cissé, G.; Nauta, M. Disease burden due to gastrointestinal pathogens in a wastewater system in Kampala, Uganda. Microb. Risk Anal. 2016, 4, 16–28. [Google Scholar] [CrossRef]
  258. Corcoran, E. Sick Water? The Central Role of Wastewater Management in Sustainable Development: A Rapid Response Assessment; UNEP/Earthprint: Nairobi, Kenya, 2010. [Google Scholar]
  259. Prüss-Ustün, A.; Bartram, J.; Clasen, T.; Colford, J.M.; Cumming, O.; Curtis, V.; Bonjour, S.; Dangour, A.D.; De France, J.; Fewtrell, L. Burden of disease from inadequate water, sanitation and hygiene in low-and middle-income settings: A retrospective analysis of data from 145 countries. Trop. Med. Int. Health 2014, 19, 894–905. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  260. Wolf, J.; Prüss-Ustün, A.; Cumming, O.; Bartram, J.; Bonjour, S.; Cairncross, S.; Clasen, T.; Colford, J.M.; Curtis, V.; France, J. Systematic review: Assessing the impact of drinking water and sanitation on diarrhoeal disease in low-and middle-income settings: Systematic review and meta-regression. Trop.Med. Int. Health 2014, 19, 928–942. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  261. Mok, H.F.; Hamilton, A.J. Exposure factors for wastewater-irrigated Asian vegetables and a probabilistic rotavirus disease burden model for their consumption. Risk Anal. 2014, 34, 602–613. [Google Scholar] [CrossRef] [PubMed]
  262. Shakoor, M.B.; Niazi, N.K.; Bibi, I.; Rahman, M.M.; Naidu, R.; Dong, Z.; Shahid, M.; Arshad, M. Unraveling health risk and speciation of arsenic from groundwater in rural areas of Punjab, Pakistan. Int. J. Environ. Res. Public Health 2015, 12, 12371–12390. [Google Scholar] [CrossRef] [PubMed]
  263. Mara, D.; Sleigh, A. Estimation of Ascaris infection risks in children under 15 from the consumption of wastewater-irrigated carrots. J. Water Health 2010, 8, 35–38. [Google Scholar] [CrossRef] [PubMed]
  264. Hien, B.T.T.; Scheutz, F.; Cam, P.D.; Mølbak, K.; Dalsgaard, A. Diarrhoeagenic Escherichia coli and other causes of childhood diarrhoea: A case–control study in children living in a wastewater-use area in Hanoi, Vietnam. J. Med. Microbiol. 2007, 56, 1086–1096. [Google Scholar] [CrossRef] [PubMed]
  265. Cotruvo, J.A.; Dufour, A.; Rees, G.; Bartram, J.; Carr, R.; Cliver, D.O.; Craun, G.F.; Fayer, R.; Gannon, V.P. Waterborne Zoonoses; Iwa Publishing: London, UK, 2004. [Google Scholar]
  266. Parasidis, T.; Vorou, E.; Theodoropoulou-Rodiou, G.; Katsantridou, G.; Stamatopoulou, G.; Vantarakis, A. Outbreak of gastroenteritis occurred in North-Eastern Greece associated with several waterborne strains of noroviruses. Int. J. Infect. Dis. 2008, 12, e104–e105. [Google Scholar] [CrossRef]
  267. Muller, E.; Grabow, W.; Ehlers, M. Immunomagnetic separation of Escherichia coli O157: H7 from environmental and wastewater in South Africa. Water SA 2003, 29, 427–432. [Google Scholar] [CrossRef]
  268. Seguí Amórtegui, L.A. Sistemas de Regeneración y Reutilización de Aguas Residuales. Metodología Para el Análisis Técnico-Económico y Casos; Universitat Politècnica de Catalunya: Barcelona, Spain, 2004. [Google Scholar]
  269. Vilar, J.L.B.; Bernabeu-Mestre, J. La Salud y el Estado: El Movimiento Sanitario Internacional y la Administración Española (1851–1945); Universitat de València: València, Spain, 2011. [Google Scholar]
  270. Angelakis, A.N.; Snyder, S.A. Wastewater treatment and reuse: Past, present, and future. Water 2015, 7, 4887–4895. [Google Scholar] [CrossRef]
  271. World Health Organization. Health Guidelines for the Use of Wastewater in Agriculture and Aquaculture: Report of a WHO Scientific Group [Meeting held in Geneva from 18 to 23 November 1987]; WHO: Geneva, Switzerland, 1989. [Google Scholar]
  272. Xiong, T.; Dumat, C.; Dappe, V.; Vezin, H.; Schreck, E.; Shahid, M.; Pierart, A.; Sobanska, S. Copper oxide nanoparticle foliar uptake, phytotoxicity, and consequences for sustainable urban agriculture. Environ. Sci. Technol. 2017, 51, 5242–5251. [Google Scholar] [CrossRef] [PubMed]
  273. Farahat, E.A.; Galal, T.M.; Elawa, O.E.; Hassan, L.M. Health risk assessment and growth characteristics of wheat and maize crops irrigated with contaminated wastewater. Environ. Monit. Assess. 2017, 189, 535. [Google Scholar] [CrossRef] [PubMed]
  274. Antoniadis, V.; Levizou, E.; Shaheen, S.M.; Ok, Y.S.; Sebastian, A.; Baum, C.; Prasad, M.N.; Wenzel, W.W.; Rinklebe, J. Trace elements in the soil-plant interface: Phytoavailability, translocation, and phytoremediation–A review. Earth Sci. Rev. 2017, 171, 621–645. [Google Scholar] [CrossRef]
  275. Bakhat, H.F.; Zia, Z.; Fahad, S.; Abbas, S.; Hammad, H.M.; Shahzad, A.N.; Abbas, F.; Alharby, H.; Shahid, M. Arsenic uptake, accumulation and toxicity in rice plants: Possible remedies for its detoxification: A review. Environ. Sci. Pollut. Res. 2017, 24, 9142–9158. [Google Scholar] [CrossRef] [PubMed]
  276. Shabir, R.; Abbas, G.; Saqib, M.; Shahid, M.; Shah, G.; Akram, M.; Niazi, N.; Naeem, M.; Hussain, M.; Ashraf, F. Cadmium tolerance and phytoremediation potential of acacia (Acacia nilotica L.) under salinity stress. Int. J. Phytoremed. 2018. [Google Scholar] [CrossRef]
  277. Tijani, M.N.; Onodera, S. Hydrogeochemical assessment of metals contamination in an urban drainage system: A case study of Osogbo township, SW-Nigeria. J. Water Resour. Protect. 2009, 1, 164. [Google Scholar] [CrossRef]
  278. Oti, W.O. Bioaccumulation factors and pollution indices of heavy metals in selected fruits and vegetables from a derelict mine and their associated health implications. Int. J. Environ. Sustain. 2015, 4, 15–23. [Google Scholar] [CrossRef]
  279. Nirola, R.; Megharaj, M.; Palanisami, T.; Aryal, R.; Venkateswarlu, K.; Naidu, R. Evaluation of metal uptake factors of native trees colonizing an abandoned copper mine—A quest for phytostabilization. J. Sustain. Min. 2015, 14, 115–123. [Google Scholar] [CrossRef]
Figure 1. The possible environmental contamination by the use of wastewater; (PTE: potentially toxic elements).
Figure 1. The possible environmental contamination by the use of wastewater; (PTE: potentially toxic elements).
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Figure 2. The percentage (%) of untreated wastewater discharged into the environment in low and high-income countries.
Figure 2. The percentage (%) of untreated wastewater discharged into the environment in low and high-income countries.
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Figure 3. The possible food chain contamination by wastewater crop irrigation.
Figure 3. The possible food chain contamination by wastewater crop irrigation.
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Table 1. The wastewater production, collection, treatment, and reuse for crop irrigation in different countries in relation to the total agricultural area (Source, Aquastat-FAO) [9].
Table 1. The wastewater production, collection, treatment, and reuse for crop irrigation in different countries in relation to the total agricultural area (Source, Aquastat-FAO) [9].
CountryTotal Area (1000 ha)Cultivated Area (1000 ha)Total Cultivated Area (%)Produced Municipal Wastewater
(109 m3/year)
Collected Municipal Wastewater
(109 m3/year)
Treated Municipal Wastewater
(109 m3/year)
Use of Treated Wastewater for Irrigation
(109 m3/year)
Australia774,12247,3076.11--20.28
Brazil851,57786,58910.1--3.10.008
China960,001122,52412.748.5131.1442.371.26
Germany35,73812,07433.7-5.2875.2135.183
India328,726169,36051.5--4.416-
Itlay30,134912130.23.926-3.9020.087
Jordan89323223.60-0.1150.1130.103
Pakistan79,61031,25239.23.06---
South Africa121,90912,91310.53.5422.7691.919-
Turkey78,53523,94430.44.297-3.483-
UK24,361627925.74.0894.0484.048-
USA983,151157,20515.960.4147.2445.35-
Canada998,46750,8465.096.6135.8195.632-
Sweden44,74226085.820.671-0.436-
Table 2. The effect of wastewater and freshwater on vegetable nutrients and heavy metal contents.
Table 2. The effect of wastewater and freshwater on vegetable nutrients and heavy metal contents.
Nutrients and Heavy MetalVegetables/CropsConcentration in Vegetables Irrigated by Fresh Water (mg/kg)Concentration in Vegetables Irrigated by Wastewater (mg/kg)% Decrease or IncreaseReference
NLettuce39,50042,8808.56[61]
Rice29645353.04[62]
Coriander40249924.13
Wheat1601748.75[63]
Rice1351425.185
PLettuce4480553023.44[61]
Rice283835.71[62]
Alfalfa0.260.273.85[64]
Rice354528.57[65]
KRice1364835−38.78[66]
Rice22531238.67[62]
Coriander41651724.28
Alfalfa2.22.513.64[64]
Rice106230116.98[67]
PbTomato4.49.6118.18[68]
Panicum0.010.09800[69]
Brinjal414.15253.75[70]
Radish12.5150[71]
Cypress1.63.2100[72]
Onion11.22.7415[73]
Garlic8.154.94165
Tomato12.74.45285
Brinjal14.154.35325
CdTomato0.030.0433.33[68]
Maize0.020.0350[74]
Cypress0.050.0620[72]
Radish3.45.150[75]
Garlic203050[76]
vegetables, cereal crops3.121.49209[21]
NiTomato4.678.3378.37[68]
Cabbage0.770.8814.29[77]
Tomato1.65.65253[73]
Brinjal37.45148
Maize0.621.1280.65[74]
Lettuce1.311.4712.21[78]
vegetables, cereal crops23.649.06261[21]
AsMaize0.030.08166.67[74]
Carrot0.120.1525[78]
Radish0.490.52.04[78]
Radish0.1353746.15[79]
CrOnion5.051.05481[73]
Garlic2.61260
Tomato6.16.1No
Brinjal12.557.5167
vegetables, cereal crops19.29.07212[21]
FeTomato11822086.44[68]
Onion6.1526.15325.20[73]
Brinjal30037023.33[62]
Sunflower140324131.43[74]
Lettuce510430−15.69[61]
Table 3. The number of microorganisms in soils colony-forming unit per gram (CFU/g) irrigated by wastewater.
Table 3. The number of microorganisms in soils colony-forming unit per gram (CFU/g) irrigated by wastewater.
MicrobesMicrobes CountReference
Coliforms3.3 × 102 cfu/g[130]
Coliforms
Fecal Coliforms
4.39 × 103/100 mL
7.5 × 107 cfu/g
[131]
Fecal streptococci
Fecal coliform
65
240
[132]
Bacteria
(Escherichia coli, Staphylococcus aureus, Streptococcus faecalis)
7.6 × 107 cfu/g
4.6 × 107 cfu/g
[133]
Fungi
(Aspergillus niger, Aspergillus fumigatus, Aspergillus flavus)
6.0 × 106 cfu/g
9.0 × 106 cfu/g
Bacteria
(Lactobacillus plantarum, Pseudomonas aeruginosa)
3.36 × 107 cfu/g[134]
Salmonella
Shigella
Clostridium bacteria
3.5 × 106 cfu/g
5.4 × 104 cfu/g
7.8 × 102 cfu/g
5.1 × 104 cfu/g
[135]
Penicillium expansum
Aspergillus spp.
5.45 × 104 cfu/g
1.30 ×105 cfu/g
[135]
Escherichia coli8.0 × 106 cfu/g
3.8 × 106 cfu/g
[136]
Bacteria
Actinomycetes
Fungi
1.34 × 107 cfu/g
2.21 × 106 cfu/g
9.99 × 103 cfu/g
[137]
Total coliforms2.1 × 103 cfu/g
4.2 × 103 cfu/g
[138]
Fecal coliforms1.2 × 102 cfu/g
4.2 × 102 cfu/g
Table 4. The heavy metal concentration in wastewater, soil, and plants in relation to the transfer and bioaccumulation factors.
Table 4. The heavy metal concentration in wastewater, soil, and plants in relation to the transfer and bioaccumulation factors.
MetalVegetableConcentration in Wastewater (mg/L)Concentration in Soil (mg/kg)Concentration in Plant (mg/kg)Transfer FactorBioaccumulation FactorReference
CdCupressus sempervirens0.060.030.060.52[72]
CdRaphanus sativus-0.840.93-1.29[20]
CdVicia faba-0.110.1-0.9[173]
CdOryza sativa0.0131.13000.4[174]
CdSpinacia oleracea105.8150.62.6[175]
CdLactuca sativa0.0510.2200.2[176]
PbTriticum-41.562.77-0.1[177]
PbRaphanus sativus0.1849.42.6274.40.04[20]
PbTriticum0.585411.726.23703.80.064[178]
PbConvolvulus arvensis-24.71.433-0.058[179]
PbTriticum0.133.42.3334.00.069[151]
PbOryza sativa-5.10.37-0.073[180]
PbCupressus sempervirens9.27.13.20.80.5[72]
ZnRaphanus sativus-15757-0.41[20]
ZnDaucus carota0.2712.42.545.90.202[181]
ZnVicia faba0.360.420.071.20.2[76]
ZnAmaranthus116767167.00.4[176]
ZnBeta vulgaris0.241.7257.114.7[182]
ZnHordeum vulgare0.191.432.27.423.0[116]
ZnCitrus x sinensis0.02134.224.156711.00.031[89]
NiCupressus sepervirens7.111.34.71.60.4[72]
NiOryza sativa1.03351.834.00.051[174]
NiRaphanus sativus-24.911-0.42[20]
NiZea mays-28.132.65-0.09[183]
NiAbelmoschus esculentus1.60.31.40.24.67[132]
NiVicia faba0.040.550.0913.80.2[76]
NiTriticum0.22276.627.191257.30.098[178]
CuCupressus sempervirens4.75.49.41.11.7[72]
CuRaphanus sativus0.25.41.227.00.222[181]
CuRaphanus sativus-32.89-0.32[20]
CuLactuca sativa-7.48.05-1.088[184]
CuXanthium strumarium0.6160.7680.7911.21.0[185]
CuVicia faba0.1810.490.042.70.1[76]
CuCitrus x sinensis0.0394.384.3523146.00.046[89]
TF = Transfer factor from wastewater to the soil, BF = Bioaccumulation Factor from soil to vegetable.
Table 5. The health risk assessment for vegetables cultivated using wastewater.
Table 5. The health risk assessment for vegetables cultivated using wastewater.
MetalVegetableEstimated Daily IntakeHealth Risk IndexHazard QuotientReference
CdCupressus sempervirens0.000030.03150.000009[72]
CdRaphanus sativus0.000490.48790.000134[20]
CdVicia faba0.000050.05250.000014[20]
CdOryza sativa0.000580.57710.000158[174]
CdSpinach oleracea0.007877.86900.002156[175]
CdLactuca sativa0.000110.10490.000029[176]
PbTriticum0.001450.41520.000398[177]
PbRaphanus sativus0.001360.38970.000374[20]
PbTriticum0.013803.93150.003770[178]
PbConvolvulus arvensis0.000750.21480.000206[179]
PbTriticum0.001210.34470.000331[151]
PbOryza sativa0.000190.05550.000053[180]
PbCupressus sempervirens0.001680.47960.000460[72]
ZnRaphanus sativus0.029900.09970.008192[20]
ZnDaucus carota0.001310.00440.000359[181]
ZnAmaranthus0.035100.11720.009630[176]
ZnBeta vulgaris0.013100.04370.003593[182]
ZnHordeum vulgare0.016900.05630.004628[116]
ZnCitrus x sinensis0.002180.00730.000596[89]
NiCupressus sempervirens0.002470.12330.000676[72]
NiRaphanus sativus0.005770.28850.001581[20]
NiZea mays0.001390.06950.000381[183]
NiAbelmoschus esculentus0.000730.03670.000201[132]
NiVicia faba0.000050.00240.000013[76]
NiTriticum0.014300.71320.003908[178]
CuCupressus sempervirens0.004930.12330.001351[72]
CuRaphanus sativus0.000630.01570.000172[181]
CuRaphanus sativus0.004720.11800.001294[20]
CuLactuca sativa0.004220.10560.001157[184]
CuXanthium strumarium0.000420.01040.000114[185]
CuVicia faba0.000020.00050.000006[76]
CuCitrus x sinensis0.002280.05710.000625[89]
Table 6. The heavy metal soil contamination, soil-plant transfer, root-shoot translocation, and health risk assessment parameters used in different risk assessment and remediation studies.
Table 6. The heavy metal soil contamination, soil-plant transfer, root-shoot translocation, and health risk assessment parameters used in different risk assessment and remediation studies.
Soil Contamination and Soil-Plant Transfer IndicesReferencesRisk Assessment IndicesReferences
Degree of contamination (Cdeg)[277]Root-shoot translocation factor (TrF)[215]
Geo-accumulation index (Igeo)[274]Plant pollution index (PPI)[274]
Contamination factor (CF), Enrichment factors (EF)[274]Estimated daily intake (EDI) or Average daily intake (ADI)[31]
Mobilization factor (MF)[215]Hazard quotient (HQ)[31]
Bioaccumulation factor (BF)[278]Maximum allowable daily intake (MDI)[4]
Bioconcentration factor (BCF)[215]Life time cancer risk (ILTCR)[31]
Plant enrichment factors (PEF)[25,279]Health risk index (HRI)[4]
Soil-plant transfer factor (TF) or transfer coefficient (TC)[274]Tolerance index (TI)[274]

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Khalid, S.; Shahid, M.; Natasha; Bibi, I.; Sarwar, T.; Shah, A.H.; Niazi, N.K. A Review of Environmental Contamination and Health Risk Assessment of Wastewater Use for Crop Irrigation with a Focus on Low and High-Income Countries. Int. J. Environ. Res. Public Health 2018, 15, 895. https://0-doi-org.brum.beds.ac.uk/10.3390/ijerph15050895

AMA Style

Khalid S, Shahid M, Natasha, Bibi I, Sarwar T, Shah AH, Niazi NK. A Review of Environmental Contamination and Health Risk Assessment of Wastewater Use for Crop Irrigation with a Focus on Low and High-Income Countries. International Journal of Environmental Research and Public Health. 2018; 15(5):895. https://0-doi-org.brum.beds.ac.uk/10.3390/ijerph15050895

Chicago/Turabian Style

Khalid, Sana, Muhammad Shahid, Natasha, Irshad Bibi, Tania Sarwar, Ali Haidar Shah, and Nabeel Khan Niazi. 2018. "A Review of Environmental Contamination and Health Risk Assessment of Wastewater Use for Crop Irrigation with a Focus on Low and High-Income Countries" International Journal of Environmental Research and Public Health 15, no. 5: 895. https://0-doi-org.brum.beds.ac.uk/10.3390/ijerph15050895

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