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 km
2 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.