Abstract
This study aimed to determine the potentially toxic metal contents in soil and spinach samples in areas irrigated with industrial wastewater and to evaluate the potentially toxic metal accumulation in spinach samples according to pollution indices. Water, soil and spinach samples were analysed using atomic absorption spectrophotometer (Perkin-Elmer AAS-300). In this study, it was determined that the potentially toxic metal values in the spinach samples irrigated with groundwater and sugar industry wastewater varied between 1.59 and 1.84, 0.22–0.68, 0.56–1.14, 1.41–1.56, 1.62–3.23, 0.57–1.02, 0.86–1.33, 0.20–0.32 and 0.35–2.10 mg/kg for Cd, Co, Cr, Cu, Fe, Ni, Pb, Zn and Mn, respectively. It was concluded that the difference between the metal values in the spinach samples according to the irrigation sources was statistically significant, except for Cu and Pb (p > 0.05). According to the results of this study, there is no health risk for Pb, Co and Cr with HRI values below 1.0, while there is a risk for Cd, Cu, Fe, Ni, Mn and Zn. The much higher HRI values of Cd than 1 (196.8 and 169.6) suggested that this metal is likely to cause significant health problems in the region.
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Industrialization has both direct and indirect negative effects on the environment (Ugulu et al. 2021a, b, c, d, e). One of the direct effects of this issue is the wastewater generated in the industrial production process. Wastewater contains potentially toxic metals and pollutants are released into water and soil, posing a serious risk to humans (Khan et al. 2021). These metals can cause metal toxicity, which can cause damage or decrease in the mental and central nervous system, lungs, kidneys, liver and other body organs. In addition, multiple sclerosis, physical, muscular and neurological degeneration processes that mimic Alzheimer's disease occur as a result of long-term exposure to potentially toxic metals. However, it has been reported that the main contributors to soil pollution are by-products of industrial processes, different industries such as sugar processing, energy and power, cement and petrochemicals (Ugulu 2015a, b).
The use of industrial wastewater and municipal wastewater for irrigation is widely used in farmland and suburban areas in many countries (Khan et al. 2019a, b, c). The discharge of wastewater into the environment and agricultural soil without treatment adds large amounts of organic and inorganic pollutants to these areas. In general, industrial wastewater carries many toxic substances, including trace metals. Long-term use of such wastewater in agricultural lands causes high levels of potentially toxic metal accumulation in soil and plants (Sharma et al. 2006). As a result of prolonged wastewater irrigation, vegetables and crops grown in metal-contaminated soil accumulate more potentially toxic metals than those grown in uncontaminated soil. Potentially toxic metals, which can be easily taken up by vegetable roots, can accumulate in the edible parts of vegetables at high levels (Karak et al. 2014).
Spinach (Spinacia oleracea L.) belongs to the Amaranthaceae family and is an eatable vegetable family which is mostly grown in Central and Western Asia spinach grows up to 30 cm tall. It is an annual plant. Spinach has great dietary value, especially when quickly boiled or frozen and steams. The plant contains manganese, magnesium, vitamin A and Vitamin C. It is a rich source of dietary fibre, vitamin B6, riboflavin, B vitamins, vitamin E, potassium and calcium like other green leafy vegetables. However, spinach contains a high level of oxalate which inhibits the absorption of iron (Nadeem et al. 2019).
In Pakistan, where agriculture is among the most important inputs of the country's economy, wastewater such as sewage water, urban wastewater and industrial wastewater are used in agricultural irrigation in various regions of the country (Khan et al. 2018a, b, c). It is seen that many studies have been carried out on the risks to human health of using wastewater in agricultural irrigation for many agricultural products produced in various regions of the country (Ahmad et al. 2018, 2019; Chen et al. 2021; Munir et al. 2019; Nadeem et al. 2019; Rasheed et al. 2020; Siddique et al. 2019; Ugulu et al. 2020; Yang et al. 2020; Tariq et al. 2021). This study aimed to determine the potentially toxic metal contents in soil and spinach samples in areas irrigated with industrial wastewater and to evaluate the potentially toxic metal accumulation in spinach samples according to pollution indices.
Materials and Methods
Sargodha District is surrounded by Jhelum District in the north and Chenab River in the east. Located on the south side is the Jhang District. It is separated from the Khushab District on its western side by the Jhelum River. Sargodha District has a total area of 5854 km2 and consists of five tehsils; Bhalwal, Kot Momin, Sahiwal, Shahpur and Sillanwali. While the maximum temperature in Sargodha Region is 45°C in summer, it drops to 0°C in winter. Currently, 7 textile mills, 4 sugar mills, 12 flour mills and 24 peeling units operate in Sargodha (Khan et al. 2018a, b).
The areas of influence of Chishtia Sugar Mill Limited were selected for sampling in sample collection studies. Sugar Factory is located next to Farooka in tehsil Sillanwali. It was established in 1990 and is pure sugar industry. Chishtia Sugar Mill Limited, which has an annual installed capacity of 7000 Tcd, employs approximately 213 people in Farooka, Sillanwali (Khan and Khan 2019).
100 mL samples were taken from each source to determine the metal content of each of the sugar industry wastewater and groundwater sources used for irrigation of Site 1 and Site 2. The bottles were washed with acid polypropylene and 1 mL of HNO3 was added to prevent microbial growth. Samples were chilled before further analysis.
The first of the soil samples taken from the designated locations was irrigated with groundwater and the second was irrigated with sugar industry wastewater. Soil samples were randomly selected and taken from the upper crust (0–2.5 cm). After all, samples were dried, they were passed through a 2 mm crush strainer. Soil samples were placed on croft paper and stored for examining vegetables. One gram soil sample taken for digestion was mixed with nitric acid (HNO3) in a beaker. After the mixture was left to stand overnight, it was boiled in a digestion tube at 75°C for 1 h and hydrogen peroxide (H2O2) was added until the solution became clear. After digestion was completed, the digested material was removed from the digestion tube and filter paper was used for filtration. This extract was mixed with distilled water to make a volume of 50 mm.
Twenty-five samples were taken from the spinach grown in Site 1 and Site 2, which were irrigated with groundwater and industrial wastewater, respectively. Spinach samples were first washed with deionized water and then dried at 80°C. Samples of 1 g of each vegetable were placed in digestion tubes and nitric acid (HNO3) was added to the tubes. The digestive tube was placed on a 75°C hot plate the next day. After 35 min, hydrogen peroxide (H2O2) was added to the tube and boiled until the resulting solution was clear. The digested material was removed from the digestion tube and filtered using Whatman No.42 filter paper and deionized water was added to increase its volume to 50 mm.
Water, soil and spinach samples were analysed using atomic absorption spectrophotometer (Perkin-Elmer AAS-300). Experimental procedures and analytical methods in the analyzes performed with AAS were performed according to the manufacturer's instrumentation and application guidelines following European Commission (2006) guidelines. The metals identified in the current research are Cd, Co, Cr, Cu, Fe, Ni, Pb, Zn and Mn. Chromium (Cr) and Nickel (Ni) were detected by the very sensitive hydride method. To avoid chemical pre-treatment, these elemental analyses usually use graphite furnace AAS (GFAAS), from which the molten sample can be directly calculated. However, GFAAS is not as sensitive as the hydride technique. Therefore, the use of particularly powerful hollow cathode lamps (super lamps) becomes important for precise measurements. In this study, analyzes were performed for Cr and Ni in aqueous standards (Table 1).
The values of the Limit of Detection (LOD) were evaluated according to standard methods reported by Armbruster et al. (1994). The standard deviation (SD) and signal-to-noise ratio values of the blank solution were determined as 10, and the value was defined as LOD. The detection limits for the analysed potentially toxic metals are given in Table 2.
Diagnostic marker standardization values from Merck (Germany) were used for instrument calibration. In the study, deionized water was applied and crystalline pupils were systematically cleaned. Specialized Position Quantifiable (SRM-2711 for soil and SRM NIST 1577b for plant) assessments were performed to confirm the constancy of the results. The average recoveries of SRM for soil were 107%, 103%, 98%, 97%, 97%, 98% and 91% for Pb, Cu, Co, Mn, Cd, Cr, Zn and Fe, respectively, and the mean recoveries of SRM for spinach were 105%, 99%, 94%, 102%, 102%, 93%, and 95%, respectively.
One-way analysis of variance was used to evaluate the differences in metal values in irrigation areas using IBM SPSS 24 (Statistical Package for Social Sciences) (Dogan et al. 2011). The differences between the values were statistically tested at 0.05, 0.01 and 0.001 levels (Yorek et al. 2010; Ugulu and Erkol 2013; Ugulu et al. 2021a, b). In addition, the similarity/difference relationships regarding the metal values in the samples were evaluated by Hierarchical Clustering Analysis.
The bioconcentration factor (BCF) is an index used to evaluate the level of metal accumulation in plants. In this study, BCF values were calculated with the following formula:
While Cveg stands for metal values in plant tissues (mg/kg, dry weight), Csoil refers to metal concentration in soil (mg/kg, dry weight) (Khan et al. 2019a, b).
The pollution load index (PLI) aims to provide an estimate of the pollution state based on the value of the metal in the soil. The following formula was used in this study (Liu et al. 2005):
The reference values (mg/kg) of Cd (1.49), Cr (9.07), Cu (8.39), Fe (56.90), Ni (9.06), Zn (44.19) and Mn (46.75) for soil were taken according to Ugulu et al. (2021a, b, c, d, e).
Daily metal intake (DIM) is used to find health risks from food consumption. In this study, it was calculated with the following formula (Sajjad et al. 2009):
where Cmetal represents the value of metals ingrains, Dfood intake represents the daily food intake and Baverage weight represents average body weight. In the calculation, the average daily vegetable intake rate for adults is 0.345 kg/person/day and the average body weight is 55.9 kg (Wajid et al. 2020).
HRI was used in this study to calculate potentially toxic metal exposure that could occur if radish samples were consumed by humans. The HRI is calculated by taking the ratio of the daily metal intake (DIM) in food products to the oral reference dose (RfD) (Khan et al. 2020a, b):
The RfD values used in this study are 0.001, 0.04, 1.5, 0.04, 0.7, 0.02, 0.003, 0.3 and 0.04 mg/kg/day for Cd, Co, Cr, Cu, Fe, Ni, Pb, Zn and Mn, respectively (USEPA 1997).
Results and Discussion
In Pakistan, where agricultural production is an important economic sector, groundwater and wastewater from different sources are mixed in certain proportions and used in agricultural irrigation in the form of canal waters due to the scarcity of clean water (Wajid et al. 2020). The metal values in the groundwater and sugar industry wastewater samples used for irrigation purposes varied between 0.84 and 1.67, 0.08–0.22, 0.42–0.72, 0.45–0.85, 2.51–9.99, 1.21–1.92, 0.02–0.15, 1.82–9.98 and 0.64–0.91 mg/kg for Cd, Co, Cr, Cu, Fe, Ni, Pb, Zn and Mn, respectively (Fig. 1). The Fe and Zn concentrations for both samples were higher than other metals. According to statistical analysis, inter-sample values were not significant for Cd, Co, Cr, Cu, Mn, Ni and Pb (p > 0.05), but were statistically significant for Fe and Zn (Table 3). FAO, WHO, European Standard Guidelines (Chiroma et al. 2014) and USEPA (1997) set the maximum allowable limits for Cd, Co, Cr, Cu, Fe, Mn, Ni, Pb and Zn in water as 0.01, 0.05, 0.5, 0.2, 5, 0.2, 0.2, 0.065 and 2 mg/L, respectively. When these values were compared with the findings, potentially toxic metal values in this study were above the maximum allowable limits in water, except for Mn. This evaluation shows that the metal values in poor-quality water used for irrigation are higher than they should be and pose a risk of pollution (Ugulu et al. 2009). While this risk is of industrial origin for sugar industry wastewater, it can be caused by many sources such as urban runoff, soil erosion, vehicular traffic, industry and aerosol particles for groundwater (Ugulu et al. 2008; Wajid et al. 2020).
Wastewaters contain potentially toxic metals that can easily accumulate in the soil, easily pass from soil to vegetables and cause contamination (Wajid et al. 2020). In this study, it was determined that the metal values in soil samples irrigated with groundwater and sugar industry wastewater varied between 1.84 and 2.09, 0.66–0.74, 1.14–1.75, 1.56–2.16, 32.31–40.15, 0.57–0.84, 1.33–1.51, 0.32–0.38 and 0.35–0.78 mg/kg for Cd, Co, Cr, Cu, Fe, Mn, Ni, Pb, and Zn respectively (Fig. 2). While the effect of irrigation was insignificant on Cd, Ni, Zn, Fe, Cu, Mn and Cr values in soil samples, a significant effect was found for Pb and Co values (p < 0.05) (Table 4). However, the potentially toxic metal values were lower than the maximum allowable limits of Co (9.1), Cr (9.07), Cu (8.39), Fe (56.9), Mn (46.74), Ni (9.06), Pb (3.50), Zn (44.19) mg//kg (CSEPA 1995; Dutch Target and Intervention Values 2000; Singh et al. 2010), while Cd values were higher than the maximum allowable limit (1.49 mg/kg) (Singh et al. 2010). Similar results were reported for Cd above the allowable limit for different plant samples and locations, seasons, wastewater types and local environments, so the current study is in line with previous findings (Khan et al. 2021).
High potentially toxic metal concentrations in the habitat may result in higher translocation from soil to vegetables (Khan et al. 2021). In this study, the potentially toxic metal values in the spinach samples irrigated with groundwater and sugar industry wastewater varied between 1.59 and 1.84, 0.22–0.68, 0.56–1.14, 1.41–1.56, 1.62–3.23, 0.57–1.02, 0.86–1.33, 0.20–0.32 and 0.35–2.10 mg/kg for Cd, Co, Cr, Cu, Fe, Ni, Pb, Zn and Mn, respectively (Fig. 3). It was concluded that the difference between the metal values in the spinach samples according to the irrigation sources was statistically significant, except for Cu and Pb (p > 0.05) (Table 5). Current results for metals were below the maximum allowable limits reported by FAO/WHO (2001) for Co (50 mg/kg), Cr (2.3 mg/kg), Cu (73.3 mg/kg), Fe (425.5 mg/kg), Mn (500 mg/kg), Ni (67 mg/kg), Pb (0.3 mg/kg), Zn (99.4 mg/kg). However, Cd values in spinach samples were higher than the maximum allowable limit (0.2 mg/kg) reported by FAO/WHO (2001). Qadir et al. (2000) stated that the sources of Cd in environmental elements such as water, soil and plants are phosphate fertilizers, irrigation wastewater and wastes from industries. These sources support the high Cd values in the spinach samples in the study. However, according to a literature review conducted by Rai et al. (2019), the main route of transport of potentially toxic metals and other pollutants to crops in developing countries is irrigation with wastewater or sewage sludge.
Dendrogram for measured metals in the spinach samples according to Average Linkage cluster analysis revealed two main groups (Fig. 4). The first main group includes only Fe while the second main group includes the other 8 metals. Also, the second main group was divided into two subgroups with the first subgroup involving Cd, Cu and Zn, and the second subgroup involving the 5 metals. The second subgroup was further separated into two subgroups first of which contains only Pb and Co, and the second contains the remaining metals (Fig. 4). Ugulu et al (2021a, b, c, d, e), in a study on the effect of different organic fertilizers on potentially toxic metal accumulation in vegetables in Sargodha-Pakistan, determined that Fe and Zn accumulations were separated from other metals as a result of hierarchical cluster analysis. In this respect, the present study is similar to the findings and study area of Ugulu et al (2021a, b, c, d, e).
The bioconcentration factor can be used to express the bioavailability level of metals in the environment of a plant species (Ugulu et al. 2021c, d). In this study, the highest BCF value was found for Zn (2688) at Site 2 and the lowest for Fe (0.04) at Site 2 (Table 6). Zinc (Zn) is the second most common element in the structure of plants (Ugulu et al. 2021a, b, c, d, e). The high Zn concentration observed in plants can be attributed to the relative abundance of potentially toxic metals in the earth's crust in the upper layers of the soil (Zn > Cr > Pb > Ni > Cu > Cd) (Alloway 2013). However, long-term use of wastewater in agricultural irrigation may increase the content of Zn and other potentially toxic metals (Rattan et al. 2005). The high BCF values determined for Zn in this study support these findings. Jolly et al. (2013) also reported the higher bioconcentration factor of zinc observed in some vegetables. The BCF values determined for these vegetables are as follows: 0.263 (Raphanus sativus), 0.872 (Amaranthus caudatus), 0.189 (Solanum melongena) and 1.55 (Beta vulgaris). According to these findings, it can be said that leafy vegetables show higher BCF values among the vegetables examined.
In this study, the highest PLI value was observed for Fe (0.705) at Site 2 and the lowest PLI value for Mn (0.003) was observed at Site 1 (Table 6). An estimated PLI value of more than 1.0 indicates that the soil is contaminated with potentially toxic metals, while a value of less than 1.00 indicates that it is not contaminated (Khan et al. 2019a, b, c). PLI values of less than 1.0 determined for metals in this study showed that the land was not heavily contaminated with related potentially toxic metals (Khan et al. 2019a, b, c). Ugulu et al (2021a, b, c, d, e) investigated the effects of using organic wastes as fertilizer on potentially toxic metal accumulation in pepper in Sargodha city of Pakistan and reached the following PLI values for Cd, Co, Cr, Cu, Fe, Mn, Pb and Zn: 0.057–0.231, 0.049–0.638, 0.043–0.455, 0.081–0.700, 0.005–0.299, 0.105–0.511, 0.001–0.062 and 0.261–0.400, respectively. Except for Cd, the PLI values obtained in this study were lower than the values in the related study. In addition, the Zn, Fe, Cd, Co and Mn PLI values obtained in this study are lower than the values determined for contaminated vegetables from the wastewater irrigated areas of Varanasi, India (Singh et al. 2010).
The highest DIM value was 1.67 mg/kg/day for Zn at Site 2, and the lowest value was 0.0003 mg/kg/day for Pb at Site 1 (Table 7). WHO (1996), FAO/WHO (2001) and EFSA (2013) reported tolerable daily metal intake values of 0.0007, 0.0005, 0.3, 0.023, 0.43 and 0.8 mg/kg for Cd, Pb, Cr, Co, Zn and Fe. The DIM values of Cd, Pb, and Fe for both sites and the Co (Site 1) and Zn (Site 2) were higher than these tolerable values. Khan et al. (2008) obtained DIM values of 0.032, 0.008, 0.002, 0.0003, 0.005 and 0.005 for Zn, Cu, Pb, Cd, Cr, and Ni, respectively, in S. oleracea samples irrigated with wastewater in Beijing China. The current DIM values are higher than those obtained by Khan et al. (2008). The differences between the results may vary according to the wastewater content and characteristics, as well as the characteristics of the region and the facility.
The highest HRI value was found to be 196.8 for Cd at Site 1 and the lowest value to 0.006 for Co and Cr at Site 2 (Table 7). Increasing the use of wastewater for irrigation is a very important factor that increases metal accumulation in the soil and plants, causes an increase in the uptake of metals to the vegetative parts of plants and causes health risks (Nawaz et al. 2021). According to the results of this study, there is no health risk for Pb, Co and Cr with HRI values below 1.0, while there is a risk for Cd, Cu, Fe, Ni, Mn and Zn. The much higher HRI values of Cd than 1 (196.8 and 169.6) suggested that this metal is likely to cause significant health problems in the region. Cadmium (Cd) is defined as a very risky carcinogen for humans. It is also a potent and multi-tissue carcinogen for animals (Ugulu et al. 2019a, b). For this reason, it is thought that new studies on the health risks arising from metals and bioremediation in the region will be beneficial.
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Ugulu, I., Bibi, S., Khan, Z.I. et al. Potentially Toxic Metal Accumulation in Spinach (Spinacia oleracea L.) Irrigated with Industrial Wastewater and Health Risk Assessment from Consumption. Bull Environ Contam Toxicol 109, 1117–1125 (2022). https://doi.org/10.1007/s00128-022-03606-3
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DOI: https://doi.org/10.1007/s00128-022-03606-3