Ecological risk assessment of heavy metals in vegetables irrigated with groundwater and wastewater: The particular case of Sahiwal district in Pakistan

Agricultural Water Management 226 (2019) 105816

Contents lists available at ScienceDirect

Agricultural Water Management journal homepage: www.elsevier.com/locate/agwat

Ecological risk assessment of heavy metals in vegetables irrigated with groundwater and wastewater: The particular case of Sahiwal district in Pakistan

T

Khalil ur Rehmana, Syed Mohsin Bukharib, Shahla Andleeba, , Adeel Mahmooda, Kehinde O. Erinlec, Mian Muhammad Naeemd, Qaiser Imrane ⁎

a

Department of Environmental Science Government College, Women University, Sialkot 51300, Pakistan Department of Wildlife and Ecology, Faculty of Fisheries & Wildlife, University of Veterinary and Animal Sciences, Lahore, Pakistan School of Agriculture, Food and Wine, The University of Adelaide, SA 5005, Australia d Department of Civil Engineering, NFC Institute of Engineering & Fertilizer Research, Faisalabad, Pakistan e Department of Environmental Science, Zhejiang 310058, China b c

ARTICLE INFO

ABSTRACT

Keywords: Daily intake of metals Human health Lahore Metal accumulation Risk assessment Vegetables

The use of wastewater for irrigation is a common practice in the developing world. It is a major route of heavy metal contamination in vegetables. The groundwater, an alternative source for irrigation, is under threat of heavy metal contamination due to long-term use of wastewater. The present study investigated heavy metals contamination from irrigation with wastewater compared to groundwater in District Sahiwal situated in the vicinity of Lahore, Pakistan. Irrigated water, soil and vegetables were analyzed for Iron, Nickel, Lead, copper, Cadmium, Manganese and Zinc; Metal transfer factor (MTF); daily intake of metals (DIM) and health risk index (HRI) were calculated. Manganese (Mn) and Cd in wastewater irrigated soil, Pb, Cd, Mn and Fe in wastewaterirrigated vegetables and Pb, Mn and Fe in groundwater-irrigated vegetables exceeded the permissible limits (WHO, 1996), particularly in Mustard and Spinach. Generally, MTF was higher in wastewater than groundwaterirrigated vegetables, particularly with Fe followed by Ni. HRI was higher for wastewater-irrigated than groundwater-irrigated vegetables. Wastewater-irrigated Mustard and Spinach showed a HRI > 1 only for Mn. Quality control mechanisms need to be applied for long-term use of groundwater. Also, treatment of wastewater prior to application to plants must be considered to save crops from contamination.

1. Introduction Water is the basis of life on earth. It is the main component of the environment and an essential element to human life (Shiklomanov, 2000). According to the OECD (2012), water demand is projected to increase by 55% globally between 2000 and 2050, with about +130% being from domestic uses. Further, about 40% of the world's population living in the river basin has been predicted to undergo severe drought by year 2050 (OECD, 2012). Agriculture accounts for about 70% of global freshwater use, and food production will need to grow by 69% by 2035 to feed the growing population (FAO, 2016a,b). Severe water scarcity levels appear to prevail in regions with either high population density or the presence of much irrigated agriculture, or both: Pakistan is included in the list of countries with severe water scarcity during more than half of the year (Mekonnen and Hoekstra, 2016).

⁎

Under the changing climate, sustainable water use in agricultural and domestic sectors face severe challenges, particularly in arid regions like Pakistan. As noted by Amin et al. (2018), Pakistan has moved from a water-stressed country to a water-scarce country. This has made farmers with farmlands around wastewater drainages to use wastewater as alternative source for irrigation. For example, in vicinity of Lahore district, Pakistan, the use of wastewater is a common practice among urban and peri-urban farmers (Mahmood and Malik, 2014). Lahore, a metropolitan city and business mart of Pakistan, is home for about 1120 unplanned industries, which include steel rolling factories, textile industries, leather tanneries, electroplating miles, pigment factories, etc. (Saleemi, 1990). According to Saleemi (1990), about 1350 million liters of wastewater is generated per day from these companies along with municipal wastes that is discharged into the Ravi River. Local farmers across this region use the surface wastewater to irrigate their farms due

Corresponding author. E-mail address: [email protected] (S. Andleeb).

https://doi.org/10.1016/j.agwat.2019.105816 Received 10 June 2019; Received in revised form 19 September 2019; Accepted 22 September 2019 0378-3774/ © 2019 Elsevier B.V. All rights reserved.

Agricultural Water Management 226 (2019) 105816

K. ur Rehman, et al.

to easy access and scarcity of fresh water (Hossain et al., 2015 However, irrigation with wastewater significantly contribute to accumulation of inorganic and organic contaminants in the soil (Arora et al., 2008), and hence uptake in irrigated plants (Singh et al., 2004). No doubt wastewater irrigational practices decreased the stress on freshwater use but added significant impacts on human health directly and indirectly (Cao et al., 2018). Heavy metals taken by plants are not only harmful to plants but also caused serious impacts on human health (Cao et al., 2016). Heavy metals are non-biodegradable, have long biological halflife, and are able to accumulate in different parts of the plants. Even when ingested in low concentration, heavy metals are extremely toxic to both humans and animals. Groundwater is usually considered an invaluable renewable natural resource in the semi-arid and arid regions, because of its reliability in quantity and quality (Asare-Donkor et al., 2016). It has become the most preferred source of sustainable water supply to meet agricultural needs in rural and urban settings (Anim-Gyampo et al., 2019). Despite the general positive thoughts about groundwater, it is still vulnerable to contaminations due to different anthropogenic activities overtime (Anim-Gyampo et al., 2019). For example, several authors have reported the increase in groundwater contamination due to increased use of wastewater for irrigation (Jampani et al., 2018). Dominant contaminants in the groundwater of wastewater irrigated farms include organic and inorganic chemical compounds (nitrates, phosphates, organochloro-pesticides, heavy metals, etc.) and microbial contaminants (Ascaris spp., Giardia spp., E. coli and other coliform bacteria, etc.) (Amerasinghe et al., 2009; Gallegos et al., 1999). In Lahore, Pakistan, groundwater contamination due to improper disposals of industrial effluents and the subsequent implications are of greatest concern to the government (Abbas et al., 2018, 2015). Such effects, if not rapidly regulated, could result in serious quality degradation and further reduce the use of groundwater for urban supply and agricultural use (Trabelsi and Zouari, 2019). Therefore, the objectives of present study were to (1) determine the heavy metal concentrations in soils, water and vegetable crops collected from different wastewater- and groundwater-irrigated fields; (2) determine daily intake of heavy metals through the consumption of vegetables for adult populations; and (3) evaluate human health risk associated with food chain contamination of heavy metals routing from irrigation with wastewater compared to groundwater.

conductivity of 0.7–9 dS/m. Soil sample of about 500 g was randomly collected from each sub-site of all selected zones. All samples were collected in triplets to minimize the experimental error. Soil samples were collected by digging out a monolith of 10 × 10 × 15 cm3 and preserved in labelled plastic bags. Non-soil material like wooden pieces, rocks, gravels and organic debris were removed manually. Groundwater and wastewater samples were collected from each sub-site, filtered and stored in labeled 1 l plastic bottle, which were previously soaked in 10% HNO3 for 24 h and washed with de-ionized water to remove toxicity prior to sample storage. Water samples were preserved at 4 °C for further analyses (American Public Health Association, 2005). Six replicates of vegetables collected from each subsite are Mustard leaf (Spinacia oleracea L.), Carrot (Daucus carota L.), Turnip (Brassica rapa L.), Cabbage (Brassica oleracea var. capitata), Spinach (Spinacia oleracea L.), and cauliflower (Brassica oleracea). Vegetable samples were transferred to the laboratory, where they were washed with distilled water, oven dried (130 °F) and preserved for further analysis. 2.3. Heavy metal analyses One gram of each vegetable type or soil samples was digested by adding 15 ml of tri-acid mixture (HNO3, H2SO4, and HClO4 in 5:1:1 ratio) at a temperature of 80 °C until a clear solution was obtained (APHA, 2005). Filtration of digested samples was done with Whatman No. #42 filter paper. The filtrate was maintained up to 50 ml by adding distilled water. 10 ml concentrated HNO3 was used to digest the 50 ml water sample at 80 °C until a clear solution was obtained (APHA, 2005). The solution was further filtered with Whatman No. #42 filter paper and distilled water was added to maintain the 50 ml total volume. 2.4. Analysis of heavy metals Heavy metal concentrations in the vegetable and soil filtrates obtained above and the water samples (groundwater and wastewater) was detected using atomic absorption spectrophotometer (UVAS, Lahore). Atomic absorption spectrophotometer was calibrated manually. A standard solution of respective heavy metals as well as drift blanks was used for calibration (APHA, 2005). 2.5. Reagents

2. Materials and methodology

Analytical grade chemicals were purchased and used for sample preparation and analyses. Solutions were prepared in distilled water. For each metal calibration, standards were prepared from the stock solution (Fig. 1).

2.1. Study site description Sahiwal (31° 58’ 23’’ North, 72° 19’ 32’’ East) is the 14th major city in the province of Punjab, situated about 83 km from the provincial capital of Lahore. The city is in the heavily populated area between the Ravi and Sutlej rivers, with major cultivated crops including cotton, wheat, oil seeds and potato. According to a reconnaissance survey conducted in the peri-urban sites, vegetables and fodder crops grown on nearby agricultural lands are usually irrigated with wastewater generated from various urban activates (sewage and industrial) (Ashfaq et al., 2015) or water from the underlying unconfined aquifer (groundwater) sourced from the Ravi river (Basharat, 2012). For this study, two main sampling zones (wastewater or groundwater irrigation) were investigated according to our earlier survey of Sahiwal. Selected farms were irrigated with wastewater or groundwater for over 20 years. To fulfil the purpose of the study, three sites were selected from each zone and each site was further divided into three sub-sites. Soil, water and vegetables samples were collected from each site using the methods described by American Public Health Association (APHA, 2005).

2.6. Data analysis 2.6.1. Daily intake of metals (DIM) Following equation was used to measure Daily Intake of Metals (Chary et al., 2008). DIM = (Cmetal × Cfactor × Dfood

intake)/Baverage weight

Where, Cmetal, Cfactor, Dfood intake and Baverage weight represent the heavy metal concentrations in plants (mg/kg), conversion factor, daily intake of vegetables and average body weight, respectively. Fresh to dry weight conversion factor (0.085) was used for these vegetables (Mahmood and Malik, 2014). The average daily vegetables intake (300 mg person−1 day−1) from 200 adults with average body weight of 50 kg was used in the calculation.

2.2. Sample collection

2.6.2. Risk assessment The health risk indices (HRIs) for heavy metal intake through the consumption of contaminated vegetables were calculated using the

The composite soil has pH within 7.6–8.27 and electrical 2

Agricultural Water Management 226 (2019) 105816

K. ur Rehman, et al.

Fig. 1. Location map of the sample collection points in the polluted area.

following equation adopted from Cui et al. (2004). Hazard indices must be < 1 in order for it not to pose any health hazards. When the hazard index values > 1, there may be concerns for potential health risks associated with over exposure (USEPA, 2006).

3. Results 3.1. Heavy metal concentration in soil and water (ground and waste) samples

HRI = DIM/RfD

Heavy metals were higher in wastewater than in groundwater samples. In the groundwater samples, the concentrations of heavy metals ranged from < 0.01 to 1.10 mg kg−1, with Pb having the highest mean concentration (0.63 ± 0.28 mg L−1) and lowest mean concentration in Cu and Cd concentrations (< 0.01 mg L−1) (Table 2). Total concentration of heavy metals detected in the groundwater was lower than the WHO permissible levels. In the wastewater samples, the concentrations of heavy metals ranged from 0.02 to 33.00 mg L−1, with Mn having the highest mean concentration (28 ± 9 mg L−1) and lowest mean concentration in Ni (0.06 ± 0.01 mg L−1). Total concentration of heavy metals detected in the wastewater was lower than the WHO permissible levels, except it was a bit higher with Cd (0.15 ± 0.10 mg L−1), and multiple folds higher with Mn (Table 2). In soil irrigated with groundwater, the concentrations of heavy metals ranged from < 0.01 to 45 mg kg−1, with Mn having the highest mean concentration (32 ± 6 mg kg−1) and lowest mean concentration in Cd (< 0.01 mg kg−1). In soil irrigated with wastewater, the

Where HRI represented daily intake of heavy metals (DIM; mg metal kg−1 body weight day−1) and reference oral dose (RfD), respectively. 2.6.3. Metal transfer factor (MTF) Soil to plant metal transfer factor (MTF) was computed as the ratio of metal concentrations in plants (Cplant; dry weight basis) to metal concentrations in soil (Csoil). The MTF was calculated using the following equation (Mirecki et al., 2015): MTF = Cplant/Csoil 2.6.4. Statistical analysis The data were statistically analyzed using SPSS version 12. Descriptive statistics were applied to compare with set standards (Table 1). Table 1 Description of vegetables examined in this study. Local name

English name

Part sampled

Family

Plant species

Saag Gajr Shaljum Band Gobi Paalak Phool Gobi

Mustard Carrot Turnip Cabbage Spinach Cauliflower

Leaves Underground stem Underground stem Leaves Leaves Fruiting flower

Amaranthaceae Apiaceae Brassicaceae Brassicaceae Amaranthaceae Brassicaceae

Spinacia oleracea L. Daucus carota L. Brassica rapa L. Brassica oleracea capitata Spinacia oleracea L. Brassica oleracea

3

Agricultural Water Management 226 (2019) 105816

K. ur Rehman, et al.

Table 2 Mean values of heavy metals concentrations in water (mg L−1) and soil (mg kg−1) irrigated with different water sources. Heavy Metals

Groundwater

Wastewater

Range

Value (Mean ± SD)

Range

Value (Mean ± SD)

Water Pb Cd Cu Zn Mn Ni Fe

0.18–1.10 < 0.01 < 0.01 0.01–0.15 0.01–0.02 0.01–0.03 0.01–0.02

0.63 ± 0.28 0.002 ± 0.002 0.001 ± 0.000 0.07 ± 0.04 0.01 ± 0.004 0.02 ± 0.01 0.03 ± 0.03

1.00–1.69 0.02–0.39 0.02–0.35 0.34–1.85 13–43 0.04–0.09 11.50–33.00

1.35 ± 0.20 0.15 ± 0.10 0.12 ± 0.09 1.09 ± 0.54 28 ± 9 0.06 ± 0.01 23 ± 6

5 0.1 0.2 2 0.2 0.2 Not Listed

Soil Pb Cd Cu Zn Mn Ni Fe

0.80–2.20 < 0.01 0.01–0.09 0.10–0.90 23–45 0.06–0.15 2–11

1.48 ± 0.50 0.003 ± 0.001 0.04 ± 0.02 0.49 ± 0.23 32 ± 6 0.09 ± 0.02 7.00 ± 2.90

1.39–4.51 0.01–0.03 0.41–1.25 5.42–9.50 23–191 0.27–0.36 11–36

2.94 ± 0.94 0.01 ± 0.01 0.89 ± 0.27 7.05 ± 1.18 89 ± 63 0.30 ± 0.02 23 ± 8

84 3 140 300 80 75 NL

Table 4 Transfer factor (MTF) of heavy metals in vegetables grown with groundwater and wastewater.

Standard (WHO)

Vegetables

Pb

Cd

Cu

Zn

Mn

Ni

Fe

Groundwater Mustard Carrot Turnip Cabbage Spinach Cauliflower

0.050 0.010 0.015 0.014 0.199 0.016

0.816 0.238 0.316 0.266 0.908 0.280

0.467 0.151 0.070 0.115 0.460 0.122

0.231 0.008 0.011 0.069 0.197 0.136

0.665 0.143 0.164 0.092 0.614 0.327

3.333 1.544 0.421 1.298 2.912 0.674

12.028 2.689 4.292 2.170 10.142 6.792

Wastewater Mustard Carrot Turnip Cabbage Spinach Cauliflower

0.759 0.507 0.437 0.616 0.910 0.470

5.036 0.597 0.958 0.667 2.396 0.366

0.979 0.695 0.206 0.508 0.979 0.561

0.329 0.088 0.065 0.070 0.265 0.086

0.775 0.294 0.320 0.250 0.832 0.395

6.093 2.522 1.537 1.818 5.314 1.310

15.876 6.523 7.213 6.724 12.055 7.342

0.02 ± 0.005 mg kg−1; 0.09 ± 0.03 mg kg−1; 20 ± 2 181 mg kg−1 and 71 ± 3 mg kg−1) and Mustard leaf (0.006 ± 0.002 mg kg−1; −1 0.02 ± 0.01 mg kg ; 0.11 ± 0.01 mg kg−1; 21 ± 3 mg kg−1 and 85 ± 7 mg kg−1), but only Mn was higher than the WHO standard (16.61 mg kg−1). Ni was highest in Turnip (0.80 ± 0.10 mg g−1), but was much lower than the WHO standard (10 mg kg−1). Among the vegetables irrigated with wastewater, highest mean heavy metals concentrations were found in Spinach and Mustard leaf. In both vegetables, 186 Pb was about 40-fold higher (2.68 ± 0.39 mg kg−1 and 2.23 ± 0.21 mg kg−1), Cd (0.08 ± 0.009 mg kg−1 and 0.09 ± 0.005 mg kg−1) and Mn (74 ± 14 mg kg−1 and 69 ± 18 mg kg−1) were about four-fold higher than the WHO standard (0.02 mg kg−1 and 16.61 mg kg−1).

concentrations of heavy metals ranged from 0.01 to 191 mg kg−1, with Mn having the highest mean concentration (89 ± 63 mg kg−1) and lowest mean concentration in Cd (0.01 ± 0.01 mg kg−1). Total concentration of heavy metals detected in the irrigated soils was lower than the WHO permissible levels, except it was higher with Mn. 3.2. Measurement of heavy metal in vegetables Heavy metal accumulations were higher in vegetables irrigated with wastewater than with groundwater (Table 3). Among the vegetables irrigated with groundwater, highest mean concentration of Pb was found in Spinach (0.296 ± 0.394 mg kg−1) and was about four-fold higher than the WHO standard (0.05 mg kg−1). Highest mean concentrations of Cd, Cu, Zn, Mn and Fe 180 were found in Spinach (0.007 ± 0.001 mg kg−1;

3.3. Heavy metals transfer factor from soil to vegetables Heavy metal transfer factor (MTF) was higher in vegetables irrigated with wastewater than with groundwater, and was highest for Fe than other metals (Table 4). Among the vegetables irrigated with groundwater, heavy metal transfer factor was highest with Spinach and

Table 3 Comparison of mean ± standard deviation (SD) of heavy metals concentration (mg kg−1) in vegetables grown with groundwater and wastewater. Vegetables Groundwater Mustard Carrot Turnip Cabbage Spinach Cauliflower Wastewater Mustard Carrot Turnip Cabbage Spinach Cauliflower Standard

Value Mean ± Range Mean ± Range Mean ± Range Mean ± Range Mean ± Range Mean ± Range Mean ± Range Mean ± Range Mean ± Range Mean ± Range Mean ± Range Mean ± Range WHO

SD SD SD SD SD SD

SD SD SD SD SD SD

Pb

Cd

Cu

Zn

Mn

Ni

Fe

0.074 ± 0.006 0.069–0.080 0.015 ± 0.005 0.010–0.020 0.022 ± 0.003 0.019–0.025 0.021 ± 0.008 0.016–0.030 0.296 ± 0.394 0.063–0.750 0.023 ± 0.006 0.017–0.028

0.006 ± 0.002 0.004–0.008 0.002 ± 0.00 0.001–0.002 0.002 ± 0.001 0.002–0.003 0.002 ± 0.001 0.001–0.003 0.007 ± 0.001 0.006–0.007 0.002 ± 0.001 0.001–0.003

0.02 ± 0.01 0.010–0.03 0.007 ± 0.002 0.005–0.009 0.003 ± 0.002 0.001–0.005 0.005 ± 0.003 0.003–0.009 0.02 ± 0.005 0.018–0.027 0.006 ± 0.003 0.002–0.008

0.11 ± 0.01 0.10–0.13 0.004 ± 0.003 0.001–0.006 0.005 ± 0.002 0.004–0.007 0.03 ± 0.01 0.02–0.05 0.09 ± 0.03 0.06–0.13 0.06 ± 0.01 0.05–0.08

21 ± 3 19–25 4±2 3–7 5±2 3–7 3±2 1–6 20 ± 2 18–23 10 ± 3 8–14

0.31 ± 0.03 0.29–0.35 0.14 ± 0.04 0.11–0.19 0.80 ± 0.10 0.70–0.90 0.12 ± 0.02 0.10–0.14 0.27 ± 0.07 0.22–0.36 0.06 ± 0.04 0.01–0.10

85 ± 7 77–91 19 ± 4 15–23 30 ± 5 25–35 15 ± 4 11–19 71 ± 3 69–75 48 ± 4 43–52

2.23 ± 0.21 1.99–2.37 1.49 ± 0.32 1.12–1.70 1.28 ± 0.09 1.23–1.39 1.81 ± 0.15 1.63–1.92 2.68 ± 0.39 2.23–2.92 1.38 ± 0.11 1.29–1.51 0.05

0.09 ± 0.005 0.08–0.09 0.05 ± 0.01 0.04–0.06 0.05 ± 0.02 0.023–0.07 0.03 ± 0.02 0.01–0.06 0.08 ± 0.009 0.08–0.09 0.03 ± 0.01 0.02–0.05 0.02

0.87 ± 0.08 0.79–0.95 0.62 ± 0.07 0.54–0.69 0.18 ± 0.13 0.03–0.29 0.45 ± 0.04 0.43–0.50 0.87 ± 0.09 0.81–0.98 0.50 ± 0.09 0.40–0.59 40

2.3 ± 0.4 1.98–2.89 0.6 ± 0.2 0.33–0.91 0.4 ± 0.06 0.41–0.53 0.4 ± 0.3 0.15–0.70 1.8 ± 0.2 1.65–2.10 0.6 ± 0.2 0.39–0.79 50

69 ± 18 55–90 26 ± 6 19–31 28 ± 4 24–33 22 ± 4 19–27 74 ± 14 62–90 35 ± 6 28–41 16.61

1.8 ± 0.1 1.78–2.05 0.7 ± 0.09 0.68–0.87 0.4 ± 0.1 0.35–0.59 0.5 ± 0.07 0.49–0.64 1.6 ± 0.08 1.55–1.71 0.4 ± 0.1 0.31–0.51 10

368 ± 40 325–405 151 ± 46 124–205 167 ± 39 124–201 156 ± 39 123–200 279 ± 26 250–300 170 ± 24 143–189 45

4

Agricultural Water Management 226 (2019) 105816

K. ur Rehman, et al.

Table 5 Daily intake of metals (DIM; mg person −1 day−1) from vegetables grown with groundwater and wastewater. Vegetables

Pb

Cd

Cu

Zn

Mn

Ni

Fe

Groundwater Mustard Carrot Turnip Cabbage Spinach Cauliflower

3.80E-05 8.00E-06 1.10E-05 1.10E-05 1.51E-04 1.20E-05

4.00E-06 3.00E-06 1.00E-06 1.00E-06 1.00E-06 3.00E-06

1.10E-05 4.00E-06 2.00E-06 3.00E-06 1.10E-05 3.00E-06

5.80E-05 2.00E-06 3.00E-06 1.80E-05 5.00E-05 3.40E-05

1.11E-02 2.38E-03 2.72E-03 1.53E-03 1.02E-02 5.44E-03

1.62E-04 7.50E-05 4.08E-04 6.30E-05 1.41E-04 3.30E-05

4.34E-02 9.69E-03 1.55E-02 7.82E-03 3.66E-02 2.45E-02

Wastewater Mustard Carrot Turnip Cabbage Spinach Cauliflower

1.14E-03 7.62E-04 6.56E-04 9.25E-04 1.37E-03 7.06E-04

4.70E-05 2.80E-05 2.70E-05 1.80E-05 4.30E-05 1.60E-05

4.45E-04 3.16E-04 9.40E-05 2.31E-04 4.45E-04 2.55E-04

1.19E-03 3.19E-04 2.33E-04 2.52E-04 9.52E-04 3.11E-04

3.54E-02 1.34E-02 1.46E-02 1.14E-02 3.80E-02 1.80E-02

9.58E-04 3.97E-04 2.42E-04 2.86E-04 8.35E-04 2.06E-04

1.88E-01 7.72E-02 8.53E-02 7.96E-02 1.43E-01 8.69E-02

Mustard leaf. In Spinach, the MTF was in the order Fe (10.142) > Ni (2.912) > Cd (0.908) > Mn (0.614) > Cu (0.460) > Pb (0.199) = Zn (0.197). In Mustard leaf, the MTF was in the order Fe (12.028) > Ni (3.333) > Cd (0.816) > Mn (0.665) > Cu (0.467) > Zn (0.231) > Pb (0.050). Among the vegetables irrigated with wastewater, heavy metal transfer factor was highest with Spinach and Mustard leaf. In Spinach, the MTF was in the order Fe (12.055) > Ni (5.314) > Cd (2.396) > Cu (0.979) > Pb (0.910) > Mn (0.832) > Zn (0.265). In Mustard leaf, the MTF was in the order Fe (15.876) > Ni (6.093) > Cd (5.036) > Cu (0.979) > Mn (0.775) > Pb (0.759) > Zn (0.329).

Table 6 Health risk index (HRI) for heavy metals (mg/kg) in vegetables grown with groundwater and wastewater.

3.4. DIM and HRI of heavy metals Values for the daily intake of metals (DIM; mg person−1 day−1) were generally higher for vegetables irrigated with wastewater than vegetables irrigated with groundwater (Table 5). Among vegetables irrigated with groundwater, the highest DIM (4.34E-02) was found for Fe in Mustard leaf followed by in Spinach (3.66E-02). Daily intake of metal for Cd, Cu, Zn, Mn, and Fe was highest in Mustard leaf followed by in Spinach (Pb, Cu, Zn, Mn, and Fe). The trend for DIM in Mustard leaf grown with groundwater was in the order of Fe (4.34E-02) > Mn (1.11E-02) > Ni (1.62E-04) > Zn (5.80E-05) > Pb (3.80E-05) > Cu (1.10E-05) > Cd (4.00E-06), and for Spinach was in the order of Fe (3.66E-02) > Mn (1.02E-02) > Pb (1.51E-04) > Ni (1.41E04) > Zn (5.00E-05) > Cu (1.10E-05) > Cd (1.00E-06). Among vegetables irrigated with wastewater, the highest DIM (1.88E-01) was found for Fe in Mustard leaf followed by in Spinach (1.43E-01). Daily intake of all the heavy metals was highest in Mustard leaf followed by in Spinach, except Zn in Spinach. The trend for DIM in Mustard leaf grown with wastewater was in the order of Fe (1.88E-01) > Mn (3.54E-02) > Zn (1.19E-03) > Pb (1.14E-03) > Ni (9.58E-04) > Cu (4.45E-04) > Cd (4.70E-05), and for Spinach was in the order of Fe (1.43E-01) > Mn (3.80E-02) > Pb (1.37E-03) > Zn (9.52E04) > Ni (8.35E-04) > Cu (4.45E-04) > Cd (4.30E-05). The health risk index (HRI) for heavy metals by consumption of vegetables irrigated with wastewater was generally greater than those irrigated with groundwater (Table 6). Among vegetables irrigated with groundwater, the highest HRI was found for Mn in Mustard (0.335) and Spinach (0.309), but were less than 1. Among vegetables irrigated with wastewater, the highest HRI was found for Mn in Mustard (1.072) and Spinach (1.150), and were greater than 1.

Vegetables

Pb

Cd

Cu

Zn

Mn

Ni

Fe

Groundwater Mustard Carrot Turnip Cabbage Spinach Cauliflower

0.010 0.002 0.003 0.003 0.038 0.003

0.000 0.000 0.000 0.000 0.000 0.000

0.000 0.000 0.000 0.000 0.000 0.000

0.000 0.000 0.000 0.000 0.000 0.000

0.335 0.072 0.082 0.046 0.309 0.165

0.008 0.004 0.020 0.003 0.007 0.002

0.062 0.014 0.022 0.011 0.052 0.035

Wastewater Mustard Carrot Turnip Cabbage Spinach Cauliflower

0.285 0.190 0.164 0.231 0.342 0.176

0.001 0.001 0.001 0.001 0.001 0.001

0.011 0.008 0.002 0.006 0.011 0.006

0.004 0.001 0.001 0.001 0.003 0.001

1.072 0.407 0.443 0.345 1.150 0.546

0.048 0.020 0.012 0.014 0.042 0.010

0.268 0.110 0.122 0.114 0.204 0.124

were below the WHO standard (WHO, 1996), except Cd and Mn that were higher. Water is a critical and limiting resource for sustained agricultural development (FAO, 2016a,b), particularly in Pakistan, located in the arid region. Wastewater irrigation is common among farmers who have farmlands near wastewater canals, due to scarcity and poor access to quality water for irrigation. In Lahore, where this study was carried out, 1350 million liters of wastewater is generated per day (Saleemi, 1990) that drains into the Ravi River through the city drainages, managed by the Water and Sanitation Agency (WASA), Lahore. Industrial and municipal sewage are discharged into these drainages, which are the main route of heavy metal accumulation in the wastewater (Mahmood and Malik, 2014; Wozniak and Huang, 1982). Groundwater has become the most preferred source of sustainable water supply to meet agricultural needs in rural and urban settings (Anim-Gyampo et al., 2019). However, in Pakistan, groundwater contamination and the subsequent implications are of greatest concern to the government (Abbas et al., 2018, 2015). Results from the present study show that heavy metals were detected in groundwater in the Sahiwal district, though at the moment concentrations are under permissible limits recommended by world health organization (World Health Organization, 1996). Previous studies conducted in Lahore district, nearby of Sahiwal district, reported higher concentrations of heavy metals in groundwater. The contamination was attributed to leaching of heavy metals from nearby wastewater canals or dumping sites (Abbas et al., 2018; Aiman et al., 2016). Same wastewater collection system is bedded in Sahiwal district; hence, suggesting the possibility of groundwater contamination by heavy metals sourced from the wastewater channels, as noted in this study. Therefore, necessary control measures are needed to be put in place, in order to disallow the

4. Discussion 4.1. Content of heavy metals in different water sources and soil In the present study, the heavy metal concentrations in wastewater 5

Agricultural Water Management 226 (2019) 105816

K. ur Rehman, et al.

concentration of heavy metals in ground water to rise beyond allowable limits. Since groundwater is a major source of drinking water for the nearby populace, this could lead to heavy metal poisoning for the entire surrounding communities. In order to achieve the goal of preserving the quality of groundwater in Lahore, there could be the need to efficiently treat the surface wastewater thus reducing the concentration of contaminants that is leached to the groundwater aquifer. Different methods have been employed for the treatment of wastewater in agricultural system. For example, Wu et al. (2005) has reported the use of raw and modified diatomite for advanced treatment of wastewater. Petala et al. (2006) also reported an advanced wastewater treatment system, which consists of a moving-bed sand filter, a granular activated carbon adsorption bed and ozone disinfection. The use of ultrafiltration methods using hollow-fiber and polysulfone membranes have also been reported by Tchobanoglous et al. (1998). A natural-based treatment method for wastewater in vegetable irrigation, named extensive tertiary treatment system, has also been described (Licciardello et al., 2018). The use of tertiary or advanced treatment of wastewater is regarded as the maximum level of cleaning treatment used for wastewater recovery, which is focused on the removal of (biological and chemical) contaminants ensuring fruit/ vegetable quality and safety (Nicolás et al., 2016; Pedrero et al., 2012, 2014; Petousi et al., 2015; Wu et al., 2005). Tertiary treated wastewater can be additional water resource for irrigation in water-scarce Mediterranean environments (Petousi et al., 2015).

et al. (2007). In wastewater irrigated vegetables, only Pb had DIM values higher than the recommended daily intake (Harmanescu et al., 2011). DIM values in this study are generally lower than those reported in vegetables grown in old mining areas in Romania (Harmanescu et al., 2011). In our study, DIM values for Ni were lower, but DIM values for Pb were higher than reported in vegetables grown at a wastewaterirrigated site in Dhaka, Bangladesh (Hossain et al., 2015). Consumption of heavy metal contaminated vegetables can potentially cause damage to kidney, brain, developing fetus, and liver (Alloway, 1990; Sharma et al., 2016; Zhou et al., 2016). Gandhi and Kumar (2004) showed that consumption of heavy metal contaminated water and foods increased DNA damage in recipients. The health risk index (HRI) must be < 1 in order for it not to pose any health hazards; when HRI is > 1, there may be concerns for potential health risks associated with over exposure (USEPA, 2006). HRI for heavy metals in vegetables irrigated with wastewater was higher than in vegetables irrigated with groundwater. Generally, the HRI for heavy metals in groundwater irrigated vegetables was < 1, this indicates that the vegetables were almost safe for consumption. Though the HRI for heavy metals in wastewater irrigated vegetables were mostly < 1, Mustard and Spinach showed a HRI > 1 for Mn, suggesting a possibility of exposure to Mn toxicity in consumers. Manganese, while essential to human health, toxicity could be associated with devastating neurologic impairment clinically known as “manganism,” a motor syndrome similar to, but partially distinguishable from idiopathic Parkinson’s disease (IPD) (Kwakye et al., 2015; Olanow, 2004). Symptoms of Mn toxicity, once established, are usually irreversible, showing a permanent damage to the neurologic structures (WHO, 2004; Zheng et al., 2011).

4.2. Content of heavy metals in vegetables irrigated with different water resources The accumulation of heavy metals in vegetables is a major cause of public health (Zhou et al., 2016). In our study, heavy metal concentrations were higher in wastewater-irrigated than in groundwaterirrigated vegetables. However, Fe was the most accumulated, followed by Mn. Compared to the WHO allowable limits (WHO, 1996), concentrations of Pb, Cd, Mn and Fe were higher in wastewater-irrigated vegetables, while concentrations of Pb, Mn and Fe were higher in groundwater-irrigated vegetables, particularly in Mustard leaf and Spinach. Similar finding was also reported by Mahmood and Malik (2014), who found higher Pb and Cd in vegetables cultivated with wastewater beyond the European Union Standards. Khan et al. (2018) also found higher heavy metal contamination in wheat cultivated with wastewater in Sahiwal, Pakistan. Among the vegetables irrigated with groundwater or wastewater, heavy metal concentrations were highest in Mustard and Spinach. The higher heavy metal concentrations may be due to translocation of metals from the contaminated soil into the vegetables. This corroborates the results of metal transfer factor (MTF) in the vegetables, where it was higher in wastewater irrigated than in groundwater irrigated vegetables. In both irrigation systems, in all the vegetables similarly, the MTF was highest in Fe followed by Ni, but other heavy metals (Pb, Cd, Cu, Zn and Mn) showed variable transfer factors in the vegetables. Metal transfer factor from soil to plants is a key module of human exposure to heavy metals via food chain. Transfer factor of metals is essential to investigate the human health risk index (Cui et al., 2004).

5. Conclusion Present study investigated the impact of irrigation with wastewater compared to groundwater, on heavy metal accumulation in soil and vegetable parts. The study was carried out in District Sahiwal in the vicinity of Lahore city in Pakistan. Findings indicated that constant irrigation with wastewater caused deposition of various heavy metals in soil and enhanced the chances of transfer of heavy metals from soil to vegetables grown in such affected soil. Heavy metals in vegetables could cause serious health problems on consumption. Only way to control such health impacts was to control heavy metal contamination in irrigational water and soil. Heavy metals were also detected in ground water of the experimental area, though at the present, the groundwater quality seemed within acceptance limit according to WHO standards but there is a possibility for contamination with heavy metals at a long run, which could pose a threat to the quality and utility of the groundwater in Sahiwal District near Lahore as waste water channels are not cemented or lined. Proper mitigation methods are required to control leaching of heavy metals from waste water drainage to ground water. Quality control mechanisms need to be applied for long term use of groundwater, while also developing methods to recycle the large volume of available wastewater in order to provide alternative source of water for irrigation or other domestic purposes. Declaration of Competing Interest

4.3. Daily intake of metals (DIM) and health risk index (HRI)

We confirm there is no conflict of interest.

Values for the daily intake of metals (mg person−1 day−1) were generally higher for wastewater; like Cu and Zn concentration was 9.40 ± 05 mg person−1 day−1 9.52 ± 04 mg person−1 day−1 in turnip and spinach respectively while Cu and Zn concentration was found comparatively lower in turnip (4 ± 06 mg person−1 day−1) and spinach (5 ± 05 mg person−1 day−1) irrigated than groundwater. However, all DIM values were lower than the upper tolerable daily intakes limit recommended by Trumbo et al. (2001) and García-Rico

Acknowledgement The authors acknowledge the Higher Education Commission of Pakistan for the research grant (SRGP-1567). References Abbas, Z., Mapoma, H.W.T., Su, C., Aziz, S.Z., Ma, Y., Abbas, N., 2018. Spatial analysis of

6

Agricultural Water Management 226 (2019) 105816

K. ur Rehman, et al.

Hum. Ecol. Risk Assess. 24, 1409–1420. Kwakye, G., Paoliello, M., Mukhopadhyay, S., Bowman, A., Aschner, M., 2015. Manganese- induced parkinsonism and Parkinson’s disease: shared and distinguishable features. Int. J. Environ. Res. Public Health 12, 7519–7540. Licciardello, F., Milani, M., Consoli, S., Pappalardo, N., Barbagallo, S., Cirelli, G., 2018. Wastewater tertiary treatment options to match reuse standards in agriculture. Agric. Water Manag. 210, 232–242. Mahmood, A., Malik, R.N., 2014. Human health risk assessment of heavy metals via consumption of contaminated vegetables collected from different irrigation sources in Lahore, Pakistan. Arab. J. Chem. 7, 91–99. Mekonnen, M.M., Hoekstra, A.Y., 2016. Four billion people facing severe water scarcity. Sci. Adv. 2, e1500323. Mirecki, N., Agic, R., Sunic, L., Milenkovic, L., Ilic, Z.S., 2015. Transfer factor as indicator of heavy metals content in plants. Fresenius Environ. Bull. 24, 4212–4219. Nicolás, E., Alarcón, J., Mounzer, O., Pedrero, F., Nortes, P., Alcobendas, R., RomeroTrigueros, C., Bayona, J., Maestre-Valero, J., 2016. Long-term physiological and agronomic responses of mandarin trees to irrigation with saline reclaimed water. Agric. Water Manag. 166, 1–8. OECD, 2012. OECD Environmental Outlook to 2050: The Consequences of Inaction. OECD Publishing, Paris. Olanow, C.W., 2004. Manganese‐induced parkinsonism and Parkinson’s disease. Ann. N. Y. Acad. Sci. 1012, 209–223. Pedrero, F., Allende, A., Gil, M.I., Alarcón, J.J., 2012. Soil chemical properties, leaf mineral status and crop production in a lemon tree orchard irrigated with two types of wastewater. Agric. Water Manag. 109, 54–60. Pedrero, F., Maestre-Valero, J., Mounzer, O., Alarcón, J., Nicolás, E., 2014. Physiological and agronomic mandarin trees performance under saline reclaimed water combined with regulated deficit irrigation. Agric. Water Manag. 146, 228–237. Petala, M., Tsiridis, V., Samaras, P., Zouboulis, A., Sakellaropoulos, G., 2006. Wastewater reclamation by advanced treatment of secondary effluents. Desalination 195, 109–118. Petousi, I., Fountoulakis, M., Saru, M., Nikolaidis, N., Fletcher, L., Stentiford, E., Manios, T., 2015. Effects of reclaimed wastewater irrigation on olive (Olea europaea L. cv. ‘Koroneiki’) trees. Agric. Water Manag. 160, 33–40. Saleemi, M., 1990. Environmental scenario of Lahore. Brief of Selected Articles and Lectures. EPA, Punjab, Lahore, pp. 44–48. Sharma, A., Katnoria, J.K., Nagpal, A.K., 2016. Heavy metals in vegetables: screening health risks involved in cultivation along wastewater drain and irrigating with wastewater. SpringerPlus 5, 488. Shiklomanov, I.A., 2000. Appraisal and assessment of world water resources. Water Int. 25, 11–32. Singh, K.P., Mohan, D., Sinha, S., Dalwani, R., 2004. Impact assessment of treated/untreated wastewater toxicants discharged by sewage treatment plants on health, agricultural, and environmental quality in the wastewater disposal area. Chemosphere 55, 227–255. Tchobanoglous, G., Darby, J., Bourgeous, K., McArdle, J., Genest, P., Tylla, M., 1998. Ultrafiltration as an advanced tertiary treatment process for municipal wastewater. Desalination 119, 315–321. Trabelsi, R., Zouari, K., 2019. Coupled geochemical modeling and multivariate statistical analysis approach for the assessment of groundwater quality in irrigated areas: a study from North Eastern of Tunisia. Groundw. Sustain. Dev. 8, 413–427. Trumbo, P., Yates, A.A., Schlicker, S., Poos, M., 2001. Dietary reference intakes: vitamin A, vitamin K, arsenic, boron, chromium, copper, iodine, iron, manganese, molybdenum, nickel, silicon, vanadium, and zinc. J. Acad. Nutr. Diet. 101, 294. USEPA, 2006. United States, Environmental Protection Agency, Integrated Risk Information System. http://www.epa.gov/iris/substS. WHO, 1996. Trace Elements in Human Nutrition and Health. World Health Organization, Geneva. WHO, 2004. Manganese in Drinking Water: Background Document for Development of WHO Guidelines for Drinking-water Quality. World Health Organization. Wozniak, D.J., Huang, J.Y.C., 1982. Variable affecting removing metals removal from sludge. J. Water Pollut. Control Fed. 54, 1574–1580. Wu, J., Yang, Y.S., Lin, J., 2005. Advanced tertiary treatment of municipal wastewater using raw and modified diatomite. J. Hazard Mater. 127, 196–203. Zheng, W., Fu, S.X., Dydak, U., Cowan, D.M., 2011. Biomarkers of manganese intoxication. Neurotoxicology 32, 1–8. Zhou, H., Yang, W.-T., Zhou, X., Liu, L., Gu, J.-F., Wang, W.-L., Zou, J.-L., Tian, T., Peng, P.Q., Liao, B.-H., 2016. Accumulation of heavy metals in vegetable species planted in contaminated soils and the health risk assessment. Int. J. Environ. Res. Public Health 13, 289.

groundwater suitability for drinking and irrigation in Lahore, Pakistan. Environ. Monit. Assess. 190, 391. Abbas, Z., Su, C., Tahira, F., Mapoma, H.W.T., Aziz, S.Z., 2015. Quality and hydrochemistry of groundwater used for drinking in Lahore, Pakistan: analysis of source and distributed groundwater. Environ. Earth Sci. 74, 4281–4294. Aiman, U., Mahmood, A., Waheed, S., Malik, R.N., 2016. Enrichment, geo-accumulation and risk surveillance of toxic metals for different environmental compartments from Mehmood Booti dumping site, Lahore city, Pakistan. Chemosphere 144, 2229–2237. Alloway, B., 1990. Soil processes and the behaviour of metals. Heavy Met. Soils 7–28. Amerasinghe, P., Weckenbrock, P., Simmons, R., Acharya, S., Drescher, A., Blummel, M., 2009. Water Quality, Health and Agronomic Risks and Benefits Associated With “Wastewater” Irrigated Agriculture. American Public Health Association, 2005. Standard Methods for the Examination of Water and Wastewater, 21st ed. American Public Health Association, Washington DC, pp. 1220. Amin, A., Iqbal, J., Asghar, A., Ribbe, L., 2018. Analysis of current and future water demands in the upper Indus basin under IPCC climate and socio-economic scenarios using a Hydro-Economic WEAP model. Water 10, 537. Anim-Gyampo, M., Anornu, G., Appiah-Adjei, E., Agodzo, S., 2019. Quality and health risk assessment of shallow groundwater aquifers within the Atankwidi basin of Ghana. Groundw. Sustain. Dev. 9 100217. Arora, M., Kiran, B., Rani, S., Rani, A., Kaur, B., Mittal, N., 2008. Heavy metal accumulation in vegetables irrigated with water from different sources. Food Chem. 111, 811–815. Asare-Donkor, N.K., Boadu, T.A., Adimado, A.A., 2016. Evaluation of groundwater and surface water quality and human risk assessment for trace metals in human settlements around the Bosomtwe Crater Lake in Ghana. SpringerPlus 5, 1812. Ashfaq, A., Khan, Z.I., Bibi, Z., Ahmad, K., Ashraf, M., Mustafa, I., Akram, N.A., Perveen, R., Yasmeen, S., 2015. Heavy metals uptake by cucurbita maxima grown in soil contaminated with sewage water and its human health implications in peri-urban areas of Sargodha city. Pak. J. Zool. 47, 1051–1058. Basharat, M., 2012. Spatial and temporal appraisal of groundwater depth and quality in LBDC command-issues and options. Pak. J. Eng. Appl. Sci. 11, 14–29. Cao, C., Chen, X.P., Ma, Z.B., Jia, H.H., Wang, J.J., 2016. Greenhouse cultivation mitigates metal-ingestion-associated health risks from vegetables in wastewater-irrigated agroecosystems. Sci. Total Environ. 560–561, 204–211. Cao, C., Zhang, Q., Ma, Z.B., Wang, X.M., Chen, H., Wang, J.J., 2018. Fractionation and mobility risks of heavy metals and metalloids in wastewater-irrigated agricultural soils from greenhouses and fields in Gansu, China. Geoderma 328, 1–9. Chary, N.S., Kamala, C.T., Raj, D.S., 2008. Assessing risk of heavy metals from consuming food grown on sewage irrigated soils and food chain transfer. Ecotoxicol. Environ. Saf. 69, 513–524. Cui, Y.-J., Zhu, Y.-G., Zhai, R.-H., Chen, D.-Y., Huang, Y.-Z., Qiu, Y., Liang, J.-Z., 2004. Transfer of metals from soil to vegetables in an area near a smelter in Nanning, China. Environ. Int. 30, 785–791. FAO, 2016a. AQUASTAT Website. Food and Agriculture Organization of the United Nations (FAO). (Website accessed on 30 May 2019). http://www.fao.org/nr/water/ aquastat/countries_regions/Profile_segments/PAK-GeoPop_eng.stm#top. FAO, 2016b. AQUASTAT Website. Food and Agriculture Organization of the United Nations (FAO). (Accessed on 02 June 2019). http://www.fao.org/nr/water/ aquastat/water_use/index.stm. Gallegos, E., Warren, A., Robles, E., Campoy, E., Calderon, A., Sainz, M.G., Bonilla, P., Escolero, O., 1999. The effects of wastewater irrigation on groundwater quality in Mexico. Water Sci. Technol. 40, 45–52. Gandhi, G., Kumar, N., 2004. DNA damage in peripheral blood lymphocytes of individuals residing near a wastewater drain and using underground water resources. Environ. Mol. Mutagen. 43, 235–242. García-Rico, L., Leyva-Perez, J., Jara-Marini, M.E., 2007. Content and daily intake of copper, zinc, lead, cadmium, and mercury from dietary supplements in Mexico. Food Chem. Toxicol. 45, 1599–1605. Harmanescu, M., Alda, L.M., Bordean, D.M., Gogoasa, I., Gergen, I., 2011. Heavy metals health risk assessment for population via consumption of vegetables grown in old mining area; a case study: Banat County, Romania. Chem. Cent. J. 5, 64. Hossain, M.S., Ahmed, F., Abdullah, A.T.M., Akbor, M.A., Ahsan, M.A., 2015. Public health risk assessment of heavy metal uptake by vegetables grown at a waste-waterirrigated site in Dhaka, Bangladesh. J. Health Pollut. 5, 78–85. Jampani, M., Huelsmann, S., Liedl, R., Sonkamble, S., Ahmed, S., Amerasinghe, P., 2018. Spatio-temporal distribution and chemical characterization of groundwater quality of a wastewater irrigated system: a case study. Sci. Total Environ. 636, 1089–1098. Khan, Z.I., Ahmad, K., Iqbal, S., Ashfaq, A., Bashir, H., Mehmood, N., Dogan, Y., 2018. Evaluation of heavy metals uptake by wheat growing in sewage water irrigated soil.

7