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Article

Heavy Metals Contaminants in Watercress (Nasturtium officinale R. BR.): Toxicity and Risk Assessment for Humans along the Swat River Basin, Khyber Pakhtunkhwa, Pakistan

by
Nasrullah Khan
1,
Jawad Khan
1,
Rafi Ullah
1,
Kishwar Ali
2,*,
David Aaron Jones
3 and
Muhammad Ezaz Hasan Khan
2
1
Department of Botany, University of Malakand, Chakdara Dir Lower 18800, Khyber Pakhtunkhwa, Pakistan
2
College of General Education, University of Doha for Science and Technology/College of the North Atlantic-Qatar, Doha P.O. Box 24449, Qatar
3
College of Health Sciences, University of Doha for Science and Technology/College of the North Atlantic-Qatar, Doha P.O. Box 24449, Qatar
*
Author to whom correspondence should be addressed.
Sustainability 2022, 14(8), 4690; https://doi.org/10.3390/su14084690
Submission received: 28 March 2022 / Revised: 11 April 2022 / Accepted: 12 April 2022 / Published: 14 April 2022
(This article belongs to the Special Issue Heavy Metal Pollution and Remediation of Agricultural Soils)
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Abstract

:
This research aimed to investigate the bioaccumulation and health risk associated with absorption of the selected heavy metals (HMs) i.e., lead (Pb), cadmium (Cd), zinc (Zn), and copper (Cu) in a wild leafy vegetable Nasturtium officinale that grows along the Swat River in swampy areas. The areas were categorized using the ecological risk index (RI), which indicates how heavy metal concentrations in soil and plants change over time. The bioaccumulation factor was greater than that at the 400 ≤ RI sites, indicating a probable health risk of these metals from N. officinale consumption. Furthermore, the health risk index for Cd and Pb was more significant, i.e., greater than one in the majority of the samples, indicating health concerns associated with consuming N. officinale from the study site. However, Zn and Cu levels were lower than the nutritionally needed levels, raising the risk of deficiency in the population. Plants cultivated in Pb and Cd-polluted sites were nutrient deficient in Cu and Zn. Intake of such plants can expose people to HM contamination and nutritional deficiencies. The results concluded that the plants accumulated significant HM contents and may have health concerns but are safe for consumption in children and adults.

1. Introduction

It is estimated that by 2030–2050, the human body’s daily energy needs will exceed 3000 calories, and fresh plant-based edible vegetables will play an essential role in ensuring that the human body grows healthy [1]. Vegetables eaten as leaves, particularly leafy green vegetables, include a wide range of bioactive chemicals that make them a part of nutritious diets worldwide [2]. Because of their incredible nutritional value, wild edible vegetables are the most critical source of fresh produce and food replacements [3]. However, even though they are less likely to contain agricultural toxins, nothing is known about the potential health effects of these vegetables [4]. Wild leafy vegetables and culinary herbs are widely used as a nutritious food source in many parts of the globe [5]. However, some of these plants have mineral and toxicological elements that may harm human health [6]. Whether trace metals are required or not, people may have morphological deformities, growth decrease, and an increase in mortality due to exposure to them [7]. Concerns around trace metals, their build-up, and related health issues have emerged worldwide due to human ingestion of them [8].
Heavy metals (HMs) that impact human nutrition include lead (Pb), cadmium (Cd), zinc (Zn), and copper (Cu) [9]. Non-essential and essential HMs, when surpassing threshold levels, cause genetic, physiological, and morphological problems such as retarded growth, malignancy, and higher mortality [8,10]. The dietary food chain is polluted with HMs by the unnecessary practice of agronomic substance addition with the use of community wastewater, industrial waste, and raw sewage for irrigation purposes [11]. Biogeochemical cycles and food chains are critical for integrating non-essential metals in the upper soil horizon of the earth’s crust [9]. The Agency for Toxic Substances and Disease Registry classified environmental HMs such as Arsenic (As), Pb, and Cd into category 1, 2, and 7, respectively [7].
In developing countries, environmental concerns arise from soil polluted with HMs, when the resulting absorption and bioaccumulation of these pollutants in food crops threaten health [12]. Various soil (water content, soil composition, and nutrient balance) and plant (metal content, water content, permissibility, and absorption capacity) factors impact HM concentrations in different vegetables [13]. In soil, heavy metal toxicity is evaluated by one of the most widely used approaches, the Ecological Risk Index (RI), developed by Hakanson (1980) [14]. Heavy metal enrichment in vegetables is assessed by the accumulation factor (AF) that expresses metal levels in the soil in relation to plant components [7]. In humans, the health risk is assessed by the Health Risk Index (HRI), which compares the metal’s concentration in edible portions to the metal’s reference dose and the quantity consumed/unit of body weight [15]. Various studies in a number of countries have been conducted to assess the risk of HMs in different types of agricultural products, viz., China [16,17], India [18,19], Pakistan [20], Saudi Arabia [21,22], Ethiopia [23], and Romania [24]. However, very few studies have reported risks associated with wild leafy vegetables [25,26]. Cu, Zn, Cd, and Pb have been reported to have high accumulation and transfer factors in most food crops [21]. These HMs can migrate easily and settle in edible parts of plants [22], and hence, were focused on in the present study.
People in Pakistan’s suburbs and rural areas often eat wild vegetables, which they deem healthy and safe to consume [25]. Pakistanis consume wild vegetables regularly, especially in the country’s northern parts, known as the Lesser Himalaya. Many vegetables grow well in this area due to the variety of climates [26]. However, no systematic research on the health risks associated with heavy metal contamination in these vegetables has been conducted. Nasturtium officinale, also known as watercress, is a well-known wild perennial green vegetable that grows in swampy areas and is widely consumed raw or cooked in many countries [27,28]. The species has long been used for therapeutic purposes, since the Roman period, has a spicy or peppery taste, and is often used in salads, soups, and other foods, having a short shelf life of one week [29]. However, its shelf life may be extended by freezing and storing [30]. The plant is a nutritional food because it includes essential minerals such as calcium (Ca), potassium (K), magnesium (Mg), manganese (Mn), phosphorus (P), vitamins A, C, E, and K, carotenoids (zeaxanthin and lutein), and glucosinolates [27].
N. officinale’s horticultural value and invasive ecology have been the subjects of research. However, this aquatic plant species has received minimal attention, despite the possible health risks linked with its ingestion. The present study hypothesized that the plants collected from such soils in the Swat catchment regions can accumulate HMs as they are typically harvested from contaminated soils and may have higher quantities of the selected HMs that pose a health risk to the local people (children and adults). Therefore, the research aimed to determine the bioaccumulation factors of HMs (Pb, Cd, Cu, and Zn) and examine the relationships between the different HM concentrations. This research also aimed to analyze the health risk to children and adults in the region by assessing the daily metal intake and prospective health hazards index.

2. Materials and Methods

2.1. Study Area

Boggy areas along the Swat River were chosen for sampling because of the abundance of N. officinale and its routine harvesting for consumption. The study area lies to the North of 34 degrees latitude and east of 72 degrees longitude (Figure 1). Pakistan’s Khyber Pakhtunkhwa Province has an area of 14,737 km2, fed by rain, snowfall, and glaciers (Mohamed et al., 2003). The River Swat spans the District Swat, Tehsil Ranizai in District Malakand, and Tehsil Adinzai in Dir Lower [31].
These areas have subtropical and temperate climates [32]. Summers may be scorching, having a temperature of 41.9 °C, while winters can be freezing, with lows of 0.8 °C. The most significant rainfalls occur in February and March (a combined 162 millimetres), as recorded by the Pakistan Meteorological Department, having a yearly average of 1003 millimetres. Relative humidity remains low in April, i.e., 40%, while it increases in July, reaching 85% [33].

2.2. Sample Collection

During March–July 2020, 120 plant and soil samples were collected randomly from 60 places along the Swat River. Plant samples were hand-picked and carefully packed into plastic bags using gloves. All plant samples were carefully cleaned twice with double distilled water and stored in transparent polythene bags to remove air and soil-borne contaminants. Soil samples were collected using a steel crab at 10 and 20 cm depth. The samples were air-dried at room temperature, sieved at 2 mm, homogenized, and stored in polythene bags [34].

2.3. Acid Digestion and Metal Analysis

The leaves (edible portion) were cut into small pieces, oven-dried (70–80 °C), and then ground using a mortar and pestle to convert into a powdered sample [6,35,36] Desiccators were used to dry the samples until the powder was fine enough to filter through a muslin cloth. At 80–85 °C, the vegetable powder sample was digested in a nitric (HNO3) and perchloric acid (HClO4) solution, resulting in an uncolored solution [37,38,39]. The analysis accuracy was checked using a blank sample proceeded with the test sample. Similarly, each soil sample was digested with a freshly made acid solution (9 mL HNO3 + 3 mL hydrochloric acid (HCl) (1 g). Each digestion was preceded by a blank sample containing the same amount of acid but no soil material. After acid digestion, the materials were filtered through fine filters and kept at 4 °C [40]. HM concentrations were determined by atomic absorption spectrophotometry (VARIAN model AA2407, VARIAN, Palo Alto, CA, USA) in the department of chemistry Kohat University of Science and Technology (KUST).

2.4. Data Analysis

2.4.1. Ecological Risk Index

According to [18], the Ecological Risk Index (RI) was computed as a ratio of the quantity of HM pollution in soil, metal toxicity, and environmental response. The RI formula quantifies the ecological risk of heavy metals extensively, as shown in Equations (1)–(3).
Fi = Cn/Co
Er = Tr × Fi
RI = ∑Er
whereas Fi represents the metal pollution index, Cn represents the metal concentration in the samples, and Co represents the metal reference value, Er represents the monomial potential ecological risk factor. Tr represents the metal toxic response factor. Each metal’s values are in the following order: Zn = 1, Cu = Pb = 5, Cd = 30. The possible ecological risk posed by total metal pollution is RI. Based on RI, the data were categorized into four groups and subsequently analyzed and listed in Table 1.

2.4.2. Bioaccumulation Factor

Following [46], the bioaccumulation factor was determined;
BAF   =   C p l a n t C s o i l
where C s o i l and C p l a n t represent HM concentration in samples of soil and plant.

2.4.3. Daily HM Intake

The average daily intake of metal (DIM) was calculated using the following Equation:
DIM = Cf × Cm × Cfi/Baw
Cf represents the conversion factor (fresh to dry vegetable weight), Cm indicates the HMs concentrations in plants (mg kg−1), Cfi represents the daily vegetable intake, and Baw represents the average body weight. Adults’ and children’s daily vegetable intakes (DIM) were calculated to be 0.345 and 0.232 kg person−1 day−1, respectively. Adult and child body weights were 73 kg [47] and 32.7 kg [48], respectively.

2.4.4. Health Risk Index

Equation (6) [49] was used to determine the health risk index for the local population as a result of consuming N. officinale:
HRI = DIM/RfD
where DIM stands for daily metal intakes and RfD stands for heavy metal reference dose. The Cd, Pb, Cu, and Zn oral reference dosages were 0.001, 0.0036, 0.04, and 0.300 mg kg−1 day−1, respectively. An HRI of less than one indicates that the exposed population is safe, according to the assumptions of the health risk index [50].

2.5. Statistical Analyses

SPSS version 22.0 was used for all analyses (SPSS Inc., Chicago, IL, USA). The metal contents’ mean and standard deviations (SD) were computed for each sample category, followed by post-hoc Turkey tests. For paired wise differences, honestly significant differences (HSD) are used. p < 0.05 was set to evaluate all statistical significance.

3. Results and Discussion

3.1. Heavy Metals in Soil and Plant Samples

Table 2 presents the physicochemical soil parameters based on ecological risk index (RI) categories. The variations in soil pH were insignificant (p > 0.05), ranging from 7.90 to 7.94. The highest mean organic matter concentration is found in RI 400 ≤ RI < 400, followed by RI < 110, 110 ≤ RI < 200, and 400 ≤ RI. Electrical Conductivity was observed to range from 0.21 ± 0.03 to 0.31 ± 0.01 along the RI gradient. The soil samples’ texture was silty-sandy loams, which indicate the boggy plant’s growth in swampy places. Electrical conductivity is a critical factor in HM ions bioavailability in plants [37], and our results reflect the same by significant variations (p < 0.05) across the RI gradient. The organic content of the soil affects the concentration of heavy metals [51]. While heavy metal concentrations in industrial waste soil often exceeded 1000 mg/kg, organic waste soil typically contains less than 1000 mg/kg [52]. Metal-enriched soil has elevated levels and changes in the distribution of heavy metals, which raises plants’ HM levels [53]. Heavy metal contamination in the food chain comes mainly from the soil, since it is essential for waste management and garbage disposal [54,55].
Table 2 depicts the mean concentrations of selected HMs in soil groups based on RI across the River Swat area. HM concentrations varied significantly throughout the RI gradient. Except for Cd in RI < 110, mean Zn and Cu concentrations were within the FAO recommended limits [41,42], while Cd and Pb concentrations were over the reference ranges. Cd, Pb, Cu, and Zn concentrations ranged from 0–17.53, 10.80–136.87, 0.67–6.14, and 5.78–49.91, respectively. The variation in metal concentrations was insignificant except for Cd (p < 0.05, F = 76.2). When compared to previous research, Pb and Cd levels were greater or equal to those described by [37,56,57,58]. Nonetheless, Zn and Cu concentrations were comparable to or slightly lower than those previously reported. This pattern of HM content might be explained by the fact that these soils have been treated with sewage water or household waste for many years. According to [59,60], the metal concentrations were higher than or equal to those recorded in irrigated agricultural soils in the vicinity.
Similarly, [61] found substantial concentrations of HMs in soils of Kolkata (India), while [62] found high concentration of HMs in soils in Beijing (China), under wastewater irrigation systems. According to [63], soils irrigated with wastewater in Harare (Zimbabwe), contained elevated HM levels. These vegetable crops can be protected from absorbing higher quantities of HMs by different methods, e.g., adding organic manure to vary soil texture, monitoring of transportation to far-flung areas, and vegetable growing techniques. These methods are essential because the population in the vicinity frequently uses this green leafy vegetable as a staple crop.
The RI strategy describes metal-contaminated regions by employing soil quality values as criteria [64,65]. These values are used to assess polluted soils and are based on dose-response data from laboratory studies on ecological systems or specific plants or animals [66]. In addition, it considers metal toxicity, total metal concentrations, and other relevant characteristics such as chemical form, electric potential, and ion activity [67,68,69]. Non-soluble heavy metal forms are less bioavailable and hazardous than soluble and free metal ions [70].
Figure 2 depicts heavy metal concentrations in edible components of N. officinale. The mean Cd contents in N. officinale were highest at sites with RI > 110. Similarly, the mean concentration of Pb varied over the RI gradient. Additionally, the mean concentrations of Cd and Pb were higher than the FAO-recommended health standard threshold level [43,44]. Pb is among the minor mobile heavy elements in the earth’s crust; the increasing levels were most likely caused by artificial activity. On the other hand, Pb released from anthropogenic sources may be absorbed by N. officinale since it is water-soluble and generally bioavailable. The usage of such food may be hazardous and, if ingested, may cause health hazards. In contrast, Zn and Cu values were below FAO recommendations [44,45]. Zn is an essential mineral in the human body, where it performs several roles such as catalysis in chemical reactions, structure development (brain, heart, immune and reproductive systems), and regulation of metabolism [71,72]. Zn deficiency causes pregnancy and delivery difficulties, early birth, decreased development, lack of appetite, and lethargy in impoverished areas [72,73]. According to the FAO, 20% of the world’s population is at risk of Zn deficiency. Compared to various wild plants reported from Nigeria and India, this wild vegetable contains similar quantities of Zn [74,75]. Cu concentration in our study (Table 3) was greater than that of some wild leafy vegetables in India but lower than that of certain plants in Nigeria [75,76].

3.2. Bioaccumulation Factor

Table 3 shows the bioaccumulation factor (BAF) that can be ordered as Zn > Pb > Cu > Cd. The BAF for 400 ≤ and 200 ≤ RI < 400 RI was 1 or above, indicating the toxic accumulation of HMs. Thus, in the current investigation, particular emphasis should be given to the high HM levels in N. officinale, which has a high accumulating capability compared to the sanitary standard. Soil-to-plant transfer and HM deposition are of concern and have been described by various studies as critical health risk assessment components [46,77,78,79,80,81,82,83]. HMs accumulate in plant tissues when soil-to-plant translocation increases [81]. According to [81,82], total soil metal concentrations are inversely associated with soil-to-plant transfer factors. Total metal concentrations in soil, on the other hand, dictate soil-to-plant translocation [84].
The most significant source of HM pollution is anthropogenic activities [6,85,86,87,88], whereas soil-crop systems are the most significant source of HM consumption by the human body [89]. Human exposure to heavy metals in the environment occurs predominantly via eating, skin absorption, and inhalation of dust particles, among other routes [85,90,91,92,93]. Artificial sources, such as automotive emissions and power plants, tyre wear particles, auto repair businesses, and car wash centers, are the primary causes of soil contamination [94,95,96]. As a result of their interaction with roots via absorption in polluted soil, HMs have the potential to have severe consequences for plants and animals [97,98]. For determining the extent of soil pollution, plant HM analysis, both wild and cultivated, is an essential source [98,99,100]. The potential for biomonitoring of HM contamination may be found in these plants [99,101,102,103].

3.3. Daily Intake of Metal and Health Risk Index

Table 4 shows the DIM from the various N. officinale samples. The findings suggest that daily element intake from the wild vegetable diet was in the sequence Pb > Zn > Cu > Cd, with noteworthy variation across the RI index for children and insignificant for adults (p > 0.05), except for Cu. In children, the DIM for Pb, Zn, Cu, and Cd is 0.016–0.048, 0.004–0.02, 0.0007–0.002, and 0.0–0.003, respectively and in adults, it is 0.015–0.026, 0.0055–0.0095, 0.0009–0.001, and 0–0.01. Furthermore, all DIM values obtained from N. officinale ingestion were less than one, indicating that these are safe for consumption.
Provisional daily intakes for Cd (0.06 mg), Cu (3 mg), Pb (0.214 mg), and Zn (60 mg) have been recognized by the national council of research [104]. DIMs measured lie below the corresponding PTDIs or came close to approaching the dosages for any of the metals. The maximum DIM in heavy metals was observed in 400≤ RI and was reported from Pb (0.048 mg/d) with the consumption of the analyzed vegetable. The DIM values were similar to or significantly lower than those reported for Pakistan and other countries by [54,105,106,107], respectively: Pakistan (0.00529 mg/d), India (0.032 mg/d), Tanzania (0.021 mg/d), and China (0.059 mg/d) [54]. When compared to Cu, Zn, and Cd, Pb contributed the most to the DIM in this research. Similarly, the DIM values for these metals in the present investigation are significantly lower than their corresponding PTDIs, indicating their risk-free nature. Similar estimates from other countries found that daily intakes were greater than PTDIs [108,109].
Table 5 indicates the health risk of ingesting the green vegetables produced on wastewater–irrigated sites, used to calculate the Health Risk Index (HRI). The HRI is a valuable tool for determining the risk of eating food contaminated with HMs [54,110]. An HRI score of less than 1 implies little or no health risk associated with eating metal-contaminated foods (USEPA, 2007). The HRI value for Pb and Cd was more than 1 (except for Cd at RI < 110 and 110 ≤ RI < 200), but less than 1 for Cu and Zn. For Cd, Pb, Cu, and Zn, HRI values varied from 0.0–3.36, 4.7–13.5, 0.025–0.19, 0.015–0.099 in children and 0–1.61, 4.36–7.36, 0.021–0.028, 0.018–0.031 respectively, in adults.
Consuming the vegetables under investigation poses a health risk due to the presence of Pb and Cd. Dietary Cd and Pb may constitute a health concern to residents. The results of this analysis corroborated with HRI values published by researchers from different areas [54,110,111]. Throughout the RI index for Pb, the highest metal HRI values were for the consumption of wastewater-irrigated vegetables. According to independent analyses for areas near the Huludao zinc facility in Huludao, China, Pb and Cd were reported to be the primary components contributing to the HRI [110], as were those areas around the Dabaoshan mine in Shaoguan, China [54]. These findings suggested that the principal components contributing to the possible health risk posed to residents in Khyber Pakhtunkhwa Province by consuming locally available N. officinale were Cd and Pb.

4. Conclusions

The HM concentrations in plants and soil follow an increasing trend across the RI. Similarly, the bioaccumulation factors progressively increase, with RI having more than 1 in 400 ≤ RI, indicating that consumption of plants from these sites may accumulate higher quantities of these HMs in humans. In contrast, the DIM and HRI do not follow such regular variations. HMs are substantial sources of carcinogenic and non-carcinogenic health concerns when consumed in vegetables. Our results concluded that N. officinale accumulates significant quantities of these HMs; however, the HRI and DIM revealed that its consumption is safe from the health point of view. The levels of Cd and Pb in wild vegetables were much greater than the permitted limits set by SEPA China, FAO/WHO, the EU, and Indian norms, impacting the nutritious components. Many HM contaminations and their impacts on plant nutritional components need further investigation, and contaminated soil should not be used for farming until preventative and rehabilitative measures have been implemented.

Author Contributions

N.K. supervised the research project. J.K. conducted the research and performed the initial analysis. The manuscript draft was prepared by R.U. and K.A. provided valuable information in data visualization and methodology section. D.A.J. and M.E.H.K. edited the manuscript and provided significant insight into the discussion of the results. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding but a 10% discount of APC was provided due to corresponding author’s affiliation to Qatar National Library.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

All the data related to research is presented in the manuscript and is available.

Acknowledgments

We greatly acknowledged Muhammad Sadiq, Scholar in Pharmacy department of Malakand University for his support in Laboratory analysis of the samples. We also acknowledge the Kohat University of Science and Engineering Chemistry department for samples analysis.

Conflicts of Interest

The authors declare no conflict of interest regarding the submission and processing of this manuscript for possible publication.

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Figure 1. Sample sites distribution based on the ecological risk index.
Figure 1. Sample sites distribution based on the ecological risk index.
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Figure 2. Heavy metal concentration in N. officinale of different vegetation groups identified by ecological risk indices.
Figure 2. Heavy metal concentration in N. officinale of different vegetation groups identified by ecological risk indices.
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Table
Table 1. Grade of potentially toxic metal contamination risk to the environment and reference ranges for selected HM.
Table 1. Grade of potentially toxic metal contamination risk to the environment and reference ranges for selected HM.
IndexCategoryRisk GradeHMSRV
(mg/kg)		PRV
(mg/kg)		DL
(mg/kg)		QL
(mg/kg)
Ecological Risk Index (RI)RI < 110Low riskCd0.31 (a)0.10 (c)0.00820.027
110 ≤ RI < 200ModeratePb8.15 (b)5 (d)0.00270.0091
200 ≤ RI < 400Considerable riskCu8.39 (b)10 (d)0.00060.002
400 ≤ RIVery high riskZn44.19 (b)60 (e)0.00490.016
HM (Heavy metal); SRV (Soil references value); PRV (Plant references value); (a) [41]; (b) [42]; (c) [43]; (d) [44]; (e) [45]; DL (Detection limit); QL (Quantification limit).
Table
Table 2. Heavy metal concentration in soil of different vegetation groups identified by ecological risk indices.
Table 2. Heavy metal concentration in soil of different vegetation groups identified by ecological risk indices.
VariableRI < 110110 ≤ RI < 200200 ≤ RI< 400400 ≤ RIF-Valuep-Value
CLY10.4 ± 2.0312.33 ± 1.510.38 ± 0.6411.38 ± 1.090.550.65
SLT49.2 ± 4.4547 ± 3.1346.88 ± 1.4350.69 ± 2.890.610.61
SND40 ± 5.2940.33 ± 4.1742.88 ± 1.5938.53 ± 2.990.660.58
pH7.96 ± 0.107.9 ± 0.117.94 ± 0.027.94 ± 0.040.0260.99
EC0.21 ± 0.030.32 ± 0.0320.31 ± 0.010.24 ± 0.014.500.007
OM%0.92 ± 0.060.91 ± 0.050.953 ± 0.010.88 ± 0.041.160.33
Cd (mg/kg)0 ± 01.5 ± 0.082.6 ± 0.14.7 ± 0.276.29.20 × 10−20
Pb (mg/kg)61.6 ± 18.151.1 ± 7.862 ± 4.353 ± 8.10.50.64
Cu (mg/kg)3.09 ± 0.5 2.6 ± 0.32.8 ± 0.14.2 ± 1.21.30.27
Zn (mg/kg)8.38 ± 0.74 7.3 ± 2.26.1 ± 0.47.7 ± 1.03 1.40.24
CLY (Clay percentage); SLT (Silt percentage); SND (Sand percentage); pH (potential of hydrogen); EC (Electrical conductivity); OM (Organic matter percentage); RI (Ecological Risk Index).
Table
Table 3. Heavy metal bioaccumulation in N. officinale of various groups determined by ecological risk indices.
Table 3. Heavy metal bioaccumulation in N. officinale of various groups determined by ecological risk indices.
MetalGroups-RI < 110110 ≤ RI < 200200 ≤ RI < 400400 ≤ RIF-Valuep-Value
M ± SEM ± SEM ± SEM ± SE
Cd (mg/kg)0 ± 00.6 ± 0.090.9 ± 0.061.1 ± 0.169.596.90 × 10−19
Pb (mg/kg)0.7 ± 0.20.8 ± 0.11.07 ± 0.092.1 ± 0.54.120.010
Cu (mg/kg)0.5 ± 0.10.7 ± 0.081.02 ± 0.071.4 ± 0.16.379 × 10−4
Zn (mg/kg)0.9 ± 0.072.1 ± 0.43.9 ± 0.45.7 ± 0.76.497 × 10−4
Table
Table 4. Daily intake of metal (DIM) due to the consumption of N. officinale in the diets of various groups classified by ecological risk indices.
Table 4. Daily intake of metal (DIM) due to the consumption of N. officinale in the diets of various groups classified by ecological risk indices.
MetalsCdPbCuZn
M ± SEM ± SEM ± SEM ± SE
DIM for Children
Group-RI < 1100 ± 01.6 × 10−2 ± 68 × 10−47.7 × 10−4 ± 5 × 10−54 × 10−3 ± 1.7 × 10−4
110 ≤ RI < 2007 × 10−4 ± 4 × 10−51.8 × 10−2 ± 5.5 × 10−41.4 × 10−3 ± 1.8 × 10−56.4 × 10−3 ± 1.4 × 10−4
200 ≤ RI < 4001.32 × 10−3 ± 1.7 × 10−53.5 × 10−2 ± 4.6 × 10−41.5 × 10−3 ± 8 × 10−51.1 × 10−2 ± 1.1 × 10−4
400 ≤ RI3.3 × 10−3 ± 1.8 × 10−44.8 × 10−2 ± 1.6 × 10−32 × 10−3 ± 3 × 10−52.2 × 10−2 ± 3 × 10−4
ANOVA************
DIM for Adults
Group-RI < 1100 ± 01.5 × 10−2 ± 1.7 × 10−39.4 × 10−4 ± 8.1 × 10−45.5 × 10−3 ± 5.8 × 10−4
110 ≤ RI < 2001 × 10−3 ± 1.6 × 10−42.1 × 10−2 ± 1.6 × 10−38.6 × 10−4 ± 5 × 10−57.6 × 10−3 ± 5.7 × 10−4
200 ≤ RI < 4001.1 × 10−3 ± 1 × 10−52.6 × 10−2 ± 3.6 × 10−41.1 × 10−3 ± 1.7 × 10−59.5 × 10−3 ± 1.2 × 10−4
400 ≤ RI1 × 10−3 ± 13 × 10−41.9 × 10−2 ± 9.8 × 10−41.1 × 10−3 ± 4.2 × 10−57.4 × 10−3 ± 3.5 × 10−4
ANOVA*NSNSNS
Note: NS (Not significant); * (p < 0.05); *** (p < 0.001); M ± SE (Mean ± Standard Error).
Table
Table 5. Health risk index (HRI) of heavy metals due to consumption of N. officinale in food for groups identified by ecological risk indices.
Table 5. Health risk index (HRI) of heavy metals due to consumption of N. officinale in food for groups identified by ecological risk indices.
MetalsCdPbCuZn
M ± SEM ± SEM ± SEM ± SE
Children HRI
Group-RI < 1100 ± 04.75 ± 1.8 × 10−11.9 × 10−1 ± 1 × 10−21.5 × 10−2 ± 5.9 × 10−4
110 ≤ RI < 2007.1 × 10−1 ± 4 × 10−25.13 ± 1.5 × 10−12.5 × 10−2 ± 4.6 × 10−42.1 × 10−2 ± 3.3 × 10−4
200 ≤ RI < 4001.39 ± 1 × 10−29.93 ± 1.2 × 10−13.9 × 10−2 ± 2.2 × 10−59.6 × 10−2 ± 3.9 × 10−4
400 ≤ RI3.36 ± 1.8 × 10−113.55 ± 4 × 10−16 × 10−2 ± 8.4 × 10−47.5 × 10−2 ± 15 × 10−3
ANOVA************
Adults HRI
Group-RI < 1100 ± 04.37 ± 4 × 10−12.3 × 10−2 ± 2.1 × 10−31.8 × 10−2 ± 1.9 × 10−3
110 ≤ RI < 2001.23 ± 1.6 × 10−25.85 ± 4.4 × 10−12.1 × 10−2 ± 1.4 × 10−42.1 × 10−2 ± 6.9 × 10−3
200 ≤ RI < 4001.14 ± 18 × 10−27.38 ± 1.3 × 10−12.4 × 10−2 ± 2.5 × 10−43.1 × 10−2 ± 4.1 × 10−4
400 ≤ RI1.71 ± 1.3 × 10−15.35 ± 2.7 × 10−12.8 × 10−2 ± 1.1 × 10−32 × 10−2 ± 1.1 × 10−3
NSNSNSNS
Note: NS (Not significant); *** (p < 0.001); M ± SE (Mean ± Standard error).
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Khan, N.; Khan, J.; Ullah, R.; Ali, K.; Jones, D.A.; Khan, M.E.H. Heavy Metals Contaminants in Watercress (Nasturtium officinale R. BR.): Toxicity and Risk Assessment for Humans along the Swat River Basin, Khyber Pakhtunkhwa, Pakistan. Sustainability 2022, 14, 4690. https://doi.org/10.3390/su14084690

AMA Style

Khan N, Khan J, Ullah R, Ali K, Jones DA, Khan MEH. Heavy Metals Contaminants in Watercress (Nasturtium officinale R. BR.): Toxicity and Risk Assessment for Humans along the Swat River Basin, Khyber Pakhtunkhwa, Pakistan. Sustainability. 2022; 14(8):4690. https://doi.org/10.3390/su14084690

Chicago/Turabian Style

Khan, Nasrullah, Jawad Khan, Rafi Ullah, Kishwar Ali, David Aaron Jones, and Muhammad Ezaz Hasan Khan. 2022. "Heavy Metals Contaminants in Watercress (Nasturtium officinale R. BR.): Toxicity and Risk Assessment for Humans along the Swat River Basin, Khyber Pakhtunkhwa, Pakistan" Sustainability 14, no. 8: 4690. https://doi.org/10.3390/su14084690

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