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Environ Monit Assess (2016) 188:525 DOI 10.1007/s10661-016-5535-5 Accumulation and potential health risks of cadmium, lead and arsenic in vegetables grown near mining sites in Northern Vietnam Anh T. K. Bui & Ha T. H. Nguyen & Minh. N. Nguyen & Tuyet-Hanh T. Tran & Toan V. Vu & Chuyen H. Nguyen & Heather L. Reynolds Received: 17 February 2016 / Accepted: 9 August 2016 # Springer International Publishing Switzerland 2016 Abstract The effect of environmental pollution on the safety of vegetable crops is a serious global public health issue. This study was conducted to assess heavy metal concentrations in soil, irrigation water, and 21 local vegetable species collected from four sites near mining activities and one control site in Northern Vietnam. Soils from vegetable fields in the mining areas were contaminated with cadmium (Cd), lead (Pb), and arsenic (As), while irrigation water was contaminated with Pb. Average concentrations of Pb and As in fresh vegetable samples collected at the four mining sites exceeded maximum levels (MLs) set by international food standards for Pb (70.6 % of vegetable samples) and As (44.1 % of vegetable samples), while average Cd concentrations in vegetables at all sites were below the A. T. K. Bui (*) : C. H. Nguyen Institute of Environmental Technology, Vietnam Academy of Science and Technology, 18 Hoang Quoc Viet, Hanoi, Vietnam e-mail: [email protected] H. T. H. Nguyen : M. N. Nguyen VNU University of Science, Vietnam National University, 334 Nguyen Trai, Hanoi, Vietnam T.<H. T. Tran Hanoi School of Public Health, Environmental Health, Hanoi,, Vietnam T. V. Vu Thuyloi University, 175 Tay Son Street, Hanoi, Vietnam H. L. Reynolds Department of Biology, Indiana University, Bloomington, IN 47405, USA MLs of 0.2. The average total target hazard quotient (TTHQ) across all vegetable species sampled was higher than the safety threshold of 1.0, indicating a health risk. Based on the weight of evidence, we find that cultivation of vegetables in the studied mining sites is an important risk contributor for local residents’ health. Keywords Heavy metal . Vegetable . Mining site . Health risk . Northern Vietnam Introduction The toxicities of heavy metals such as cadmium (Cd), lead (Pb), and arsenic (As) are recognized as major human health risks worldwide (Krejpcio et al. 2005; Hu et al. 2013; Chang et al. 2014). Cadmium exposure has been linked to lung and prostate cancers (Fraser et al. 2013; Oteef et al. 2015) in addition to kidney and bone diseases (Järup and Åkesson 2009; Oteef et al. 2015). Lead impairs the hematological, cardiovascular, and neurological systems (Jooste et al. 2015; Oteef et al. 2015). Based on evidence of kidney and brain tumors in animal studies, lead is also likely to be a human carcinogen (U.S. 2003). Arsenic compounds are associated with many forms of skin, lung, bladder, kidney, and liver cancers (U.S. 2003). Food consumption is the main source of human exposure to Cd and Pb which provides up to 80–90 % of daily doses (Krejpcio et al. 2005). Vegetables may account for substantial fractions of total exposures to Cd, Pb, and As, since vegetables are an 525 Page 2 of 11 important part of the human diet and vegetable crops can uptake heavy metals from contaminated environments (Hu et al. 2013; Chang et al. 2014). Mining and smelting activities have released heavy metals to the surrounding environment (Navarro et al. 2008; Zhuang et al. 2009). Vietnam has a total of 73 Pb– Zn mines, distributed mainly in the northern mountainous provinces including Bac Kan, Ha Giang, Tuyen Quang, and Thai Nguyen (DREBK 2012). Concentration of Cd, Pb, and As is very high in soil and water affected by Pb–Zn mining activities in Thai Nguyen and Bac Kan provinces (Bui et al. 2011; Ha et al. 2011). Vegetables were reported to accumulate high concentrations of heavy metals if they grew on miningcontaminated soil (Hu et al. 2013). For example, leafy vegetables can accumulate substantial amounts of heavy metals in their leaves (Kananke et al. 2014). There are, however, still a limited number of studies on heavy metal contents in vegetables in Vietnam (Ngo 2007). Maximum permitted levels (MLs) for contaminants and toxins in foods are specified by international food standards (Codex 2014; Dijk et al. 2015; Oteef et al. 2015). Vietnam’s standards for Cd, Pb, and As contamination in food follow international standards (QCVN 8.2-BYT 2011). Additionally, the target hazard quotient (THQ) developed by USEPA (1989) has been used to evaluate potential non-cancer health risks associated with long-term exposure to chemical pollutants in foodstuffs (Chien et al. 2002; Hu et al. 2013). The aims of this study were (1) to determine the concentrations of Cd, Pb, and As in leafy vegetables cultivated around several mining sites in Northern Vietnam and assess potential health risks to the exposed local people and (2) to provide a comparison of MLs versus the THQ in assessing heavy metal safety concerns in vegetable crops. Materials and methods Study area A monitoring program for vegetable metal contamination was set up in Cho Don district, BacKan province in North Vietnam (Fig. 1). In this area, mining activities have been operating since the eighteenth century (Ha et al. 2011), involving wastewater release into the surrounding environment without treatment (DREBK 2012). Use of potentially contaminated stream water Environ Monit Assess (2016) 188:525 may enhance the heavy metal concentrations in vegetables produced near the mining areas. Vegetable tissue and associated soil samples were taken from crop fields cultivated by local households at four streamside sites near Pb–Zn mines: site 1 (105° 34′ 17″ E, 22° 8′ 58″ N), site 2 (105° 34′ 13″ E, 22° 8′ 50″ N), site 3 (105° 34′ 22″ E, 22° 8′ 22″ N), and site 4 (105° 34′ 22″ E, 22° 8′ 18″ N) and from one upstream control site (Una, 105° 34′ 26″ E, 22° 9′ 58″ N; Fig. 1). Sampling and analysis Vegetable, soil, and water samples were collected from February to April of 2015. A total of 21 vegetable species were sampled across the five sites, with six replicates per species per site (sites differed in which species were grown; site 1: 8 species, site 2: 12 species, site 3: 7 species, and site 4: 7 species, yielding 228 total samples). All the collected samples were leafy vegetables (except string beans). Plant samples were collected approximately 40 days after sowing. Approximately 200 g of soil was collected around the sampled plants at the five study sites (90 samples total; 9 samples per site × 2 times × 5 sites). The collection steps for soil samples followed Chang et al. (2014): Soil samples were taken from the surface layer (0–20 cm), using a bamboo shovel to uproot each vegetable plant and gently shake soil from the roots. All samples were sealed in polyethylene bags and were transported to the Institute of Environmental Technology within 6 h of collection. Fifty water samples were collected near the mine area, mine drainage, and at five streamside locations at each site using a PVC tube column sampler at depth of half meter from the water surface. The samples at each position were mixed in a plastic bucket, and a sample of 1 liter was contained in a polyethylene bottle. Water samples were acidified with nitric acid to pH <2 after collecting and transferred on ice to the laboratory for analysis. Ten milliliters of each sample was filtered through a 0.45-μm Whatman pore-size disposable capsule filter before elemental determination. Sample preparation and digestion methods for vegetables followed Ha et al. (2011); methods for soil followed Bui et al. (2011) with some modifications. The vegetable samples were washed with tap water to remove dust, rinsed with deionized water, and oven dried at 80 °C for 2 days. The dried samples were ground into fine powder using a mortar mill. After grinding, samples (200 mg per each) were digested with Environ Monit Assess (2016) 188:525 Page 3 of 11 525 Fig. 1 Map showing the location of the sampling sites 0.4 ml H2O2 (Merck, 30 %), 1 ml HF (Merck, 40 %), and 2 ml HNO3 (Merck, 65 %) using the Multiwave PRO (Anton Paar) microwave. The microwave was set to 8 min ramping to 140 °C, then held at this temperature for 15 min. Soil samples were oven dried at 80 °C for 2 days, crushed to pass through a 1-mm sieve, and stored at 4 °C in dark plastic bags until analysis. Dried samples (1 g ± 1 mg) were digested with HNO3 65 % (2.35 ml) and HCl 37 % (7 ml) using the microwave as described above. After cooling to room temperature, in both soil and vegetable samples, the content of the vessel was transferred into acid-washed plastic bottles diluted to 10 ml with ultra-pure water and analyzed for elemental concentrations. Soil pHKCl was measured on a 1:2 ratio of soil/KCl(1N) by Lab 850 pH meter (Schott Instruments, Germany). Total (inorganic + organic) heavy metal concentrations in plant, soil, and water samples were measured using an inductively coupled plasma-mass spectrometer (ICP-MS, ELAN 9000, PerkinElmer, USA). The accuracy and precision in elemental analyses by ICP-MS were assessed using reagent blanks and internal standards (Ha et al. 2011). We used standard reference soil material (NIST SRM 2587) from the National Institute of Standard and Technology, USA, standard reference plant material (NIES CRM No. 1) from the National Institute for Environmental Studies, Japan, and standard reference solutions of 1000 mg l−1 for As, Pb, and Cd from Merck, Germany. Heavy metal concentrations of vegetables were determined on a dry weight (dw) basis and converted to a fresh weight (fw) basis for comparison with the MLs for contaminants and toxins in foods. The water content and the ratio of fresh to dry weight (F/D) of vegetables were calculated by their biomass before and after oven drying (Table 1). Dry to fresh weight conversions were made using the respective F/D factor for each vegetable sample. Bioconcentration factor and the target hazard quotient The bioconcentration factor (BCF) is defined as the ratio of metal concentration in shoots to that in the soil (Bui et al. 2011; Ha et al. 2011; Chang et al. 2014). The THQ is the ratio of the body intake dose of a pollutant to the reference dose at which no noncancer health risks are expected, and total target hazard quotient (TTHQ) is the sum of each 525 Environ Monit Assess (2016) 188:525 Page 4 of 11 Table 1 The ratio of fresh weight (F) and dry weight (D) for the vegetable species studied (n = 3) Vegetable name Latin name F (g) D (g) Mustard green Brassica juncea 20 2.15 9.30 89.25 Kohlrabi Brassica oleracea 20 2.43 8.23 87.85 Gourd Benincasa hispida 20 2.85 7.02 85.75 Lolot Piper lolot 20 2.31 8.66 88.45 Centella Centella asiatica 20 2.12 9.43 89.40 Katuk Sauropus androgynus 20 3.21 6.23 83.95 Water spinach Ipomoea aquatica 20 2.45 8.16 87.75 Kale Brassica integrifolia 20 2.33 8.58 88.35 String beans Phaseolus vulgaris 20 2.98 6.71 85.10 Celery Apium graveolens 20 2.45 8.16 87.75 Vine spinach Basella alba 20 2.74 7.30 86.30 Purple onion Allium ascalonicum 20 1.92 10.42 90.40 Cabbage Brassica oleracea 20 2.52 7.94 87.40 Lettuce Lactuca sativa 20 1.91 10.47 90.45 Sweet potato Ipomoea batatas 20 2.36 8.47 88.20 Cauliflower Brassica oleracea 20 2.34 8.55 88.30 Mugwort Artemisia vulgaris 20 2.87 6.97 85.65 Perilla Perilla frutescens 20 2.56 7.81 87.20 Purslane Portulaca oleracea 20 2.24 8.93 88.80 Amaranth Amaranthus tricolor 20 2.17 9.22 89.15 Indian sorrel Oxalis corniculata 20 2.43 8.23 87.85 individual THQ (Chang et al. 2014; Hu et al. 2013) (Eq. 1): THQ ¼ C M vegetable EF ED 10−3 ; TTHQ BW AT RfD ¼ ∑THQ ðsingle pollutantÞ ð1Þ where C is the mean concentration of a particular metal in a fresh vegetable (mg kg−1); Mvegetable is the daily local leaf vegetable intake by the local residents, including local and extraneous vegetables (Chang et al. 2014); EF is the exposure frequency; ED is the exposure duration; BW is the average body weight of a local resident; AT is the average exposure time for non-carcinogens; RfD is the oral reference dose (mg kg−1 per day); and 10−3 is the unit conversion factor. If THQ > 1, there is a potential risk associated with the pollutant (Chien et al. 2002; Yang et al. 2011; Chang et al. 2014). We calculated THQs and TTHQs using the heavy metal concentrations measured in our study and estimates for other parameters as follows: The daily local F/D Water (%) leaf vegetable intake by the local residents (Mvegetable) was estimated to be 200 g; the ratio of local vegetable/ total vegetable consumption was set to 0.8; the ratio of leafy vegetable/local vegetable was set to 0.7 (DARD 2010); EF = 365 (days per year), and ED was set at 70 years (Hu et al. 2013; Chang et al. 2014). BW was estimated from the average weight of adults in Vietnam (50 kg; VMH 2015). AT was set to 365 days × 70 years (Hu et al. 2013; Chang et al. 2014). RfD was set to 1 × 10−3, 3.6 × 10−3, and 3 × 10−4 mg kg−1 per day for Cd, Pb, and As, respectively (USEPA 2014). Statistical analysis Statistical analyses of data were performed using the SPSS 15.0 package for Windows. Data normality and homogeneity of variance were tested using a Kolmogorov-Smirnow test. Evaluation of significant differences among sampling sites were determined using one-way ANOVA followed by Tukey’s post hoc test. Environ Monit Assess (2016) 188:525 Results and discussion Quality of measurements Recovery values of 91–104 % were obtained for Cd, Pb, and As (Table 2). These recovery values compare favorably to those reported in the literature for the analysis of metals in plants (Ha et al. 2011; Hu et al. 2013; Oteef et al. 2015), in soil (Zhuang et al. 2009; Ha et al. 2011), and in water (Arora et al. 2008; Ha et al. 2011). Soil pH and heavy metals in soil and irrigation water samples Soil pH across sites was slightly alkaline and ranged relatively narrowly between pH 7.5 – 7.9 (Table 3). Average concentrations of Cd, Pb, and As in soil samples collected at the four sites near mining activities ranged between 1.9 – 3.8, 118.2 – 160.8, and 28.9 – 39.3 (mg kg−1), respectively, all significantly higher than in samples collected at the control site at Una (Table 3). Sites 2 and 4 tended to have the highest levels of heavy metals (with the exception that As concentrations were higher at site 3 compared to site 2). The maximum acceptable levels (MLs) for Cd, Pb, and As in agricultural soil of Vietnam (QCVN.01.132.BNNPTNT 2013) are 2, 70, and 12 mg kg−1 dw, respectively. Thus, the Cd, Pb, and As concentrations at the four mining sites were 1.5 – 1.9 times, 1.7 – 2.3 times, and 2.4 – 3.3 times higher than the maximum allowable limits, respectively. The high heavy metal concentrations in these soil samples may result from continuous dispersal downstream from the tailings and wastewater of the large-scale mining and smelting operations (Ha et al. 2011; Li et al. 2015). These results corroborate other studies of mining areas, which also reported that elevated levels of heavy metals in soils were ubiquitous in the vicinities of mines and smelters (Kachenko and Singh 2006; Zhuang et al. 2009; Luo et al. 2011). For soil samples at the control site at Una, the heavy metal concentrations were lower than the permitted levels. The concentrations of heavy metals in the soil samples collected at different sites were significantly correlated (p < 0.05). This finding may indicate that all these heavy metals were derived from similar sources. Average concentrations of Cd, Pb, and As in irrigation water at the four mining sites ranged between 0.91 – 1.92, 103.6 – 198.1, and 19.3 – 72.1 μg l−1, respectively, all significantly higher than concentrations Page 5 of 11 525 measured at the control site at Una (p < 0.05, Table 3). The highest mean concentrations were recorded for Pb at all sites, followed by As, with lowest concentrations observed for Cd. The MLs of Cd, Pb, and As in irrigation water according to the Vietnam standard (QCVN.01.132.BNNPTNT 2013) are 10, 50, and 50 μg l−1, respectively. The concentrations of Pb at site 1, site 2, site 3, and site 4 averaged 2.4, 4, 2.6, and 2.1 times higher than the ML according to Vietnam standards for irrigation water, respectively. The As level at site 2 was 1.4 times higher than the ML, while As concentrations were lower than the ML at the other sites. Cadmium levels in irrigation water met the Vietnam standard at all sites. These results suggest that stream water used by local residents for irrigation at the sites near mining activities is consistently contaminated with Pb and contaminated with As at site 2. Therefore, these sites did not meet the standards for soil management and irrigation water of Vietnamese Good Agricultural Practices (VietGAP 2008). Heavy metals in vegetables grown in the vicinity of the mining sites in Bac Kan province The concentrations of Cd, Pb, and As (mg kg−1 dw) in leafy vegetables collected from the four Bac Kan mining areas varied between 0.02 ± 0.01–1.52 ± 0.56, 0.05 ± 0.02 – 8.87 ± 1.57, and 0.17 ± 0.05 – 2.66 ± 1.03 mg kg−1 dw, respectively (Table 4). Significantly lower levels of Cd, Pb, and As were found in vegetable samples collected at the control site at Una, ranging between 0.04 – 0.06, 0.03 – 0.08, and 0.03– 0.07 mg kg−1 dw, respectively. The average concentrations of heavy metals across vegetable samples were the highest for Pb, followed by As and then Cd. The highest concentrations of Cd (mg kg−1 dw) were found in mustard greens (1.52 ± 0.56, 1.44 ± 0.47, 1.04 ± 0.08, and 1.03 ± 0.04 at site 2, site 3, site 4, and site 1, respectively), kale (1.43 ± 0.09), Indian sorrel (1.39 ± 0.56), vine spinach (1.3 ± 0.32), and water spinach (1.25 ± 0.09) (Table 4). Similarly high Cd concentrations were found in leafy vegetables sampled at Dabaoshan mine (Zhuang et al. 2009). Other studies have found lower (Krejpcio et al. 2005; Osma et al. 2012; Chang et al. 2014) and higher (Maleki and Zarasvand 2008; Li et al. 2015) Cd concentrations in vegetables compared to those found in our study. We observed maximum concentrations of Pb (mg kg−1 dw) in water spinach (8.87 ± 1.57), mustard 525 Environ Monit Assess (2016) 188:525 Page 6 of 11 Table 2 Measurements of certified reference standards (mean concentrations ± SD, n = 5) Element NIST SRM 2587 Certified value (mg kg−1) Measured value (mg kg−1) As 13.7 ± 2.3 12.9 ± 1.8 Cd 1.92 ± 0.23 1.84 ± 0.34 Pb 3242 ± 57 3339 ± 86 NIES CRM No. 1 Mean recovery (%) Merck Certified value (mg kg−1) Measured value (mg kg−1) Mean recovery (%) 94 2.3 ± 0.3 2.4 ± 0.2 104 50 48.5 ± 1.1 97 96 6.7 ± 0.5 6.8 ± 0.7 101 5 4.55 ± 0.67 91 103 5.5 ± 0.8 5.4 ± 0.5 98 100 102 ± 6.3 102 greens (8.17 ± 1.09), Indian sorrel (8.07 ± 1.34), katuk (6.57 ± 1.35), and centella (6.18 ± 1.05). Levels of Pb in vegetables found in this study were comparable to those found by Mohamed et al. (2003). Other studies have found lower (Krejpcio et al. 2005; Kananke et al. 2014; Chang et al. 2014; Chopra and Pathak 2015; Oteef et al. 2015) and higher (Abdullahi et al. 2009; Osma et al. 2012; Li et al. 2015) levels of Pb contamination. Fertilizer and other agrochemicals, atmospheric deposition, and irrigation with contaminated water have been implicated in Pb contamination of crops (Oteef et al. 2015). In our study, high levels of Pb in local vegetables appear to be caused by soil and irrigation water that have become contaminated by nearby Pb–Zn mining activities. We observed the highest concentrations of As (mg kg −1 dw) in kale (2.66 ± 1.03), amaranth (1.61 ± 0.25), mustard greens (1.54 ± 0.06), and Indian sorrel (1.22 ± 0.56). There have been very few studies that explored As content in vegetables, and our results were much higher than those reported in another study conducted in Pearl River Delta, South China (Chang et al. 2014). Also of note, the fern Pteris vittata, known as an As hyperaccumulator (Bui et al. 2011; Ha et al. 2011), was abundant at the four mining sites included in our study and was rarely at the control site. The ratio of F/D ranged from 6.23 to 10.47, depending on water content in different leafy vegetables (Table 1). On a fresh weight basis, levels of Cd, Pb, and As in our vegetable samples ranged between 0.002 ± 0.001 – 0.16 ± 0.06, 0.006 ± 0.002 – 1.09 ± 0.19, and 0.02 ± 0.01 – 0.18 ± 0.11 mg kg−1, respectively (Tables 1 and 4). The maximum acceptable levels of Cd, Pb, and As in leafy vegetables to protect public health are 0.2, 0.3, and 0.1 mg kg−1 f.w. (QCVN 8.2-BYT 2011; Codex 2014). The average cadmium concentrations in vegetables at all sites were below the ML of 0.2. However, 70.6 and 44.1 % of leafy Certified value (μg l−1) Measured value (μg l−1) Mean recovery (%) vegetables collected at the four mining sites had average Pb and As concentrations, respectively, that exceeded MLs (up to 3.63 and 1.8 times higher for Pb and As, respectively) (Table 4). Our results suggest that the stream used as irrigation water for vegetable crop production was contaminated by wastewater from mining activities, resulting in elevated heavy metal concentrations in soil and vegetables of receiving areas. Lead concentrations in irrigation water, soil, and vegetables exceeded permissible standard levels. There was, however, significant variation among vegetable species in heavy metal content at the four affected sites. Heavy metal accumulation in vegetables depends on various factors. In our case, the nature of the plant appears to have been an important factor, since different levels of heavy metal concentrations were observed in vegetable leaves of different species grown with the same nutrient and soil properties. Soil-to-plant transfer is one of the key components of human exposure to metals through the food chain (Khan et al. 2008). The BCF is an important indicator of metal transfer from soil into plants (Ha et al. 2011; Chang et al. 2014). In our study, BCF values differed significantly between sites, heavy metals, and vegetables (Table 4). BCF values of vegetables were the highest for Cd, ranging from 0.01 to 0.75, 13 to 33 times higher than for Pb (BCF: 0.003 – 0.059) and 1.7 to 8.2 times higher than for As (BCF: 0.006 – 0.074). Our results indicate that Cd has a higher capacity for transferring from soil to leafy vegetable compared with Pb and As. BCF values found in this study were comparable to those observed by Chang et al. (2014), although other research has observed higher BCF values (Álvarez-Ayuso et al. 2012). The BCF of Cd in vegetables of the Brassicaceae family, including mustard greens, kohlrabi, kale, and cabbage, were higher than those in the other vegetables sampled in this study. The Brassicaceae includes 87 different metal hyperaccumulating plant species, and mustard 7.9 (7.6–8.1) 7.5 (7.4–7.7) Site 4 Unaa a Unaffected site n = 18 for soil and n = 10 for water 7.7 (7.5–7.9) 7.6 (7.4–7.7) Site 2 Site 3 7.5 (7.4–7.6) pH Site 1 Sites 0.9 (0.78–1.12) 3.7 (3.15–4.26) 2.9 (2.68–3.12) 3.8 (3.23–4.17) 1.9 (1.57–1.93) Cd Soil (mg kg−1 dw) 64.3 (60.1–67.6) 150 (141.2–158.5) 128.3 (121.4–132.6) 160.8 (152.7–169.4) 118.2 (111.3–122.7) Pb 3.8 (3.67–4.48) 28.9 (27.4–31.7) 34.1 (28.6–37.8) 39.3 (31.2–45.5) 29.2 (25.3–32.4) As Table 3 Mean (range) concentrations of Cd, Pb, and As in soil and irrigation water and of pH in soil 0.31 (0.27–0.35) 0.91 (0.61–1.13) 1.43 (0.34–2.36) 1.92 (1.23–2.51) 1.32 (0.45–2.07) Cd Irrigation water (μg l−1) 1.7 (1.62–1.75) 103.6 (93.4–111.5) 129 (115.7–142.1) 198.1 (182.3–219.2) 117.4 (106.5–124.8) Pb 1.41 (1.23–1.54) 20.1 (13.9–24.5) 19.3 (14.5–23.1) 72.1 (67.1–78.9) 45.1 (41.2–47.3) As Environ Monit Assess (2016) 188:525 Page 7 of 11 525 525 Environ Monit Assess (2016) 188:525 Page 8 of 11 Table 4 Concentration (mg kg−1 dw ± SD) of heavy metals in vegetables and associated BCF values Area Vegetable Cd BCF Pb BCF As BCF Site 1 Mustard green 1.43 ± 0.09 0.75 4.17 ± 1.09a 0.035 1.66 ± 1.03a 0.057 Kohlrabi 1.12 ± 0.07 0.59 2.04 ± 0.08 0.017 1.03 ± 0.06a 0.035 Gourd 0.24 ± 0.03 0.13 1.80 ± 0.09 0.015 0.81 ± 0.03 0.028 Kale 1.03 ± 0.04 0.54 0.09 ± 0.03 0.0008 1.32 ± 0.06a 0.045 String beans 0.07 ± 0.01 0.04 0.53 ± 0.12 0.005 0.73 ± 0.22 0.025 Site 2 Site 3 Celery 0.23 ± 0.05 0.12 1.12 ± 0.53 0.01 0.34 ± 0.11 0.012 Vine spinach 0.41 ± 0.12 0.22 1.18 ± 0.87 0.010 0.44 ± 0.06 0.015 Purple onion 0.33 ± 0.14 0.17 3.21 ± 1.12a 0.027 0.63 ± 0.32 0.022 Mustard green 1.52 ± 0.56 0.40 5.38 ± 1.13a 0.034 1.05 ± 0.17a 0.027 Celery 0.93 ± 0.11 0.24 2.25 ± 1.07 0.014 0.31 ± 0.06 0.008 Cauliflower 0.19 ± 0.07 0.05 4.12 ± 1.16a 0.026 0.37 ± 0.19 0.009 Katuk 0.59 ± 0.18 0.16 6.57 ± 1.35a 0.041 1.07 ± 0.32a 0.027 Kale 0.37 ± 0.22 0.10 3.44 ± 1.27a 0.021 0.62 ± 0.18 0.016 Mugwort 0.62 ± 0.31 0.16 4.67 ± 1.73a 0.029 0.51 ± 0.10 0.013 a Perilla 0.53 ± 0.16 0.14 3.44 ± 1.07 0.021 0.98 ± 0.16 0.025 Purslane 0.56 ± 0.23 0.15 4.09 ± 1.15a 0.025 1.16 ± 0.63a 0.030 Amaranth 0.36 ± 0.14 0.09 5.81 ± 1.21a 0.036 1.61 ± 0.25a 0.041 Indian sorrel 1.39 ± 0.56 0.37 8.57 ± 1.34a 0.053 2.92 ± 0.56a 0.074 Sweet potato 1.27 ± 0.08 0.33 3.34 ± 1.05a 0.021 0.63 ± 0.22 0.016 Centella 0.33 ± 0.12 0.09 4.75 ± 1.01a 0.030 0.42 ± 0.03 0.011 Mustard green 1.44 ± 0.47 0.50 3.38 ± 0.71a 0.026 1.53 ± 0.67a 0.045 Celery 0.98 ± 0.15 0.34 1.01 ± 0.23 0.008 0.53 ± 0.09 0.016 Vine spinach 0.82 ± 0.15 0.28 1.19 ± 0.07 0.032 0.54 ± 0.08 0.016 1.3 ± 0.32 0.45 4.12 ± 1.05a 0.009 0.56 ± 0.12 0.016 0.013 Cabbage Site 4 b Una a Lettuce 0.84 ± 0.18 0.29 0.78 ± 0.13 0.006 0.46 ± 0.13 Sweet potato 1.07 ± 0.06 0.37 3.10 ± 1.02a 0.024 0.89 ± 0.23a 0.026 Cauliflower 0.21 ± 0.07 0.07 0.09 ± 0.02a 0.0007 0.41 ± 0.13 0.012 Mustard green 1.04 ± 0.08 0.28 8.12 ± 1.01a 0.054 1.06 ± 0.04a 0.037 a 0.028 0.34 ± 0.09 0.012 Kohlrabi 0.53 ± 0.12 0.14 4.23 ± 1.14 Gourd 0.77 ± 0.02 0.21 5.37 ± 1.15a 0.036 0.64 ± 0.08 0.022 Lolot 0.02 ± 0.01 0.01 0.05 ± 0.02 0.0003 0.17 ± 0.05 0.006 Centella 0.22 ± 0.10 0.06 6.18 ± 1.05a 0.041 0.55 ± 0.12 0.019 Katuk 0.13 ± 0.03 0.04 3.18 ± 1.02a 0.021 0.35 ± 0.06 0.012 Water spinach 1.25 ± 0.09 0.34 8.87 ± 1.57a 0.059 0.94 ± 0.21a 0.033 Mustard green 0.06 ± 0.03 0.07 0.03 ± 0.01 0.0005 0.07 ± 0.03 0.018 Celery 0.04 ± 0.01 0.04 0.08 ± 0.03 0.0012 0.05 ± 0.17 0.013 Purple onion 0.05 ± 0.02 0.06 0.04 ± 0.02 0.0006 0.06 ± 0.06 0.016 Indian sorrel 0.05 ± 0.02 0.06 0.07 ± 0.04 0.0011 0.03 ± 0.01 0.008 Allowable limits of Cd, Pb and As in leafy vegetables recommended by the WHO / FAO, Codex and Vietnam National Technical Regulation are 0.2, 0.3, and 0.1 mg kg-1 f.w., respectively; (a): The heavy metal concentrations are higher than permitted standard; (b): Unaffected site; n = 6 per species per site greens were previously demonstrated to be Cd and Pb hyperaccumulators in polluted soil (Anjum et al. 2013). BCF levels of Cd and Pb in some commonly consumed local vegetables such as Indian sorrel, katuk, perilla, purslane, amaranth, and mugwort were also notably high. The highest BCF values of Cd and As were found at site 1, Environ Monit Assess (2016) 188:525 even though Cd concentrations in soil and water of this area were lower than in the other areas. Heavy metals such as Cd enter vegetable tissues mainly through root uptake and absorption by foliage, of which root uptake is the dominant pathway (Chang et al. 2014). Metals can be transferred from soil pore water into plants though the roots in the form of dissolved ions (McLaughlin et al. 2011). Our results suggest that Cd and As in site 1 may be present in more dissolved ionic form for plant uptake than at other sites. Soil pH and other properties (salinity, soil structure, water content, adsorption-desorption, complexation-dissociation, oxidation reduction, ion exchange, and other carrier transport role) can contribute to differences in BCF between sites (Chang et al. 2014; Balkhair and Ashraf 2015). Since soil pH was very similar across sites, we rule out pH as a significant driver of BCF differences in our study. Potential health risks associated with the consumption of local leafy vegetables Many studies use THQ as a more complex parameter for health risk assessment of heavy metals compared to simpler parameters such as MLs (Chien et al. 2002; Song et al. 2009; Li and Zhang 2010; Yang et al. 2011; Chandorkar and Deota 2013; Chang et al. 2014). Across all vegetable species combined, the mean THQs of Cd, Pb, and As were less than 1 at all sites, indicating no health risk (Fig. 2). Likewise, when calculated on a per-species basis across all sites, THQ values of Cd, Pb, and As were also lower than 1, ranging between 0.01 – 0.25, 0.004 – 0.39, and 0.04 – 0.9, respectively. Given that MLs for Pb and As exceeded in 70.6 and 44.1 %, respectively, of leafy vegetables collected at the four mining sites, MLs are a less conservative indicator of risk than THQ. However, THQs of As in five vegetable species were higher than 1 at certain sites: mustard green (site 1 = 1.33, 3 = 1.23); kale (site 1 = 1.15); katuk, amaranth, and Indian sorrel (site 2 = 1.28, 1.30, and 2.65, respectively). Given that As concentrations in all of these species also exceeded MLs, there is strong evidence of health risk for these vegetable species. These results suggest that, to protect against heavy metal toxicity, local residents need vegetable-specific and site-specific information and should pay attention to the kinds and amounts of vegetables consumed (Hu et al. 2013). Across vegetable species, average TTHQ values of Cd, Pb, and As at sites 1–4 varied between 1.00 – 1.44, compared to 0.06 for the control site at Una (Fig. 2). These values indicate a health risk from a diet that Page 9 of 11 525 Fig. 2 The target hazard quotient (THQ) and total THQ of three heavy metals at different study sites, calculated across all vegetable crops includes all the vegetables cultivated at the mining sites. Arsenic was the major risk contributor at all mining sites, contributing from 49 to 73 % of TTHQ. Lead was an important contributor to TTHQ at sites 2 and 4 (Fig. 2). In contrast, Cd contributed the least to TTHQ at the mining sites (13.6–24.9 %) (Fig. 2). Total THQ has been used in recent public studies as a reliable way to compare the combined toxicity risks from different foods and types of chemicals (e.g., As, Cu, Ni, Cr, Hg, Zn, Fe, Mn) (Song et al. 2009; Li and Zhang 2010; Chang et al. 2014). Still, it should be noted that TTHQ is a highly conservative index (Yang et al. 2011; Chang et al. 2014). Furthermore, leafy vegetables contribute only a part of the total daily intake of heavy metals; other sources of intake include drinking water, inhalation of dust, and consumption of local meat such as pork, chicken, ducks, and freshwater fish. Conclusions and recommendations Our results indicate that soils exceed ML safety standards for Cd, Pb, and As, irrigation water from the area exceeds ML safety standards for Pb and As, and substantial percentages of leafy vegetable crops cultivated in the area exceed ML safety standards for Pb and As. Likewise, based on THQ, certain vegetable crops pose risks for As contamination at certain sites. And based on TTHQ, a diet that includes all vegetables poses health risks, especially due to As, regardless of which mining site they were cultivated at. 525 Page 10 of 11 Considering all available evidence, we do not recommend field cultivation of vegetables in these types of mining sites. If vegetables are grown, we recommend those with low BCF values, such as lolot, celery, and string beans and caution against cultivating vegetables belonging to the Brassicaceae family. The use of irrigation water from unpolluted sources (water wells, processed surface water), the use of organic fertilizers, and growth of crops in greenhouses are recommended in these polluted areas. Replacing cultivation of leafy vegetables with fruit tree crops should also be explored, because fruits retain lower concentrations of heavy metals than leaves. 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