Introduction

Urban expansion is occurring at a quicker pace than ever before, particularly in the world’s least developed countries, resulting in the deposition of several toxic contaminants in the environment through anthropogenic activities [1, 27]. The contamination of soil with hazardous metals is prevalent in urban and peri-urban areas due to municipal and industrial (textile, garment, pharmaceuticals, and cosmetics) operations along with extensive use of agrochemicals [1, 25]. Furthermore, wastewater irrigation is one of the main sources of soil contamination in urban areas [23]. In Bangladesh, wastewater and industrial effluents are recklessly released into neighboring waterways without sufficient treatment due to uncontrolled industrialization [24]. As a consequence, heavy metals do contaminate river or canal water in many industrial areas of Bangladesh [1]. Moreover, farmers prefer to irrigate their agricultural fields with industrial wastewater as it contains N, P, Mg, and K, but they are unaware of the severity of heavy metal poisoning through crop intake [14].

Heavy metals are considered as micronutrients, requiring only a minimal quantity for plant and animal growth [15]. However, regular intake of several heavy metals like Pb, Cd, Cr, and Ni may result in serious health risks even at low concentrations [11, 47]. Chronic exposure to these hazardous metals via contaminated vegetables leads to their accumulation in the liver, kidneys, and other parts of the human body and causes DNA damage,disruption of various biochemical processes; neurological, cardiovascular, and bone diseases; and eventually cancer [1]. Several anthropogenic activities contribute to the accumulation of heavy metals in soil, which are then transmitted to the edible parts of plants [19]. Consequently, the consumption of such vegetables grown in contaminated areas is regarded as one of the principal routes of heavy metal toxicity into the human body [44].

Vegetables are an essential and frequently consumed food, which contain vitamins, minerals, and numerous bioactive components [50]. Regrettably, due to unplanned industrialization in developed and emerging economies such as Bangladesh, vegetables cultivated in these places are contaminated with carcinogenic heavy metals via the water–soil–crop pathway, making it a major and frightening concern [2, 7]. The study area (Narsingdi district) is well-known for its numerous textile industries, the majority of which discharge their effluents into the neighboring Meghna or Shitalakshya rivers [28]. Though several reports revealed the amount of heavy metal contamination in the water of these rivers [31, 41], study on analyses of heavy metal contamination and toxicity in agricultural produces provided seldom attention in the particular areas. Some studies established that vegetables cultivated with industrial effluent content have considerably greater extent of heavy metals in other industrial areas [5, 33, 35, 36]. In particular, Pb, Cd, arsenic (As), mercury (Hg), Cr, and Ni were detected above the threshold limit in fruit and vegetables grown in industrial areas of Bangladesh [2, 39, 44]. The consumption of such heavy metal-contaminated agricultural produce poses a serious threat to public health such as cancer and cardiovascular disease, etc. [39, 44]. Therefore, respective authorities must monitor the hazardous metal concentrations in vegetables cultivated in industrial areas to determine the potential health concerns. Consequently, the current study analyzed the concentrations of toxic Pb, Cd, Cr, and Ni in widely consumed vegetables to protect human health from the detrimental effect of such hazardous metals.

Materials and Methods

Chemicals

Certified reference materials (CRM) of Pb, Cd, Cr, and Ni and chemicals were purchased from Merck (Darmstadt, Germany) through the Bangladesh Scientific and Chemical Company Pvt. Ltd., Dhaka, Bangladesh. All other chemicals and reagents including nitric acid (HNO3), hydrochloric acid (HCl), hydrogen peroxide (H2O2), lead nitrate (Pb(NO3)2), zinc nitrate (Zn(NO3)2), chromium oxide (Cr2O3), manganese powder (Mn), ammonium chloride (NH4Cl), and cadmium nitrate (Cd(NO3)2) were of analytical grade.

Collection and Preparation of Vegetable Samples

In total of seventy-two vegetable (n = 72) samples were collected from Shibpur (n = 36) and Raipura (n = 36) Upazila of Narsingdi district, Bangladesh (Figure S1). For each vegetable, six (6) samples (2 kg each) were collected from six (6) different sellers in one Upazila to cover representative areas. Edible portions of WC (leaf and stem), RA (leaf and stem), AW (leaf and stem), SP (leaf), CF (inflorescence), and EP (fruit) were selected randomly from local markets and cleaned twice with deionized water to remove any adhering soil. Then, the vegetable samples were put into separate ziplock poly bags and transferred to the Department of Agricultural Chemistry laboratory at Sher-e-Bangla Agricultural University in Dhaka, Bangladesh. The detailed information concerning these vegetable samples is presented in Table S1. Twelve samples of each vegetable were processed separately. Small chunks of the air-dried edible components of vegetable samples were dried at 65 °C in an electric oven until they reached a constant weight [33]. The dried vegetable samples were crushed to prepare a fine powder using a porcelain mortar to avoid contamination, put into ziplock poly bags [21], and taken to the analytical laboratory of Bangladesh Agricultural Research Institute, Gazipur, for the determination of Pb, Cd, Cr, and Ni. All samples were stored in a desiccator until required to complete the experiments.

Sample Digestion and Analysis

Ground vegetable samples (0.5 g) were digested with 10 mL nitric acid and 2 mL H2O2 at 120–125 °C in a microwave-assisted digestion system [39]. The digested samples were then cooled at room temperature and diluted to 50 mL with deionized water and passed through a 0.45-μm syringe filter (cellulose acetate, Minisart) to a 10-mL plastic bottle. The concentration of heavy metals in the acidic solution was determined using an atomic absorption spectrophotometer (AAS) (Agilent, USA, Model No. FS 240). A calibration curve was prepared using working standard solutions for individual certified reference material (CRM) at different concentrations. Then, the response of the unknown metal ions of the vegetable samples was calculated using the individual calibration curve. The measurements were carried out with flame atomization settings, where the Deuterium lamp served as a background correction. The wavelength of 217, 228.8, 357.9, and 232 nm (sourced from hollow cathode lamp) was selected for Pb, Cd, Cr, and Ni content, respectively, and air acetylene was used as fuel gas. Triplicates (n = 3) of each vegetable sample were used for the determination of heavy metal concentration, and the average values were recorded. Initially, the analyzed heavy metal concentrations of vegetable samples were obtained on a dry weight (dw) basis and then converted to the fresh weight (fw) basis for further application.

Method Validation and Quality Control

The method was validated based on the parameters of linearity, coefficient of determination (R2), lowest of detection (LOD), accuracy, and precision. The calibration curves of Pb, Cd, Cr, and Ni were obtained using standard solutions of six concentrations (0.0–1.0 mg L−1) in deionized water with good linearity (R2 = 0.995). One g of powdered sample was randomly selected and spiked with three distinct heavy metal concentrations (1.0, 1.5, and 2.0 mg L−1) and run in with the AAS. The same procedure was followed for blank/unspiked samples, and deionized water was employed throughout the analysis. The recovery percentages were ranged from 90 to 110% using the known spiked sample with RSD < 10%. The LOD of AAS was obtained for each metal from the three standard deviations of the blank responses. Thus, the LOD of AAS for Pb, Cd, Cr, and Ni was determined to be 0.006, 0.008, 0.01, and 0.0012 mg L−1, respectively, which seems that the AAS was good enough to determine the lower level of tested metal concentration.

Data Analysis

Single-Factor Pollution Index (PI)

The PI is the ratio of heavy metal content in a sample and the permissible limits imposed by international organizations such as the WHO, FAO, and US Environmental Protection Agency (US EPA) [1, 20]:

$$PI={C}_{V}{/C}_{L}$$
(1)

where CV is the concentration of heavy metal in vegetable sample (mg kg−1) and CL is the regulatory limit by FAO/WHO (mg kg−1). PI < 1 indicates samples have not yet been polluted, whereas a value of PI > 1 suggests contamination, and PI = 1 indicates critical condition (require environmental monitoring) [20].

Average Pollution Index (PIA)

The average pollution index (PIA) of different vegetable samples was calculated as follows [1]:

$${PI}_{A}=\frac{1}{n}\sum\limits_{i=1}^{n}PI$$
(2)

where PI is the single-factor pollution index and n is the number of heavy metal species studied. PIA > 1.0 suggests higher heavy metal contamination is evident in the sample [34].

Metal Pollution Index (PIM)

The PIM is used to observe the total heavy metal concentrations in vegetables, which were calculated by using the geometrical mean of all metal concentrations in the samples [42]:

$${PI}_{M}= {({C}_{1}\times {C}_{2 }\times {C}_{3 }\times \dots \dots \dots \times {C}_{n})}^{1/n}$$
(3)

where Cn = heavy metal concentration in the nth sample (mg kg−1).

Estimated Daily Intake of Heavy Metal

The consumer health risk is assessed by obtaining the estimated daily intake (EDI) value and comparing it with the maximum tolerable daily intake (MTDI) set by regulatory bodies. According to the US EPA, the EDI values of different heavy metals were estimated as follows [29, 32]:

$$EDI=\frac{VIR\times C}{BW}$$
(4)

where VIR = vegetable ingestion rate (in kg) of Bangladesh, C = mean concentration of heavy metal in the sample (mg kg−1), and BW = body weight (kg). The average vegetable ingestion rate in Bangladesh was considered to be 0.1673 kg person−1 day−1 and BW values of 60 and 32 kg for adults and children, respectively [1, 16].

Health Risk Assessment

Both carcinogenic and non-carcinogenic risks of heavy metals in vegetable samples were estimated using the US EPA models 48.

Carcinogenic Risk

The Incremental Lifetime Cancer Risk (ILCR) is determined to evaluate the possibility of cancer risk through the intake of carcinogenic heavy metals via foodstuffs which were estimated as follows [19]:

$$ILCR=CDI\times CSF$$
(5)

where CDI = chronic daily intake of heavy metals (mg kg−1 BW day−1) and CSF = cancer slope factor (mg kg−1 day−1). According to OEHHA, [30], the oral CSF values of Pb and Cd are 0.0085 and 15 (mg kg−1 day−1), respectively. The CDI value for each heavy metal was calculated using the following equation:

$$CDI=\frac{\left(EDI\times EF\times TED\right)}{AT}$$
(6)

where EDI = estimated daily intake of heavy metal (mg kg−1 day−1); EF = exposure frequency (365 days year−1); TED = total exposure duration (70 years), which is the average lifetime of Bangladeshi people; and AT = average exposure time (365 days × 70 years = 25,550 days). The cumulative ILCR (ΣILCR) is used to assess total cancer risk due to ingestion of multiple heavy metals by a specific type of food:

$$\sum_{i=1}^{n}ILCR={ILCR}_{1}+{ILCR}_{2}\dots \dots \dots \dots \dots +{ILCR}_{n}$$
(7)

where i (= 1, 2…..n) is the individual heavy metal present in the same sample. If the estimated ILCR < 10−6, the exposure to people is considered as safe (negligible/accepted risk), whereas ILCR > 10−4 is considered as the threshold risk limit (risk requires remedial measures), and ILCR > 10−3 is reflected as moderate risk (concerning public health) [14].

Non-carcinogenic Risk

The target hazard quotient (THQ) is used to assess the non-carcinogenic risks of specific heavy metals detected in the sample, which was calculated following the formula [32, 45]:

$$THQ=\frac{CDI}{RfD}$$
(8)

where CDI = chronic daily intake of heavy metals (mg kg−1 BW day−1) and RfD = oral reference doses of heavy metals (mg kg−1 day−1). The standard RfD values of Pb, Cd, Cr, and Ni are 0.0035, 0.003, 1.5, and 0.02 mg kg−1 day−1, respectively [1, 16, 39].

The chronic hazard index (HI) is the cumulative target hazard quotient of each heavy metal present in a sample. According to USEPA [48], HI is obtained as follows:

$$\mathrm{HI}=\sum_{\mathrm{i}=1}^{\mathrm{n}}\mathrm{THQ}$$
(9)

where i (= 1, 2……., n) = individual heavy metal present in the sample. The exposed population is deemed safe when HI < 1, whereas HI > 1 indicates a potential risk of ingesting contaminated food items. Thus, control measures should be applied [26, 40].

Statistical Analysis

Descriptive statistics of heavy metal concentrations were obtained utilizing MS Excel 2016 version. The obtained results were presented as mean ± standard deviation (SD). In addition, a one-sample t test was performed to check the significant difference (< 0.05) between mean heavy metal concentration and FAO/WHO permissible limit.

Results and Discussion

Heavy Metal Concentration in Vegetable Samples

The concentrations (mean) of heavy metals (Pb, Cd, Cr, and Ni) (mg kg−1, in fresh weight basis) in different vegetable samples are presented in Table 1. The concentration (mean ± SD) of heavy metals in all samples varied significantly (p < 0.05) from the corresponding maximum allowable concentrations (MAC). The content of Pb in most vegetable samples exceeded the FAO/WHO safe limit of 0.1 mg kg−1. The order of difference from the corresponding safe consumption limit was Pb > Cd > Ni > Cr. Any variation in the heavy metal concentration in different vegetable species depends on climatic change, growth kinetics, accumulation, absorption capacity of plants, and concentrations of heavy metals in soil and irrigation water [14, 33].

Table 1 Heavy metal concentration (mg kg−1, in fresh weight basis) in different vegetables collected from Narsingdi district, Bangladesh
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The Pb concentrations in different vegetable samples varied from 0.06 to 0.46 mg kg−1 with the mean of 0.221 ± 0.10 mg kg−1, whereas the average minimum and maximum concentrations were found in EP (0.14 mg kg−1) and WC (0.38 mg kg−1), respectively. Out of six analyzed vegetable samples, WC (0.380 ± 0.07), RA (0.175 ± 0.09), and AW (0.311 ± 0.05) samples showed significantly higher Pb concentrations, whereas a threefold higher concentration than the MAC (0.1 mg kg−1) was obtained in WC (0.380 ± 0.07) and AW (0.311 ± 0.05). We found that about 67% of RA, EP, CF, and SP samples and 100% of WC and AW samples exceeded the MAC. Alarmingly, around 79.17% of total samples contained higher Pb than the MAC. However, the range of Pb concentration in this study is lower than the other industrial areas of Bangladesh reported in previous studies [6, 16, 17, 39]. Several studies reported the Pb concentration of 22 mg kg−1 in watercress [44], 6.04 mg kg−1 in varieties of vegetables [3], 0.643–3.362 mg kg−1 in a wide range of vegetables grown in different industrial areas of Bangladesh. The Pb concentration (mean) in SP, CF, and RA was reported to be 0.33, 0.51, and 0.19 mg kg−1 in the Jhenaidah district by Islam et al. [18] which is 2.35, 3.0, and 1.12 times higher than this study. Pb content above the threshold limit was also reported in different vegetables collected from industrial areas of Nigeria (0.072 ± 0.06 to 0.128 ± 0.03 mg kg−1), [43], Ethiopia (3.63 to 7.56 mg kg−1) [13], Libya (0.02 to 1.824 mg kg−1) [8], Brazil (0.04 to 1.10 mg kg−1) [12], India (0.07–0.13 mg kg−1 [42, 49], Pakistan (3.98 ± 2.29 mg kg−1) [15], and Turkey (0.9 to 2.6 mg kg−1) [38]. Cd concentrations in all the analyzed vegetables were ranged from 0.006 to 0.138 mg kg−1, with the highest mean value occurring in SP (0.114 mg kg−1) and the least in CF (0.013 mg kg−1). The Cd content was significantly lower in RA (0.048 ± 0.01), AW (0.044 ± 0.01), CF (0.013 ± 0.0), and EP (0.029 ± 0.01) samples, whereas WC (0.064 ± 0.01) and SP (0.114 ± 0.02) samples had significantly higher Cd content than FAO/WHO MAC (0.05 mg kg−1). It was found that about 17% AW, 58% RA, 92% WC, and 100% SP samples exceeded the safe limit of Cd content. In average, about 44.44% of vegetable samples were contaminated with Cd, which was higher than the threshold value (0.05 mg kg−1). Islam et al. [18] found the Cd concentration as 0.48, 0.3, and 0.23 mg kg−1 in SP, CF, and RA in the Jhenaidah district which is 4.36, 23, and 4.79 times greater than the current study. The maximum Cd concentration (mean) of different vegetables was ranged from 0.13 to 0.57 mg kg−1, reported in varieties of vegetables collected from industrial areas in Dhaka [4, 45], [2] Gazipur (0.08 to 0.15 mg kg−1) [45], Tangail (1.86 ± 0.64 mg kg−1) [33], Sathkhira (0.05 to 1.05 mg kg−1) [46], and Jessore (0.24 to 0.77 mg kg−1) [6], districts of Bangladesh. Some other studies also reported the over concentration of Cd in food products in other developing countries [11, 37, 43]. The average Cr concentration in different investigated vegetable samples was 0.135 ± 0.10 mg kg−1 (range 0.019 to 0.39 mg kg−1), whereas the average minimum and maximum concentration was detected in RA (0.054 mg kg−1) and WC (0.24 mg kg−1), respectively, and the concentrations were significantly lower than the FAO/WHO MAC (2.3 mg kg−1). According to FAO/WHO guidelines, the Cr concentration in collected vegetable samples from industrial areas of the Narsingdi district of Bangladesh indicated negligible or no risk to human health. However, the leafy vegetable samples, WC (0.241 ± 0.11), and SP (0.146 ± 0.01) showed higher Cr accumulation than others. Cr concentrations were reported in the range of 0.56–23.6 mg kg−1 [3] and 0.01–10 mg kg−1 [44] for different vegetable samples from Gazipur industrial areas, whereas lower than MAC was also reported for vegetable samples collected from Faridpur industrial areas [14] and local markets in the capital city, Dhaka [22].

The Ni concentrations were ranged from 0.74 to 11.13 mg kg−1, and most of the samples were found within the safe consumption limits as per MAC (10 mg kg−1) set by FAO/WHO, except one sample of AW, which contained 11.13 mg kg−1 Ni. The mean concentration of Ni was 3.605 ± 2.5 mg kg−1. The maximum Ni concentration (11.13 mg kg−1) was found in the AW sample, whereas the lowest Ni content (0.748 mg kg−1) was recorded in the EP samples. The mean Ni concentration in vegetable samples was in the following order: AW > WC > EP > SP > RA > CF. A comprehensive study on heavy metal concentration of Bangladeshi vegetables revealed the Ni concentration in the range of 0 to 11.33 mg kg−1 in industrial site vegetables [44] and 1.41 to 26.30 mg kg−1 in the fruit vegetables [33]. It is evident from the above discussion that Pb concentrations were higher than the FAO/WHO safe limit in all six types of vegetable samples, while Cd concentration is higher only in SP samples.

Pollution Index

The single-factor pollution index varied greatly between vegetable samples (Fig. 1). In case of Pb concentration, all samples exceeded the threshold value (PI > 1.0), indicating elevated contamination with this carcinogenic metal. The highest PI value (3.801) was observed in WC, while the lowest was in EP (1.40) samples, respectively. The pollution assessment of Cd confirmed that only WC (1.28) and SP (2.28) samples exceeded the acceptable value (PI > 1.0). However, all the analyzed vegetable samples showed PI < 1.0 for Cr and Ni contamination. It was observed that the lowest or highest values of both indexes (average pollution index and metal pollution index) were obtained in the same sample (Fig. 2). The WC (0.74) revealed the highest PIM among the six vegetables samples, followed by AW (0.63), SP (0.48), EP (0.34), RA (0.29), and CF (0.19), respectively. The PIA > 1.0 in WC (1.44), AW (1.21), and SP (1.01) suggest the potential pollution hazard is real due to the accumulation of heavy metals.

Fig. 1
figure 1

Single-factor pollution index of heavy metals in different vegetables grown in industrial areas of Bangladesh

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Fig. 2
figure 2

Comparison between average pollution index and metal pollution index in different vegetable samples

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Estimated Daily Intake of Heavy Metal

The most common route of heavy metal exposure in the human body occurs through the consumption of food. The severity of the associated risk depends on the intake rate of heavy metals through contaminated foods. In this study, the EDI values of Pb, Cd, Cr, and Ni for adults and children were calculated and compared with MTDI (Table 2). The total EDI values of Pb, Cd, Cr, and Ni for adults were 0.004, 0.001, 0.002, and 0.006 mg kg−1 day−1, while the corresponding values for children were 0.007, 0.002, 0.004, and 0.113, respectively. Among all the heavy metals, Ni and Pb have the highest EDI values for both adults and children groups. However, the calculated EDI values of any heavy metal in a single or all studied samples were lower than the corresponding MTDI.

Table 2 Estimated daily intake (EDI) of heavy metals in contaminated vegetables and corresponding maximum tolerable daily intake (MTDI)
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Health Risk Assessment

Cancer Risk

Pb and Cd are classified as carcinogenic heavy metals as their chronic exposer causes different types of cancer [14]. The calculated incremental lifetime cancer risks (ILCRs) of Pb and Cd via consuming contaminated vegetables are presented in Table 3. The calculated ILCRs of Pb and Cd ranged from 4.1 × 10−6 to 3.3 × 10−6 and 7.8 × 10−6 to 1.7 × 10−5 and 5.5 × 10−4 to 4.8 × 10−3 and 1.0 × 10−3 to 9.0 × 10−3 for adults and children, respectively. These findings demonstrated that the cancer risk of Cd in all the analyzed vegetables is higher than the threshold value (ILCR > 10−4), which poses a potential cancer risk to both target groups (children and adults). In contrast, the least cancer risk was observed from Pb, which exceeded the safe limit (ILCR > 10−6) but within the acceptable limit (ranged between 10−6 and 10−4). The sum ILCR values of analyzed vegetables for children and adults are depicted in the following order: SP > AW > RA > AW > EP > CF. Moreover, the cancer risk of some leafy and root vegetables grown in other industrial areas of Bangladesh has been reported in the literature, which exceeded the threshold value [14, 39, 40, 44].

Table 3 Non-cancer risk as total target hazard quotient (THQ) and incremental lifetime cancer risks (ILCR) of adults and children through consumption of heavy metal-contaminated vegetables
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Non-cancer Risk

The non-cancer risk of heavy metals in six vegetables for adults and children was estimated based on target hazard quotient (THQ) and hazard index (HI = ΣTHQ), which are displayed in Table 3 and Fig. 3. In general, THQ values of Pb, Cd, Cr, and Ni in most of the vegetable samples were THQ < 1.0, implying no detrimental health effect to exposed consumers experienced no damage to their health (Table 3). The value of THQ > 1.0 was observed only for Ni (1.1 and 2.0) in the investigated AW sample for adults and children, respectively, indicating severe non-cancer risk to both consumers groups. The highest TTHQ was obtained for Ni (TTHQ = 3 in adults, 5.7 in children), and the trend that emerged was Ni > Pb > Cd > Cr for both aged groups. The cumulative non-cancer risk of all studied heavy metals was expressed as hazard index (HI). The WC (1.2) and AW (1.3) samples revealed the HI > 1.0 for adults, whereas HI > 1 was observed in WC (2.2), AW (2.5), SP (1.1), and EP (1.0) for children (Fig. 3). Therefore, the current investigation reveals the potential non-carcinogenic health risk through ingestion of heavy metal-contaminated vegetables grown in industrial areas of Bangladesh.

Fig. 3
figure 3

Non-cancer risk of heavy metals through consumption of contaminated vegetables

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Study Limitations

This study did not consider other trace metals such as arsenic, antimony, copper, and zinc, and, therefore, future research should include these as well as to estimate the total elemental exposure and their consequential health hazards. Soil and water samples are also required to be thoroughly investigated for actual metal accumulation levels in vegetables.

Conclusion

This current research revealed the heavy metal contamination in vegetables grown in industrial areas of Bangladesh and associated health hazards. The concentration of Pb and Cd was predominant among the four tested metals in widely consumed WC, AW, RA, SP, CF, and EP samples. It was observed that 79.17% and 44.44% of the vegetable samples exceeded the FAO/WHO acceptable limit for Pb and Cd concentrations, respectiv ely. The computed pollution indices showed that WC, AW, and SP had contamination that exceed the FAO’s recommended threshold limit. In contrast, the MTDI values were lower than the daily intake of all heavy metals through vegetable consumption. Human health risk assessment of Cd based on ΣILCR values was found to be higher than the threshold limit (ΣILCR > 10−4) for both adults and children, indicating the lifetime cancer risk due to the consumption of Cd-contaminated vegetables. The potential non-cancer risk was also observed from AW and WC samples, and the THQ of each heavy metal was below the threshold limit (THQ < 1.0) (except Ni in few samples), indicating that consumers have no non-cancer risk of analyzed heavy metals (except Ni) when exposed to a single heavy metal. In contrast, the obtained HI values were found to be higher than 1.0 in contaminated WC and AW for adults and children, which represent the non-cancer risk when exposed to all the heavy metals. Therefore, extensive research on heavy metals in all other vegetables growing in the Narsingdi district is recommended, as it significantly increases the intake of these dangerous and toxic metals, endangering the health of biota.