Concentration of heavy metals in vegetables and potential health risk assessment in China

  • Taiyang Zhong
  • Dawei Xue
  • Limin Zhao
  • Xiuying Zhang
Original Paper

Abstract

Food safety is an important issue in the world. This study assessed the health risk for the Chinese public when consuming vegetables grown in China, based on 1335 data records from 220 published papers during 2007–2016. The results showed that the average of Pb, Cd, and Hg concentration in vegetables was 0.106, 0.041, and 0.008 mg/kg, which were lower than the maximum allowable concentrations, respectively. Leaf vegetables contained higher heavy metals than root vegetables and fruit vegetables. On a provincial scale, the highest Pb, Cd, and Hg concentrations in vegetables were determined by those in soil and atmosphere. The total health risk index showed that people in Guizhou, Yunnan, Guangxi, Hunan, Guangdong, Hubei provinces in southern China, and Liaoning Province in northeast China, faced a high risk of Pb, Cd, and Hg when consuming vegetables.

Keywords

Heavy metal concentrations Vegetables Health risks China 

Introduction

People can be exposed to toxic pollutants through several pathways, including inhalation of soil particles, water drinking, oral intake, and dermal contact (Al-Saleh et al. 2004; Liu et al. 2013). Recent studies in Guizhou and Zhejiang provinces of China showed that the consumption of food was the primary metal exposure pathway for local residents in inland areas (Zhang et al. 2010; Li et al. 2012). Vegetable is an important component of the human diet in China (Xin et al. 2015). They supply dietary fiber, essential vitamins, minerals and trace elements. China is now the largest vegetable producer and consumer in the world. Thus, the Chinese government and the public pay close attention to the safety of vegetables.

Heavy metals, including lead (Pb), cadmium (Cd), and mercury (Hg), are the key pollutants in vegetables. These metals can bind to vital cellular components, such as structural proteins, enzymes, and nucleic acids and interfere with their functioning (Landis et al. 2000). Heavy metal accumulation in vegetables is of growing concern since both soils and irrigation waters have been shown to be polluted by heavy metals in some areas, due to the rapid industrialization and the wide application of agrochemicals in agricultural activities in China (Zhu et al. 2008; Zhang et al. 2015c).

In recent years, lots of studies have investigated heavy metal concentrations in vegetables in the local markets in China and assessed the health risk to the public. For example, Pan et al. reported the levels of As, Cd, Ni, Cr, Hg and Pb in Zhejiang Province and reported 0.25% of samples for Cd and 1.56% for Pb exceeding the maximum allowable concentrations (MAC) set by the Chinese Health Ministry (Pan and Wu 2016). Also, similar investigations have been conducted in Liuzhou of Guangxi Zhuang Autonomous Region (Peng 2014), Lanzhou of Gansu Province (Qin et al. 2013), Lianyungang in Jiangsu Province (Shang et al. 2016), Chongqing (Zhang and Chen 2012), Beijing (Wang et al. 2015), and so on. Although many investigations on heavy metal accumulations in market vegetables on a regional scale have been conducted, little is known on a national scale in China.

Since it is not easy to investigate the large area (arable land areas, 1,353,850 km2) of grains and vegetables planted throughout China in a short time, Zhang et al. (2015c) evaluated the impact of soil heavy metal pollution on food safety in China based on the collected pollution rate of soil samples. They concluded that about 13.86% of grain production was affected due to the heavy metal pollution in farmland soil. Also, Wang et al. (2016) evaluated the Hg concentrations in agricultural soil and assessed its influence on food production based on the Environment Quality Standard for soil in China (GB15618-1995) and found that 4.2% of agricultural land in China should be abandoned due to Hg pollution, and 2.0% faced a high risk of Hg pollution (Wang et al. 2016). Moreover, there are several studies on health risk assessment by heavy metals on a national scale. For example, the soil heavy metal pollution from mines was reviewed, and the health risk was assessed (Li et al. 2014); the health risk from heavy metals in soil of the urban environment was evaluated (Liu et al. 2016); and the carcinogenic and non-cancer risks by As on human health through diet in China were assessed (Zhang et al. 2016).

The above-mentioned studies on food safety and human health were assessed from the heavy metal concentrations in arable soil on a national scale, which is based on the principle that soil heavy metals were absorbed by the plants’ roots, and then transferred to the edible parts (Meng et al. 2014). However, different types and parts of plants have different uptake abilities regarding heavy metals from soil (Al Mamun et al. 2016; Roba et al. 2016). Also, the edible parts of the plant, particularly for the leaf vegetables, could absorb heavy metals from atmosphere. Thus, a health risk assessment based on heavy metal concentration in soils will bring a large uncertainty when assessing health risk and food safety.

This study aimed to directly assess the health risk for the public when consuming vegetables, based on metal concentrations in market vegetables. First, the relevant studies on Pb, Cd, and Hg concentrations in market vegetables were collected from the published papers during 2007–2016; second, the levels of heavy metals in vegetables were calculated; third, the provincial distribution of heavy metals in vegetables was mapped; and eventually the total health risks from Pb, Cd, and Hg to the public in China were evaluated.

Data collection and methods

Data collection

The concentrations of Pb, Cd, and Hg, in the edible parts of vegetable were collected from papers published during 2007–2016. The collected samples came from vegetables sold in the market and planted in the field. Here we hypothesized that vegetables will be firstly provided in the local market. In total, 1335 data records on vegetable heavy metals in 220 peer-reviewed articles were collected. The studies were located by searching through (1) the ISI Web of Knowledge website using the key words “Pb, Cd, or Hg” or “heavy metal,” “vegetables,” and “China,” and (2) the CNKI website using the Chinese key words of the mentioned. Also, some studies were collected from the references of the collected papers from CNKI and ISI. The spatial distribution of collected samples is described in Fig. 1.
Fig. 1

Spatial distribution of the collected samples at point and provincial scales

Since the concentrations of heavy metals in vegetables were analyzed by different chemical analysis methods, there inevitably existed gaps of the heavy metal concentrations by different measurement techniques. However, an internal control was used to control the data quality in most of the collected studies. For example, the citrus leaves (GBW10020 (GBS-11)) were assayed during heavy meal analysis in leaf vegetables for quality control (Chang et al. 2014); the cabbage (GBW10014), celery (GBW10048), and green Chinese onion (GBW10049) were used for validation of the analytical procedure of heavy metal concentration in vegetables (Xu et al. 2013); a poplar leaf (GBW07604(GSV-3) was used as a part of the quality control protocol (Zheng et al. 2007). These internal controls guaranteed the consistence of heavy metal concentrations measured from different techniques.

Concentrations of individual heavy metal in vegetables

The sample numbers in each study are used as the weights when calculating the averaged concentration of heavy metals in vegetables due to the considerable variations of sample numbers in each data record. This means that the study with more vegetable samples would give a greater contribution to the concentrations or the pollution rates on a regional or national scale. The sample-number-weighted mean of the concentrations (Cj) of the heavy metal j is calculated as:
$$C_{j} = \frac{{C_{i,j} \times N_{i,j} }}{{\sum\limits_{i = 1}^{n} {N_{i,j} } }}$$
(1)
where i is the data record i, j is the heavy metal j, Ni,j is the sampling number in the data record i for the heavy metal j. Cij and Ni,j could be obtained from the original studies.

Health risk assessment

The US EPA model and its threshold values were employed to assess the potential human health risks posed by Pb, Cd, and Hg in this study. A hazard index (HI) approach to assess noncarcinogenic health risk is calculated:
$${\text{HI}} = {\text{HQ}}_{i} = \sum\nolimits_{i = 1}^{n} {\frac{{{\text{CDI}}_{i} }}{{{\text{RFD}}_{i} }}}$$
(2)
where the chronic hazard index (HI) is the sum of hazard quotient (HQi) of i-th heavy metal, and the hazard quotient (HQ) is the ratio of exposure to hazardous substances and is the chronic reference dose (RFDi) that is 0.0015, 0.0008 and 0.00014 mg kg−1 d−1 for Pb, Cd, and Hg, respectively.
The chronic daily intake (CDI) is calculated from consumption of main food stuff following the equations (Liu et al. 2013):
$${\text{CDI}} = \frac{{C \times {\text{IR}} \times {\text{EF}} \times {\text{ED}}}}{{{\text{BW}} \times {\text{AT}}}}$$
(3)
where C is the concentration for Pb, Cd, or Hg in vegetables, IR is the ingestion rate (kg/(person·day)) in each province, which can be obtained from the statistic books (National Bureau of Statistics of China 2011); BW is the average bodyweight (55.9 kg) (Ge 1992); ED is exposure duration of 30 years (USEPA 2011); EF is exposure frequency, 24 h/per day (h/d) (UDOE 2011); AT is the averaging time, 365 × ED d for noncarcinogens (USEPA 2011), 365 × 70 d for carcinogens (USEPA 2002).

Results and discussions

Concentrations of heavy metals in vegetables

The statistical information about the minimum, maximum, and the sample-number-weighted mean of the concentrations for Pb, Cd, and Hg is described in Table 1. The collected investigations covered all of the provincial-level administrative divisions except Taiwan Province, Tianjin, and Ningxia Hui Autonomous Region. The collected samples for Pb and Cd were above 27,000 and above 19,000 for Hg, indicating the investigated three metals had been well studied in vegetables. The concentration of Pb in vegetables ranged from 0 to 3.820 mg/kg, with a sample-number-weighted mean of 0.105 mg/kg. The range of Cd was from 0 to 1.900 mg/kg, with an average of 0.041 mg/kg. Hg concentrations ranged from 0 to 0.447 mg/kg, with an average of 0.008 mg/kg. Among the three metals, Pb showed a higher accumulation in vegetables than Cd and Hg. Although the maximum of Pb, Cd, and Hg we collected were much higher than their MAC, respectively, the averages of the three metals were lower than the MACs. This indicated that vegetables were generally safe for people to consume in China.
Table 1

Statistic information on the concentration of heavy metals in vegetables

 

Sample numbers

Averagea (mg/kg)

Minimum (mg/kg)

Maximum (mg/kg)

Pb

27,062

0.105

0

3.820

Cd

27,225

0.041

0

1.900

Hg

19,021

0.008

0

0.447

aAverage indicates the sample-number-weighted mean

The concentration of the heavy metals in vegetables is mainly by both transferring from soil and directly absoring from atmosphere. Availability of heavy metal ions in vegetables from soil is mainly influenced by the backgrounds and the characteristics of the soil. The magnitude of heavy metal background depends on the composition of the parent rock material from which the soil was derived (Zhong et al. 2016). The characteristics of the soil included pH, organic matter, clay content, Mn oxide concentration, and so on (Xian and Shokohifard 1989). Moreover, the concentrations of heavy metal in vegetables are also altered by innumerable environmental and human factors and by the nature of the plants (Sharma et al. 2007). For the non-leaf vegetables, the accumulation of metals in the edible parts mainly resulted in the translocation of metals from roots to vegetable tissues (Stalikas et al. 1997). This resulted in the higher concentration of heavy metals in root vegetables than in fruit vegetables (Table 2).
Table 2

Concentration of heavy metals in three kinds of vegetables (fresh weight)

 

Fruit vegetablesa

Root vegetables

Leaf vegetables

Sample numbers

Averageb (mg/kg)

Sample numbers

Averageb (mg/kg)

Sample numbers

Averageb (mg/kg)

Pb

8389

0.052

2756

0.068

9580

0.154

Cd

8625

0.019

2913

0.023

9729

0.061

Hg

5692

0.003

2043

0.004

672

0.014

aFruit vegetables include melon vegetables, kale vegetables, solanaceous vegetables, and legumes

bAverage, indicates the sample-number-weighted mean

Among the three kinds of fresh vegetables, leaf vegetables had the highest concentration of heavy metals. A similar result was also found by Yang and Chen (Yang et al. 2010; Chen et al. 2013). Leaf vegetables generally grow faster with higher transpiration rates than non-leaf vegetables (Luo et al. 2011), which enhances the concentration of metals taken up by plant roots in leaf vegetables. Furthermore, leaf vegetables are more susceptible to pollutant accumulation in the atmosphere. Some study confirmed that the risk elements contained in particulate matter represent a higher risk for human health via direct ingestion of the PM in vegetables than via soil–vegetable transport (Tremlova et al. 2013). This situation was particularly serious for Hg. In this study, the averaged Hg concentration in leaf vegetables was about 5 times than that in the other kinds of vegetables. An open top chambers experiment showed that the Hg concentrations in leaves of plants were significantly positively correlated with those in the air during the growth time (Niu et al. 2013), indicating the high absorption ability of Hg by leaf vegetables.

Spatial distribution of the concentration of heavy metals in vegetables

The spatial distortion of the Pb, Cd, and Hg concentrations in provinces of China is shown in Fig. 2. In vegetables, the highest Pb accumulation occurred in Yunnan, Guangxi, and Hunan Provinces, where Pb concentrations in arable soil were higher than 100 mg/kg (Zhang et al. 2015a). In these three provinces, the Pb concentrations in vegetables were even higher than the MAC in vegetables, indicating that consuming vegetables grown here will bring the local residents a high health risk. Also, Guangdong Province had Pb concentration in vegetables higher than 0.150 mg/kg, which might be due to the fast economic development there. The famous Pearl River Delta of China, located in Guangdong Province, is home to an advanced manufacturing industry base and a service industry base. The fast development of industry and urban would bring heavy metal accumulated in the environment and eventually bring the high concentration in vegetables (Deng et al. 2010; Wu et al. 2011). Moreover, Guizhou, Hubei, Henan, Hebei Provinces also showed vegetable Pb concentrations higher than 0.100 mg/kg. Mining and smelting activities might be the main reasons for the accumulation of Pb from exterior sources in Hubei and Guizhou Provinces (Zhang et al. 2015a); irrigation by wastewater and mining activities might be the sources of Pb accumulation in Henan and Hebei Province (Liu 2011; Zhou et al. 2013). For the other provinces, Pb concentrations in vegetables were relatively lower than 0.100 mg/kg, so the people in those provinces faced a low health risk when consuming locally grown vegetables.
Fig. 2

Spatial distribution of Pb, Cd, and Hg concentration in vegetables on a provincial scale

On the map of Cd concentrations in vegetables, no province had an averaged Cd concentration higher than the MAC. Hunan Province had the highest value in China, with a sample-number-weighted mean of 0.144 mg/kg. Hunan Province has a large amount of mining and smelting activities, which might result in the high Pb and Cd concentrations in the environment (Lei et al. 2008; Wei et al. 2009). The provinces of Yunnan, Guizhou, and Guangxi also showed high Cd concentrations in vegetables, which also could be mainly due to the mining and smelting activities. For the four provinces mentioned above, the Cd concentrations in arable soil ranked as the top four in China (Zhang et al. 2015b), which were resulted from the large amount of nonferrous metal reserves in these regions. For the other provinces, the Cd concentrations in vegetables were relatively lower than 0.060 mg/kg, indicating a low health risk from Cd when consuming vegetables.

On the map for Hg in vegetables, Guizhou Province had the highest value, exceeding the MAC of 0.02 mg/kg, due to the highest reserves of Hg sources in China. Since the Hg mining and smelting activities emitted a large amount of Hg into the atmosphere and soil, leading to the high Hg accumulation in vegetables. Soil Hg concentrations in Hg mining areas in Guizhou province could reach 150.00 mg/kg (Qiu 2005; Cong and Cong 2009), about 500 times the grade II reference in agricultural soil. Also, Guangxi and Jiangsu Province had high Hg concentrations in vegetables, which might be due to the high Hg concentrations from parent materials (0.289 mg/kg in Jiangsu Province and 0.152 mg/kg in Guangxi Province, which were ranked top two in China) (China Environmental Monitoring Center 1990). For the other provinces, Hg concentrations in vegetables were relatively lower than 0.01 mg/kg, half of the MAC for Hg in vegetables.

The spatial variation of the three metals in vegetables showed a little difference. On a national scale, the Pb concentration in vegetables showed higher than Hg and Cd. There were 8 provinces that had Pb concentrations in vegetables higher than 0.1 mg/kg, half of the MAC for Pb in vegetables, indicating these areas had high risk of Pb absorption for people when consuming vegetables, while only 1 and 3 provinces, respectively, had higher concentrations for the Cd and Hg concentration in vegetables than half of the MACs for the two metals. As discussed in “Concentrations of heavy metals in vegetables” section, the concentrations of metals in vegetables were mainly from soil, irrigation water, and atmosphere. Among the sources of metals, the soil might be the predominant source, particularly for the fruit and root vegetables. The concentrations of Pb, Cd, and Hg on a provincial scale were close to their spatial distributions in soil (Zhang et al. 2015ab; Wang et al. 2016).

Health risk assessment for consuming vegetables

Considering the three metals of Pb, Cd, and Hg in vegetables, the provincial HI ranged from 0.009 to 0.274, indicating strong spatial variations across China. The index in all of the provinces was much lower than 1, indicating people in China were generally safe for non-cancer risks from Pb, Cd, and Hg in consuming vegetables. In total, the high risks occurred in the southwest areas of China, while the remaining areas had relatively low risks (Fig. 3).
Fig. 3

Spatial distribution of health risk index from Pb, Cd, and Hg on a provincial scale

The total HI showed that the people in Guizhou Province faced the highest risk of Pb, Cd, and Hg in vegetables, with an HI value of 0.274. Guangxi Zhuang Autonomous Region, Yunnan Province, and Hunan Province were the next highest risk regions, with an HI of 0.167, 0.152, and 0.140, respectively. As we discussed in “Spatial distribution of the concentration of heavy metals in vegetables” section, these four provinces faced a high risk of Pb, Cd, and Hg mainly because of the related mining and smelting activities in those areas. Guangdong and Hubei provinces were within the risk index of 0.05 to 0.10. The remaining provinces were relatively safe from Pb, Cd, and Hg pollution.

Although the averaged HI showed that all of the provinces faced relatively low risks of Pb, Cd, and Hg through consuming vegetables, the issue of heavy metal pollutions in foods still should be paid attention. In this study, we only assessed the risk of three specific metals in vegetables due to the limited data we collected. If the other metals, such as Ni, Cr, and As, were considered, the total risk might be higher. For example, the soil As accumulation in some parts of China has increased as a result of mining and smelting, irrigation with As-contaminated groundwater and the application of arsenic pesticides and fertilizers (Zhang et al. 2016), which might lead to the increase of As in vegetables. Also, vegetables are only part of the foods for Chinese people consuming. About one-third of the total food consumed were vegetables, according to the food consumption structure in 2012 (National Bureau of Statistics of China 2011). If all of the pollutants in food and all of the food people consumed are considered, the risk would get high, particularly for the people in the high-risk areas of the southwest areas in China. Certainly, the Chinese government has noticed the seriousness of food pollution and has enacted a series of measures to prevent or allocate the serious pollutions (Hu et al. 2014).

Limitations and uncertainties

This study assessed the health risk of the public consuming vegetables, based on the investigation of Pb, Cd, and Hg concentrations in vegetables. However, there are still some limitations and uncertainties since this study was based on the collected data from the published papers. First, the collected samples were not evenly distributed over China, which would impact the consistency of the evaluation of the health risk. Second, the collected numbers of the samples for some kind of metals in some provinces, such as Hg in Hubei and Qinghai Province, and Pb in Liaoning, were relatively small, which would also influence the assessment result on health risk. Third, the vegetable samples were collected both from market and the field. The market vegetables were consumed by the local residents, which were proper to be used in the health risk assessment, while the field vegetables might be consumed by the local residents or be traded to other areas. If the samples from field were consumed in the other areas, which would brought some uncertainty when evaluating health risk.

Conclusions

Based on the collected data from the published studies, the average amounts of Pb, Cd, and Hg in vegetables in China were 0.105, 0.041, and 0.008 mg/kg, respectively. This averaged Pb, Cd, and Hg were lower than the MAC for each metal. Among the three kinds of vegetables, leaf vegetables had the highest metal concentrations in the edible parts, and then the root vegetables and fruit vegetables followed.

The spatial variation of Pb, Cd, and Hg on a provincial scale in China has been obtained, which were greatly influenced by the background from parent materials and human activities. The vegetable Pb pollution showed more serious than Hg and Cd in China, since 8 provinces had Pb concentrations in vegetables higher than 0.1 mg/kg, half of the MAC for Pb in vegetables, while only 1 and 3 provinces, respectively, had higher concentrations than half of the MACs for Cd and Hg. This indicated that the public faced higher health risk from Pb than Cd and Hg when consuming vegetables.

Considering the three metals of Pb, Cd, and Hg in vegetables, the provincial HI ranged from 0.009 to 0.274, indicating people in China were generally safe for noncancerous risks when consuming vegetables. The four provinces in southern China, Guizhou, Yunnan, Guangxi, and Hunan Province had the highest health risk for the public, and then the provinces of Guangdong, Hubei and Liaoning followed.

Certainly, this study only assessed the health risk from the Pb, Cd, and Hg pollution in vegetables. Further studies should address the other metals or the other kind of pollutants including the chemical fertilizers or pesticides, since bad effects on human health from the various pollutants could be accumulated in the body. Moreover, the other kinds of food, such as grains, fishes, or meats also should be addressed due to the various kinds of foods consumed by people.

Notes

Acknowledgements

This study is supported by the National Natural Science Foundation of China (No. 41271190).

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Copyright information

© Springer Science+Business Media Dordrecht 2017

Authors and Affiliations

  • Taiyang Zhong
    • 1
  • Dawei Xue
    • 2
  • Limin Zhao
    • 3
    • 4
  • Xiuying Zhang
    • 3
  1. 1.School of Geographic and Oceanographic SciencesNanjing UniversityNanjingChina
  2. 2.College of Biology and Environmental ScienceHangzhou Normal UniversityHangzhouChina
  3. 3.Jiangsu Provincial Key Laboratory of Geographic Information Science and Technology, International Institute for Earth System ScienceNanjing UniversityNanjingChina
  4. 4.Jiangsu Center for Collaborative Innovation in Geographical Information Resource Development and ApplicationNanjingChina

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