3.1. Trace elements in rice grown in study sites
The average trace element concentrations in rice samples were highest for Ni, followed by Cr, As, then Cd, and lowest for Pb (Table 1; Fig. 2). Thanh Hoa had the highest levels of trace element contamination in rice, particularly Cr, As, and Pb, followed by Ha Tinh, and Nghe An had the lowest levels (Table 1).
Table 1
Concentrations of Cr, Ni Cd, Pb, and As in rice collected from Thanh Hoa, Ha Tinh and Nghe An provinces. Values are expressed as average ± standard deviation
Province
|
Cr
|
Ni
|
As
|
Cd
|
Pb
|
Thanh Hoa
|
Quang Xuong
|
0.43±0.17
|
0.27 ± 0.071
|
0.13 ± 0.034
|
0.013 ± 0.004
|
0.05 ± 0.02
|
Bim Son
|
0.39 ± 0.20
|
0.29 ± 0.048
|
0.19 ± 0.023
|
0.022 ± 0.005
|
0.011 ± 0.002
|
Nghi Son
|
0.091 ± 0.058
|
0.12 ± 0.028
|
0.21 ± 0.018
|
0.007 ± 0.001
|
0.010 ± 0.003
|
Average
|
0.30 ± 0.11
|
0.22 ± 0.054
|
0.17 ± 0.025
|
0.014 ± 0.005
|
0.024 ± 0.013
|
Ha Tinh
|
Nghi Xuan
|
0.034 ± 0.0051
|
0.23 ± 0.065
|
0.14 ± 0.008
|
0.061 ± 0.022
|
0.013 ± 0.001
|
Duc Tho
|
0.024 ± 0.0022
|
0.16 ± 0.010
|
0.12 ± 0.020
|
0.091 ± 0.018
|
0.006 ± 0.002
|
Ky Anh
|
0.028 ± 0.0051
|
0.36 ± 0.071
|
0.16 ± 0.011
|
0.11 ± 0.039
|
0.013 ± 0.003
|
Average
|
0.029 ± 0.0030
|
0.25 ± 0.058
|
0.14 ± 0.014
|
0.088 ± 0.015
|
0.011 ± 0.002
|
Nghe An
|
Nghia Dan
|
0.045 ± 0.013
|
0.15 ± 0.044
|
0.078 ± 0.008
|
0.015 ± 0.011
|
0.007 ± 0.001
|
Do Luong
|
0.037 ± 0.010
|
0.17 ± 0.039
|
0.15 ± 0.008
|
0.045 ± 0.012
|
0.010 ± 0.002
|
Hung Nguyen
|
0.026 ± 0.004
|
0.36 ± 0.092
|
0.16 ± 0.011
|
0.097 ± 0.030
|
0.014 ± 0.003
|
Thanh Chuong
|
0.038 ± 0.004
|
0.18 ± 0.027
|
0.18 ± 0.006
|
0.038 ± 0.013
|
0.007 ± 0.001
|
Average
|
0.036 ± 0.004
|
0.21 ± 0.048
|
0.14 ± 0.021
|
0.049 ± 0.017
|
0.009 ± 0.002
|
WHO permissible limits (CAC, 2019)
|
1.30
|
10
|
0.2
|
0.04
|
0.2
|
High concentrations of Ni (mg kg−1 dw) were found in Hung Nguyen (0.36 ± 0.092), Nghe An, in Ky Anh (0.35 ± 0.071) and Nghi Xuan (0.23 ± 0.065), Ha Tinh, and in Bim Son (0.29 ± 0.045) and Quang Xuong (0.27 ± 0.071), Thanh Hoa. The highest concentrations of Cr (mg kg−1dw) were found in Thanh Hoa, with an average concentration of 0.30 ± 0.11, which was about ten times higher than in other provinces (Nghe An: 0.036 ± 0.004; and Ha Tinh: 0.029 ± 0.03; Table 1). Cr concentrations in Quang Xuong, Bim Son, and Nghi Son were 0.43 ± 0.17, 0.39 ± 0.20, and 0.091 ± 0.058, respectively (Fig. 2, Table 1).
According to the previous study (Huang et al., 2007), Cr was found in rice at relatively high concentrations of 0.29 ± 0.14 (in Changshu) and 0.107 (Taizhou). This study indicated that industrial activities might have been influenced the concentrations of Cr in rice from Changshu's area. According to Kien (Kien et al., 2010), the Co Dinh chromite mine (Thanh Hoa) contaminated lowland paddy fields with Cr, Ni, and Co, posing significant health risks through agricultural products. He also stated that water contaminated with Cr and Ni in the mining area could pollute nearby rivers. In our study, the Cr and Ni levels were well correlated with industrial and mining activities. Especially in Thanh Hoa, the ultramafic outcrops are rarely exposed and severely weathered; hence, trace elements are diluted and sedimented in the Ma River delta plain, where Quang Xuong and Bim Son are located. The distances between these two districts and the chromite mine (Co Dinh) are approximately 16 km and 50 km, respectively. Additionally, several sites of construction material mining (Ky Anh and Nghi Xuan) and industrial activities may also be factors in the high concentration of trace elements in rice from Hung Nguyen district, Nghe An province (about 12-15 km to the industrial zones of Bac Vinh and Nam Cam), or from Ky Anh district, Ha Tinh province (next to the industrial zones of Vung Ang), and Bim Son district, Thanh Hoa province (less than 10 km from Bim Son industrial zone).
The average concentrations of As (mg kg−1 dw) in rice samples collected from Thanh Hoa, Ha Tinh, and Nghe An were 0.173 ± 0.025, 0.139 ± 0.014, 0.139 ± 0.021, respectively. There have been several studies that have investigated the As contents in rice, and our findings were comparable to those reported in other studies conducted in the Red River Basin (from 0.053 to 0.469 mg kg−1 dw) (Tran et al., 2020) and near the mining sites (0.052 mg kg−1 to 0.328 mg kg−1 dw) (Chu et al., 2021). However, the average As concentration in the current study was less than 0.2 mg kg−1 (the threshold recommended by the FAO-WHO Codex Alimentarius Commission (CAC, 2019), and the As contents of samples collected from Bim Son and Nghi Son were slightly higher. According to Tran's study (Tran et al., 2020), grain As content gradually increases from mountainous and hilly regions to lowland (coastal) regions, whereas soil As content does not. In other words, the high concentration of As in rice could be due to factors other than natural sources, such as anthropogenic activities and especially the bioavailable forms of this element. Besides, mining activity could be a significant factor in rice's high As content (Chu et al., 2021). Irrigation with arsenic-contaminated water in rice fields raises the concentration of As in the topsoil and its bioavailability to rice crops (Azam et al., 2016). As accumulation in rice grains is increased due to As in paddy rice's high bioavailability and mobility (Xu et al., 2008). In our study, the lowest As content was found in samples from Nghia Dan, which is located in the highlands and was far from industrial zones; whereas, high As levels were found in samples from Bim Son (near the Bim Son industrial zone), Nghi Son (near the Nghi Son refinery and petrochemical factory, Nghi Son iron and steel company, Nghi Son Cement company), and Ky Anh (right next to the Vung Ang industrial park-seaport complex).
The highest Cd levels (mg kg−1 dw) were found in Ha Tinh (0.061 ± 0.022 to 0.11 ± 0.039), followed by Nghe An (0.015 ± 0.011 to 0.097 ± 0.030), and Thanh Hoa (0.007 ± 0.001 to 0.022 ± 0.005) (Table 1, Fig. 2). Interestingly, 60% and 40% of the rice samples collected from Ha Tinh and Nghe An, respectively, contained Cd levels above CODEX permissible limits (CAC, 2019). In comparison to the present findings, some studies have found lower Cd concentrations in rice, e.g., the Red River basin (0.033 mg kg−1 dw) (Bui et al., 2016) and Changshu city (0.019 mg kg−1 dw) (Hang et al., 2009). However, others reported that the Cd concentrations in rice cultivated from the mining sites in Hunan province (0.103 mg kg−1 dw) (Fan et al., 2017), the Yangzhong district (0.224 mg kg−1 dw) (Hang et al., 2009) and the Jin-Qu basin (0.163 mg kg−1 dw) (Guo et al., 2020) were higher than our data.
Pb concentrations (mg kg−1 dw) in the rice samples ranged considerably from 0.006 ± 0.002 (Duc Tho) to 0.050 ± 0.015 (Quang Xuong). Thanh Hoa's average Pb content was at least twice that of Ha Tinh and Nghe An. In comparison to other studies from the Red River Delta (0.075 mg kg−1 dw) (Chu et al., 2021), the Yangtze River Delta (0.957 mg kg−1 dw) (Hang et al., 2009), and the Jin-Qu Basin (0.148 mg kg−1 dw) (Guo et al., 2020), the current results showed lower Pb levels.
Mining and industrial activities could be the sources of Pb and Cd in rice grain. Another report (Hang et al., 2009) found that the erosion of these metals from e-waste recycling activities could be discharged into the surrounding environment, indicating contamination by these elements in the studied areas. Guo et al. (2020) also reported that Cd contamination in rice grains was higher in the Jin-Qu Basin than in other cultivation areas, which nonferrous metal plants could influence. This similar condition could account for the high Cd content of rice from Ha Tinh province. Ky Anh is home to the Vung Ang industrial zone, which includes a thermal power plant and a steel factory, and the industrial activities in that area may result in high Cd levels in rice. On the other hand, Pb could be introduced into rice grains through atmospheric deposition during metal-mining activities via dust and particulate material deposition. Other studies have discovered that Cd and Pb quickly transfer from soils, particularly in mining areas, and accumulate in vegetables and rice (Zhuang et al., 2009; Bui et al., 2016; Mao et al., 2019).
3.2. Daily intakes of trace elements via rice consumption and the risk to human health
3.2.1. Estimated dietary intake of trace elements
Although there are numerous pathways through which humans can be exposed to trace elements, rice consumption has been identified as one of the major routes. This means that human exposure to these contaminants will increase as rice consumption increases in Vietnam. The non-carcinogenic and carcinogenic health risk assessments of trace elements can be calculated and evaluated using the method of health risk assessment provided by the US EPA (US EPA, 2021). Table 2 depicts the dietary intake of trace elements from rice consumption for adults (both male and female) and children (including boys and girls under the age of five), assuming that the local population primarily consumes local rice.
Table 2
Estimated daily intakes (EDI) of heavy metaltrace elements from rice for adults and children (under 5 yearfive years old). The values are expressed as the average ± standard deviation
Location
|
Thanh Hoa
|
Ha Tinh
|
Nghe An
|
Cr
|
Male
|
1.66 ± 0.58
|
0.16 ± 0.03
|
0.20 ± 0.02
|
Female
|
1.96 ± 0.67
|
0.18 ± 0.03
|
0.24 ± 0.02
|
Baby boy
|
3.78 ± 1.33
|
0.34 ± 0.05
|
0.45 ± 0.05
|
Baby girl
|
4.07 ± 1.43
|
0.37 ± 0.06
|
0.49 ± 0.05
|
Ni
|
Male
|
1.23 ± 0.30
|
1.35 ± 0.32
|
1.17 ± 0.26
|
Female
|
1.45 ± 0.35
|
1.60 ± 0.38
|
1.34 ± 0.33
|
Baby boy
|
2.80 ± 0.68
|
3.08 ± 0.73
|
2.67 ± 0.60
|
Baby girl
|
2.91 ± 0.84
|
3.32 ± 0.79
|
2.88 ± 0.65
|
As
|
Male
|
0.95 ± 0.14
|
0.76 ± 0.07
|
0.76 ± 0.12
|
Female
|
1.12 ± 0.16
|
0.90 ± 0.09
|
0.87 ± 0.14
|
Baby boy
|
2.16 ± 0.31
|
1.73 ± 0.17
|
1.74 ± 0.27
|
Baby girl
|
2.33 ± 0.33
|
1.89 ± 0.18
|
1.87 ± 0.29
|
Cd
|
Male
|
0.08 ± 0.03
|
0.48 ± 0.08
|
0.27 ± 0.10
|
Female
|
0.09 ± 0.03
|
0.57 ± 0.10
|
0.31 ± 0.11
|
Baby boy
|
0.17 ± 0.06
|
1.09 ± 0.18
|
0.61 ± 0.22
|
Baby girl
|
0.19 ± 0.06
|
1.18 ± 0.20
|
0.66 ± 0.23
|
Pb
|
Male
|
0.13 ± 0.07
|
0.06 ± 0.01
|
0.05 ± 0.01
|
Female
|
0.15 ± 0.09
|
0.07 ± 0.01
|
0.06 ± 0.01
|
Baby boy
|
0.30 ± 0.16
|
0.13 ± 0.03
|
0.11 ± 0.02
|
Baby girl
|
0.32 ± 0.18
|
0.14 ± 0.03
|
0.12 ± 0.02
|
EDI trends for trace elements in rice were in the order of Cr ˃ Ni ˃ As ˃ Pb ˃ Cd. The highest EDI of Cr (4.1 µg d−1) in Thanh Hoa, Ni (3.3 µg d−1) in Ha Tinh, As (2.3 µg d−1) in Thanh Hoa, Cd (1.2 µg d−1) in Ha Tinh, and Pb (0.49 µg d−1) in Nghe An were observed. Among the investigated population groups, the baby group was estimated to have the highest intake of all five trace elements via consumption of about 205 g rice day−1. Because of the bodyweight effect, males (59.4 kg) with rice consumption of 325 g day−1 had the lowest EDI values. The EDIs for Cr, As, and Cd from rice consumption in both adults and children under five years old in this study are higher than those in the Yangtze River Delta, China (Hang et al., 2009; Mao et al., 2019), but lower than those in the mining areas of the Jin-Qu Basin (Guo et al., 2020) and Dabaoshan mine (Zhuang et al., 2009). On the other hand, the present data showed that the average EDI values for As, Cr, Ni, and Pb in the adult group from three studied provinces were higher than those found in the Red River Delta (Chu et al., 2021).
The lower EDIs in the adult group than the children group (under five years old) in this study are consistent with previous findings (Nguyen et al., 2021; Hang et al., 2009; Mao et al., 2019; Zheng et al., 2007). Even though rice consumption is very high in Vietnam, the EDI values for all trace elements for adults and children are lower than the RfD. In China, daily rice consumption ranged between 238 - 389 g person−1 day−1 (Hang et al., 2009; Guo et al., 2020; Mao et al., 2019) for adults, with children consuming 198 g person−1 day−1 (Hang et al., 2009; Mao et al., 2019), whereas Vietnamese adults and children under five years old consume 325 and 205 g person−1day−1, respectively. In addition, a previous study (Nguyen et al., 2021) discovered that the exposure dose of As from rice consumption varied across age groups and gender due to rice intake and body weight differences. According to the authors, females consumed more As than males, and children consumed more As than adults per day due to a higher rice intake/body weight ratio.
3.2.2. Potential health risk of individual trace elements
Although adults consume more rice than children, the THQ values of trace elements for adults were lower than those for children (Fig. 3). THQ values of As were the highest, exceeding 1, implying that people were exposed to health risks from consumption As contaminated rice. Furthermore, the levels of Cd and Cr in some sampling sites could pose health risks to rice consumers. For adults, the THQs from rice consumption are in decreasing order As > Cd > Cr > Ni > Pb. THQs for children under five are comparable to those for adults. According to the current findings, As ingestion from rice poses the highest potential health risk for both adults and children under five groups, while Ni ingestion poses the least risk for the population studied. In this study, the differences in health risk between the three provinces were also compared. In general, Thanh Hoa had the highest THQs for studied elements, followed by Ha Tinh and Nghe An (Fig. 3). This result indicated that the inhabitants of Thanh Hoa suffered more adverse health effects as a result of consuming rice than residents of other provinces.
THQ values of As for adults in Thanh Hoa, Nghe An, and Ha Tinh were 3.1 ± 0.45 to 7.8 ± 1.1, 2.5 ± 0.25 to 6.2 ± 0.68, and 2.5± 0.39 to 6.3 ± 0.96, respectively (Fig. 3). THQs of As for children under five years old, particularly baby girls, were 2 to 2.5 times higher than adults, implying that rice consumption may pose serious health risks depending on gender and age group. The current study's As-THQs for adults and children were significantly higher than those in the Yangtze River Delta, which were 0.028 and 2.3 (Hang et al., 2009), and 0.024 and 2.7 (Mao et al., 2019), respectively. The discrepancy in THQ values could be attributed to THQ's effective parameters and their variations across geographic regions. Furthermore, children under five in Thanh Hoa and Ha Tinh may face higher health risks because of Cr and Cd, respectively. In fact, this risk assessment was based not only on trace element levels in rice, but also on rice consumption rates. According to other studies, Vietnamese adults consume more rice (325 g day−1) than their counterparts in China, Japan, and Taiwan (238, 119, and 132 g day−1, respectively). Therefore, it can be explained that Vietnamese people primarily consume rice as a carbohydrate source, whereas wheat, buckwheat, and other grains are consumed in other Asian countries.
3.2.3. Potential health risks of combined trace elements and Target cancer risks
The HI was calculated by considering the cumulative effect of consuming five potentially hazardous elements from rice (Fig. 4). The calculated HI values range from 1.7 for males in Nghia Dan (Nghe An) to the highest value of about 11 for girls under five in Bim Son (Thanh Hoa). The current HI results were significantly higher than those in previous studies (Hang et al., 2009; Guo et al., 2020; Zheng et al., 2007; Antoine et al., 2017). The HI trends were as follows: Bim Son > Nghi Son > Ky Anh > Hung Nguyen ~ Thanh Chuong > Quang Xuong > Nghi Xuan ~ Do Luong > Duc Tho > Nghia Dan. According to our findings, As is a key component contributing to the potential health risk of non-carcinogenic effects in adults and children, with Cr and Cd serving as secondary components.
Because Cr and Ni are essential micronutrients for human health, moderate levels of Cr and Ni found in rice samples may pose a significant health risk (Uriu-Adams and Keen, 2005). Many studies have found that people are exposed to metals through other foods such as wheat, vegetables, fruit, fish, meat, eggs, water, and milk (Bui et al., 2016; Zheng et al., 2007; Antoine et al., 2017). However, Asians consume much rice on a daily basis; therefore, rice is a significant pathway for local people's dietary exposure to metals or toxic elements through food. Hence, local inhabitants need to reduce their rice consumption and diversify their diets to reduce the health risks associated with dietary Cd and As intake. It is noteworthy that this study did consider special groups, such as women and children under the age of five, who are presumably more vulnerable to pollutants with both non-carcinogenic and carcinogenic effects. Furthermore, the fact is that the average HI values for girls under five were 1.5 times higher than for other groups.
Only Ni and Pb were considered for target cancer risk (TR) assessment in this study (Table 3, Fig. 5). TR values for Ni and Pb ranged from 4.29 × 10−7 to 3.03 × 10−3, indicating a potential carcinogenic risk to rice consumers in most investigated areas, particularly Ha Tinh and Thanh Hoa (Table 3), with Ni showing the highest cancer risk (TR > 1 × 10−3). In Ha Tinh, the risks come from Ni for adults and children under five years old were 1.45 × 10−3 (female) and 3.03 × 10−3 (girls under five years old), implying that 145 per 100,000 adults and 303 per 100,000 baby girls under five years old are at the highest risk of cancer caused by Ni intake from rice. Following publications that used 10−6 to 10−4 as the range for acceptable risk of developing cancer (Antoine et al., 2017; Shaheen et al., 2016), 10−4 was accepted as the upper limit. In this study, high cancer risk would be expected to be associated with Ni (Fig. 5; Table 3). The cancer risk calculated for Pb was within the low or acceptable range of 10−7 to 10−5, indicating that the cancer risk from Pb-contaminated rice consumption in the three provinces studied was tolerable. However, the total cancer risk (TCR) analysis revealed the potential adverse cancer risk induced by Ni and Pb from rice consumption, as the TCR values were significantly higher than the threshold level (> 10−6) at all sampling sites.
Table 3
Target cancer risk (TR) of trace elements from rice consumption in adults and children (under five years old). TR < 1 × 10−6, insignificant risk; 1 × 10−6 < TR < 1 × 10−4, low or acceptable risk range; and 1 × 10−3 < TR < 1 × 10−1, high cancer risk levels
|
Groups
|
Ni
|
Pb
|
Thanh Hoa
|
Male
|
1.12E-03
|
1.11E-06
|
Female
|
1.32E-03
|
1.31E-06
|
Baby boy
|
2.55E-03
|
2.53E-06
|
Baby girl
|
2.75E-03
|
2.73E-06
|
Ha Tinh
|
Male
|
1.23E-03
|
5.00E-07
|
Female
|
1.45E-03
|
5.91E-06
|
Baby boy
|
2.80E-03
|
1.14E-06
|
Baby girl
|
3.03E-03
|
1.23E-06
|
Nghe An
|
Male
|
1.07E-03
|
4.29E-07
|
Female
|
1.22E-03
|
4.86E-07
|
Baby boy
|
2.43E-03
|
9.77E-07
|
Baby girl
|
2.62E-03
|
1.05E-06
|
In summary, the findings indicated a significant human health risk (both non-carcinogenic and carcinogenic) associated with the consumption of rice grown in most of the studied areas. As a result, strict regulatory control over the safety of vegetables originating in North-Central Vietnam should be implemented.