Cadmium, Arsenic and Mineral Nutrients in Rice, and Potential Risks for Human Health in South China

doi:10.21203/rs.3.rs-1709663/v1

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Cadmium, Arsenic and Mineral Nutrients in Rice, and Potential Risks for Human Health in South China

https://doi.org/10.21203/rs.3.rs-1709663/v1

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Rice (Oryza sativa L.) is one of the most important staple food crop worldwide. For people fed on rice, toxic elements cadmium (Cd) and arsenic (As) and mineral nutrients in rice are pivotal to evaluate potential risks of harmful element intake and malnutrition. We collected rice samples of 208 cultivars (83 inbred and 125 hybrid) from fields in South China, and determined Cd, As, As species, and mineral elements in brown rice. Histochemistry analysis shows that Cd and As in brown rice were 0.26 ± 0.32 and 0.21 ± 0.08 mg·kg^− 1, respectively. Inorganic As (iAs) was the dominative As species in rice. Brown rice Cd and iAs in 35.1% and 52.4% of the 208 cultivars exceeded rice Cd and iAs limits. Significant variations of rice subspecies and regions were found for Cd, As and mineral nutrients in brown rice (P < 0.05). Inbred rice has lower As uptake and more balanced mineral nutrition than hybrid species. Significant correlation was observed between Cd, As versus mineral elements like Ca, Zn, B and Mo (P < 0.05). Health risk assessment indicates that high risks of Cd intake and malnutrition, in particular to Ca, protein and Fe, can be caused by rice consumption in South China.

Rice

Heavy metal

Arsenic species

Mineral nutrients

Health risk evaluation

Malnutrition

In the latest report of Food and Agriculture Organization of the United Nations (FAO), about 12% of the world's population (about 928 million) is short of food security, an increase of 148 million over 2019 (FAO, 2021). And, the global population suffered from malnutrition totalled 768 million in 2020, mainly in Asia, Africa and Latin America. Therefore, the production of staple food with sufficient amount and safe quality is of vital importance. Rice (Oryza sativa L.) is the most important food crop in the world, which feeds more than 50% of the world population (Muehe et al., 2019). The global rice production was about 800 million tons in 2018, of which 90% was produced in Asia (FAO, 2021). Hence, it is pivotal to ensure adequate supply of rice in Asia and the world.

Unfortunately, rice is prone to absorb some highly toxic elements such as cadmium (Cd) and arsenic (As), which is a major threat to food security and human health in Asia and the world (Zhao and Wang, 2020). Cd uptake efficiency of rice is 6.5- and 2.2-fold higher than that of wheat and maize respectively. Cd is translocated within rice plant through the manganese (Mn) transporter OsNRAMP5. The expression of homologous NRAMP5 gene in rice is far higher than that of wheat, maize and other crops (Sui et al., 2018). Meanwhile, the efficient accumulation of As in rice is ascribed to its own special physiological mechanism and its flooded growth environment. As a phosphate analogue, arsenate [As(V)] can be accidentally absorbed by rice through the phosphate transport system (Wang et al., 2016). Arsenite [As(Ⅲ)] enters rice root through silicate absorption channel (Lsi1), and transfers from root to shoot via silicon transporter Lsi2 (Ma et al., 2008). Low concentrations of methylated arsenic compounds like monomethylarsonic acid (MMA) and dimethylarsinic acid (DMA) exist in soil as well (Zhao et al., 2013). Lsi1 also mediates the uptake of methylated As in rice. Although the absorption efficiency of methylated As is lower than that of inorganic As (iAs), they are easily transported and accumulate in rice grains, which may be due to the low complexation between methylated As and thiol compounds and the concomitant low fixation efficiency in roots (Raab et al., 2007; Mishra et al., 2017).

Long-term exposure to Cd impacts human health, such as osteoporosis, lung cancer and prostate cancer (Waalkes, 2003; Järup and Åkesson, 2009). As is classified as a non-threshold class-1 carcinogen. Excessive As intake can cause skin cancer, lung cancer, liver cancer and so on. Furthermore, it poses irreversible impact on human cardiovascular system, nervous system and reproductive system (Mawia et al., 2020; Sarwar et al., 2021). Exposure to As during pregnancy of females affects the fetal development and increases the incidence of malignant diseases (Gilbert-Diamond et al., 2011). A recent survey shows that 7.96% of the 113 polished rice samples from China nationwide accumulates Cd higher than the national Cd limit for rice (Mu et al., 2019). Li et al. (2015) found that the average iAs contents of rice in Jiangxi, Hunan, Guangxi and Jilin were 0.25, 0.27, 0.26 and 0.29 mg·kg^− 1, respectively, all of which exceed the rice iAs limit in China (0.2 mg·kg^− 1). Therefore, rice Cd and As levels need to be widely investigated, and the potential health risk associated with Cd and As intake by rice consumption is worthy to be emphasized.

On the other hand, as a staple food, the abundance of mineral nutrients in rice are crucial to human health as well. In general, more than 80% of the components of rice grain is starch, and protein content is no more than 10% (Balindong et al., 2018). Besides, abundant zinc (Zn), iron (Fe), magnesium (Mg) and other trace elements in rice can meet the requirement of human beings for basic nutrition (Pinson et al., 2015). Imbalanced mineral elements in human diet lead to many health problems. For instance, Fe deficiency induces anemia, calcium (Ca) shortage causes osteoporosis in the elderly, and Zn insufficiency is related to growth retardation and hypophrenia. Copper (Cu) participates in the development of the central nervous system, and Mn is an ingredient of a range of enzymes (Viteri and Gonzalez, 2002; Zeng et al., 2010). Although a few of studies reports the concentrations of heavy metals and elements and the health risks caused by rice consumption in Southeast Asia (Nguyen et al., 2020a; Nguyen et al., 2020b), the mineral nutrition level of rice is underestimated, and the relation between Cd and As versus mineral nutrients is sedomly concerned up to date.

In the present study, the profile of Cd, As and typical mineral nutrients in brown rice of widely planted rice cultivars from the main production areas in South China were investigated. Further, the exposure risk of Cd and As and the malnutrition susceptibility of mineral nutrients associated with rice consumption were evaluated, with the objective to (1) determine the levels of Cd, As and mineral nutrients in rice; (2) adjust human diet based on health risk and malnutrition linked with rice consumption; (3) regulate rice cultivar planning in terms of varietal variation of Cd, As and mineral nutrients and geographical discrepancy; (4) provide insights to rice cultivar breeding with low Cd and As and high mineral nutrients.

Rice sample collection

Mature plant samples of 208 late rice cultivars were collected from late October to early December in 2020 in the main rice plantation areas in South China, where was located from 22°08′ N to 28°35 ′N and from 110°87 ′E to 116°20′ E (Fig. 1). The rice cultivars were planted in nine counties or cities, including Lufeng (LUF, 15), Huiyang (HUY, 21), Guangzhou (GUZ, 14), Qujiang (QUJ, 30), Wengyuan (WEY, 30), Gaozhou (GAZ, 19) and Xinxing (XIX, 58) of Guangdong province, 12 cultivars from Jinxian (JIX) of Jiangxi province, and 9 cultivars from Changsha (CHS) of Hunan province. Rice production in these sampling spots is characterized by rice straw field return or burning and traditional water management, namely alternative flooding and drying. There were 83 inbred and 125 hybrid rice among them. All the cultivars, with the exception of two cultivars being japonica subspecies, belonged to indica. While sampled, four rice plants were randomly gathered for each cultivar from the paddy field, and then the whole plants were packaged and delivered to the laboratory immediately.

Sample preparation and analysis

All the rice grains were manually threshed and sun-dried in the laboratory, and then husked by a huller (TP-JLG-2018, China). The brown rice was ground into fine powder by a high-speed grinder (Tester-FW80, China), passed through a 0.15 mm sieve and stored at − 4°C until further analysis.

The brown rice samples were digested by HNO₃/H₂O₂ as reported by Zavala et al. (2008) to detect the contents of Cd, As and mineral elements. Briefly, 0.25 g samples were weighed into a Teflon crucible, then 6 mL concentrated HNO₃ was added and left overnight. Prior to digestion at 200 ℃ for 1 h and 180 ℃ for 4 h, 2 mL 30% H₂O₂ was added to the crucible. The digested solution was filtered by a 0.45 µm pinhole filter. Then, total Cd, As, B, Mo, Cu and Fe in the solution were determined by inductively coupled plasma mass spectrometry (ICP-MS, Agilent 7700x, USA). Zn, Mn and Mg were detected by atomic absorption spectrophotometer (AAS, Hitachi ZA3000, Japan), and Ca and S were analyzed by inductively coupled plasma optical emission spectrometer (ICP-OES, Varian 710-ES, USA). A flame photometer (INESA FP6400A, China) was used to determine K, and P was analyzed by molybdenum antimony colorimetric method (Sjösten and Blomqvist, 1997). Total N was detected by Kjeldahl procedure (Lou et al., 2007). The method quality was validated by analyzing the certified reference materials (CRM) NIST 1568b (Table S1).

As species in brown rice were extracted by 1% HNO₃ using the method reported by Šlejkovec et al. (2021) and detected by high performance of liquid chromatograph coupled with ICP-MS (Agilent 1260/7700x, USA). This instrument was equipped with a Hamilton PRPX100 anion exchange column. 0.02 M NH₄HCO₃ and 0.05 M (NH₄)₂CO₃ were used as the mobile phases, with pH of 8.5 adjusted by NH₃ (aq) or diluted HNO₃. The analysis quality was guaranteed by CRM NIST 1568b as well. The mixed standard solution was composed of [As(Ⅴ)], [As(Ⅲ)], DMA and MMA with individual concentration of 20 µg·L^− 1. The extraction efficiencies of As species were 75.3–110.7%, and the recovery rates of iAs (sum of [As(Ⅴ)] and [As(Ⅲ)]), DMA and MMA were 94.5–104.3%, 95.2–105.5%, and 94.8–105.2%, respectively.

Risk assessment of Cd and iAs exposure in rice consumption

The non-carcinogenic risk assessment of Cd and iAs was referred to the method described by Ma et al. (2017). Prior to risk evaluation, the concentrations of Cd and iAs in brown rice were converted to those in polished rice due to the fact that most of rice is eaten as polished rice and rice bran accumulating higher levels of Cd and iAs is removed during rice milling. Specifically, to estimate the Cd and iAs concentration for polished rice, the contents in brown rice must be divided by 1.16 (Jo and Todorov, 2019) and 1.10 (Meharg et al., 2008), respectively.

The estimated daily intake (EDI) of Cd and iAs from rice was calculated by formula (1). In formula (1), EDI (mg·Wkg^− 1·day^− 1), M (mg·kg^− 1), DIP (kg·day^− 1) and W (kg) represent estimated daily intake of Cd or iAs, Cd or iAs level in rice, daily intake of rice and mean body weight of local residents, respectively. The daily rice intake and the average body weight refer to the medium levels of Guangdong province, namely 0.372 kg·day^− 1 and 60 kg, respectively (Ma et al., 2017).

$$EDI=M\times DIP∕W$$

The non-carcinogenic risk to residents who consume locally grown rice for a long time was estimated by the target hazard quotient (THQ), as shown in Formula (2). THQ is the target hazard quotient index of Cd or iAs. RfD is the oral reference dose for Cd (1.0×10^− 3 mg·kg^− 1·day^− 1) and iAs (1.5×10^− 3 mg·kg^− 1·day^− 1) as regulated by USEPA (U.S.EPA, 2013).

$$THQ=EDI/RfD$$

Malnutrition risk evaluation of rice consumption

The nutritional status of rice in the present study was assessed according to Chinese dietary reference intakes (Part 1 ~ 3) (NHC, 2018). Herein, the mineral nutrient contents in white rice were treated the same as those in brown rice because no conversion coefficients between them can be referenced.

The daily intakes (DIs) of mineral elements were computed through formula (3), where DIB and M stand for the daily consumption of white rice and the content of a specific element in rice, respectively. Formula (4) was used to calculate the percentage of a specific nutrient element intake to dietary reference intakes (%DRIs). DRIs refers to the dietary reference intakes. The protein concentration in rice was multiplied by 6.25 folds of N content (Salo-väänänen and Koivistoinen, 1996).

$$DIs=DIB\times M$$

$$\%DRIs=100\%\times DIs∕DRIs$$

Statistics analysis

Data statistical analysis was carried out using SPSS 24.0 software. The concentrations of Cd, As, As species and mineral elements in brown rice were analyzed by rank-based nonparametric Mann-Whitney U test (P < 0.05). GraphPad Prism 8.0.1 software was applied to produce figures.

Total Cd and As concentrations in rice

Cd contents in brown rice of 208 cultivars ranged from not detectable to 1.61 mg·kg^− 1, with the mean and median of 0.26 and 0.11 mg·kg^− 1, respectively (Table 1). The average Cd content in brown rice in the present survey was slightly higher than that in 41 milled rice samples (0.23 mg·kg^− 1) collected from markets in Guangdong province as reported by Ma et al. (2017). Rice Cd contents in 35.1% of the total 208 cultivars exceeded the Chinese rice Cd limit (0.2 mg·kg^− 1) (GB2762, 2017), indicating that the reduction of rice Cd level is an impending task in South China.

Table 1

Descriptive statistics of Cd and As levels in brown rice of 208 cultivars from typical rice planting areas of South China
Population	Item	Cd (mg·kg^− 1)	As (mg·kg^− 1)
Total(n = 208)	Range	ND − 1.61	0.08–0.67
	Average	0.26 ± 0.32	0.27 ± 0.10
	Median	0.11	0.25
Inbred Rice(n = 83)	Average	0.32 ± 0.39a	0.24 ± 0.09b
	Median	0.11	0.23
Hybrid Rice(n = 125)	Average	0.23 ± 0.26a	0.29 ± 0.10a
	Median	0.11	0.28
“ND” indicates not detectable. Different letters indicate significant differences between inbred and hybrid rice on Cd and As content (P < 0.05)

Total As (tAs) concentrations in brown rice were in the range of 0.08–0.67 mg·kg^− 1, and averaged 0.27 mg·kg^− 1, with a median of 0.25 mg·kg^− 1 (Table 1). It is documented that tAs of 160 polished rice samples from 20 provinces in China averages to 0.09 mg·kg^− 1 (Chen et al., 2018), and the mean tAs concentration of 41 polished rice from Guangdong province is 0.11 mg·kg^− 1 (Ma et al., 2017), both of which are considerably lower than those in the current work, irrespective of the discrepancy between brown rice and polished rice.

The variations of Cd and As content in rice may be ascribed to genotype, soil properties and the interaction between plant and soil (Duan et al., 2017; Ma et al., 2017; Wang et al., 2018). When Cd contents of both rice subspecies were compared, the mean Cd level (0.32 ± 0.39 mg·kg^− 1) of the inbred was obviously higher than that of the hybrid (0.23 ± 0.26 mg·kg^− 1), but no significant variation was found between them (Table 1), which is in line with the result reported by Sun et al. (2016). Unlike Cd, As in brown rice of inbred variety (0.24 ± 0.09 mg·kg^− 1) was significantly lower than that of hybrid type (0.29 ± 0.10mg·kg^− 1) (P < 0.05) (Table 1), indicating that the hybrid type had higher As accumulating capability than the inbred one.

Significant geographical differences were observed for both rice Cd and As in 208 rice cultivars (Fig. S1). Totally, the mean Cd value of brown rice for QUJ in Guangdong province was significantly higher than that from WEY, and the latter was followed by those from CHS, JIX and so on. Brown rice from XIX was characterized by the bottom level of Cd (0.06 mg·kg^− 1). It is noticeable that the mean rice Cd (0.75 mg·kg^− 1) from QUJ was more than 3-fold higher than the Cd limit for rice in China, and those from WEY (0.58 mg·kg^− 1) and CHS (0.32 mg·kg^− 1) exceeded the limit as well (Fig. S1A). Brown rice tAs concentrations from different regions significantly decreased in the order: XIX (0.33 mg·kg^− 1), HUY (0.32 mg·kg^− 1), WEY (0.31 mg·kg^− 1) > QUJ (0.26 mg·kg^− 1), LUF (0.25 mg·kg^− 1), GUZ (0.22 mg·kg^− 1) > JIX (0.17 mg·kg^− 1), GAZ (0.17 mg·kg^− 1) > CHS (0.12 mg·kg^− 1) (P < 0.05) (Fig. S1B).

As species in rice

As compounds including [As(Ⅲ)], [As(V)], DMA, and MMA were detected in brown rice. Since [As(Ⅲ)] and [As(V)] might convert each other during extraction, they were hereinafter collectively referred to iAs. iAs and DMA were determined in all rice cultivars, while MMA was analyzed in 61% of all the rice cultivars (Table 2). iAs contents in brown rice varied from 0.06 to 0.48 mg·kg^− 1, with the average and median of 0.21 and 0.20 mg·kg^− 1, respectively. 52.4% of the total samples exceeded iAs limit. DMA and MMA were detected in low levels in brown rice, and average 0.02 ± 0.02 and 0.004 ± 0.004 mg·kg^− 1, respectively. The sum of As species (sAs) was highly correlated to tAs (Y = 0.84X + 0.012, r² = 0.91^**), and close relation was found between iAs and sAs (Y = 0.90X − 0.002, r² = 0.95^**) as well. The average percentage of iAs relative to sAs was 89.7% (Table 2), implying that all the rice varieties collected in the present work belonged to iAs-dominant type, as classified by the method of Zavala et al. (2008).

Table 2

Descriptive statistics of As species in brown rice in typical planting areas of South China
Population	Item	iAs	DMA	MMA
Total (n = 208)	Detection rate (%)	100	100	61
	Range (mg·kg^− 1)	0.06–0.48	0.00–0.14	0.000–0.011
	Average (mg·kg^− 1)	0.21±0.08	0.02±0.02	0.004±0.04
	Median (mg·kg^− 1)	0.20	0.02	0.006
	Percent^*(%)	89.7	8.5	1.7
Inbred Rice (n = 83)	Average (mg·kg^− 1)	0.19 ± 0.06b	0.02 ± 0.02a	0.004 ± 0.004a
	Median (mg·kg^− 1)	0.18	0.02	0.00
Hybrid Rice (n = 125)	Average (mg·kg^− 1)	0.23 ± 0.08a	0.02 ± 0.02a	0.005 ± 0.004a
	Median (mg·kg^− 1)	0.23	0.02	0.01
“*” indicates the percent of a specific As species over the sum of As species. Different letters indicate significant differences between inbred and hybrid rice on As species content (P < 0.05)

Previous studies reported that iAs is the dominant species in polished rice in Hunan and Guangdong province of southern China as well (Ma et al., 2016; Ma et al., 2017). In a nationwide survey, iAs and DMA account for 35–92% and 8–65% in China (Chen et al., 2018), which is greatly different from the observation of this work. The discrepancy is likely ascribed to rice subspecies characteristics per se and soil properties. Indica rice is usually planted in South China, whereas japonica is the main variety in North China. On the other hand, rice cannot methylate As by itself, and DMA in the grain originates from methylated As in soil (Zhao et al., 2013). Soil organic matter promotes microbial As methylation in paddy soil (Huang et al., 2012). Generally, black soils in Northeastern China contained higher organic matter than those in southern China (Dai and Huang, 2006), which are beneficial to the formation of methylated As and the concomitant As uptake by rice.

Additionally, iAs content of the inbred (0.19 ± 0.06 mg·kg^− 1) was significantly lower than that of the hybrid (0.23 ± 0.08 mg·kg^− 1) (P < 0.05) (Table 2), whereas both DMA and MMA stayed at similar levels for both subspecies, indicating that the difference of iAs between both subspecies was contributed to the variation of tAs for them. However, the mechanisms for discrepancy of As absorbance between both subspecies are not revealed yet. Since iAs dominated in all 208 rice cultivars, the geographical variation of As species in brown rice was not further described herein.

Mineral nutrients in rice

The profile of twelve mineral nutrients in rice, all of which are essential nutrients for higher plants, is presented in Fig. 2. The minimum levels of mineral nutrients were 2- to 10-fold lower than those of the maximum values, suggesting a great discrepancy among rice cultivars. Huge discrepancy for microelements like Fe, Zn and Cu in rice was observed in a field survey involving in 653 rice varieties in Yunnan China as well (Zeng et al., 2004). Averagely, brown rice contained N 14.8 ± 1.7, P 5.25 ± 2.26, K 5.44 ± 0.87, Ca 0.16 ± 0.05, Mg 2.32 ± 0.48, and S 1.47 ± 0.17 g·kg^− 1, respectively. The contents of microelements including Fe, Mn, Cu, Zn, B and Mo were 17.7 ± 10.7, 43.9 ± 21.5, 4.2 ± 2.0, 25.0 ± 4.4, 2.59 ± 1.35 and 1.26 ± 1.10 mg·kg^− 1, respectively.

When both rice subspecies were compared, the inbred contained significantly lower K and B, but higher Fe and Zn than the hybrid (P < 0.05) (Fig. 2). Both subspecies contained similar levels of N, P, Ca, Mg, S, Mn, Cu, B and Mo.

Unlike Cd and As, although significant difference for the twelve mineral elements in brown rice were observed among regions (Fig. S2), there was no unusually high mineral nutrients in a specific region, with the exception of Mn, Cu and Mo in WEY. The concentrations of essential elements in higher plants are primarily affected by fertilization, irrigation, soil attribute, and plant species (Du et al., 2013), which helps to explain the geographical variation of mineral elements was lower than that of Cd and As in rice. The abnormal abundance of Mn, Cu and Mo in WEY needs to be investigated in the future.

Correlations between Cd, As and mineral elements

Significant positive correlation was computed between Cd versus Ca (r = 0.220^**), Mn (r = 0.496^**), Cu (r = 0.156^*), Zn (r = 0.221^**) and Mo (r = 0.332^**) in brown rice, while negative relations was observed between Cd versus P (r = − 0.224^**) and B (r = − 0.166^*) (Table 3). Some investigators have reported a positive correlation between Cd versus Cu (r = 0.430^**) and Zn (r = 0.333^**) in grains (Hang et al., 2009). It has been demonstrated that Cd and Mn are translocated within rice plant by OsNRAMP5 transporters, and Cd and Zn share the upward transporter OsHMA2, hence, competition between Cd versus Mn and Zn may exist in rice (Sasaki et al., 2012; Satoh-Nagasawa et al., 2012). However, high mobility of metal cations in paddy soils due to soil acidification leads to enrichment of these elements in rice in southern China (Wang et al., 2018), which might shade the competition between them. Total As in brown rice was significantly correlated to K (r = 0.323^**), Ca (r = 0.266^**), Zn (r = − 0.141^*), B (r = 0.336^**) and Mo (r = 0.241^**). The significant negative correlation between As and Zn was reported in previous study as well (Williams et al., 2009). The relation between Cd and As versus mineral elements shows that the accumulation of P, Zn and B inhibited the buildup of Cd or As by rice grain, which supports the observation that application of P, Zn and B can reduce the uptake of Cd or As by rice plants (Duan et al., 2013; Rizwan et al., 2016).

Table 3

Pearson correlation coefficient between Cd, As versus mineral element concentrations in brown rice in South China (n = 208)
	Cd	As	N	P	K	Ca	Mg	S	Fe	Mn	Cu	Zn	B	Mo
Cd	1.000	-0.093	0.113	-0.224^**	0.021	0.220^**	-0.032	0.094	0.063	0.496^**	0.156^*	0.221^**	-0.166^*	0.332^**
As		1.000	0.063	-0.072	0.323^**	0.266^**	0.120	0.120	-0.100	-0.002	0.080	-0.141^*	0.336^**	0.241^**
* and ** refer to significant difference at 0.05 and 0.01 levels, respectively

An opposite chemical behavior between Cd and As in soil is noticeable. In unflooded fields, As accumulation is limited, but Cd absorption increases considerably. However, an opposite trend occurs in flooded fields (Zhao and Wang, 2020). In the present study, no close relationship between Cd and As was found for all 208 cultivars. Intriguingly, significant negative correlation between Cd and As was observed solely in WEY (n = 30) with soil heavy metal pollution linked to mining (Luo et al., 2020) (r = − 0.367^*)(Table S2), suggesting that the antagonism between Cd and As in plant maybe not easily observed in unpolluted soils. Additionally, N, P, Cu and Zn were negatively correlated to As (N-As: r = − 0.646^**; P-As: r = − 0.540^**; Cu-As: r = − 0.548^**; Zn-As: r = − 0.650^**) in WEY respectively, implying that As contamination in rice depressed mineral nutritional merits of rice.

Potential human health risk caused by rice Cd and iAs intake

THQ-Cd and THQ-iAs indexes are used to evaluate the potential health risks of Cd and iAs in rice. When THQ is lower than 1, it shows no potential non-carcinogenic risk. THQ-Cd differed from 0.02 to 8.58 for all the cultivars, with the mean of 1.40 ± 1.69 (Table 4). Among 208 varieties, 36% of them had THQ-Cd higher than 1, namely, daily rice consumption of these varieties might pose non-carcinogenic health risk to human. In terms of iAs, THQ-iAs varied within 0.24–1.81 and averaged 0.80 ± 0.28, with an exceeding threshold rate (ETR) of 26%. Ma et al. (2017) documented that the polished rice in Guangdong province was low in non-carcinogenic risk for iAs (THQ-iAs 0.38), but high in non-carcinogenic risk for Cd (THQ-Cd 1.43), which is consistent with the trend of this investigation. High levels of Cd intake by eating rice are common, which seriously threatens human health (Fang et al., 2014; Suwatvitayakorn et al., 2020). A national survey shows that the THQ-Cd of rice in five typical rice plantation areas (Hubei, Liaoning, Yunnan, Guangdong, Guizhou) in China exceeded the safe threshold of 1, and children had higher health risks than adults (Ke et al., 2015). In the present study, the THQ and ETR of both Cd and iAs indicate that more attention should be paid to the potential health risk caused by Cd intake than by iAs ingestion through rice eating in South China.

Table 4

Target Hazard Quotient (*THQ*) index and the exceeding threshold rate (*ETR*) for Cd and iAs concentrations in rice
Population	Item	Cd	iAs
Total (n = 208)	THQ	1.40 ± 1.69	0.80 ± 0.28
Total (n = 208)	ETR (%)	36.1	25.5
Inbred Rice (n = 83)	THQ	1.68 ± 2.06a	0.70 ± 0.24b
Inbred Rice (n = 83)	ETR (%)	37.3	16.9
Hybrid Rice (n = 125)	THQ	1.23 ± 1.38a	0.86 ± 0.29a
Hybrid Rice (n = 125)	ETR (%)	35.2	31.2
THQ represents the non-carcinogenic risk of Cd and As via rice consumption. ETR is the percent of the varieties with THQ ≥ 1 over all the varieties. Different letters indicate significant differences between inbred and hybrid rice on the THQ of Cd and As (P < 0.05)

Although the mean THQ-Cd of the inbred was considerably higher than that of the hybrid, the difference between them was insignificant (Table 4). And, the ETR of both rice subspecies (37% and 35%) stayed similar. Significant variation for THQ-iAs was found between both subspecies (P < 0.05). Although the average THQ-iAs of both subspecies was low than 1, there were 17% of the inbred and 31% of the hybrid generating THQ-iAs higher than 1. Therefore, cultivar selection seems to be an effective way to lessen the risk of Cd and As intake by eating rice due to differences in Cd and As accumulation (Liu et al., 2014; Saengwilai and Meeinkuirt, 2021).

Additionally, obvious regional variation was found for THQ-Cd (Fig. S3). The unusually high THQ-Cd and ETR in QUJ (3.99 ± 1.58, 100%) and WEY (3.08 ± 1.61, 97%) suggest that serious health risk might be caused by rice eating for local residents. Cultivars planted in WEY were characterized by the maximum THQ-iAs (1.05 ± 0.22) and high ETR (60%) (Fig. S3), suggesting that health risk associated with iAs intake by rice consumption needs be concerned. The THQ-iAs of rice cultivars from XIX, HUY and LUF was lower than 1, but 43%, 38% and 13% of the varieties in these three cities were subjected to high ETR, indicating high species-dependent capability to accumulate iAs in rice. THQ-iAs for cultivars in GUZ, JIX, GAZ and CHS was much lower than 1 and no cultivar exceeded the threshold of THQ-iAs.

Malnutrition risk of rice consumption

Exemplifying with Chinese adult male, DIs of protein and major mineral nutrients including P, K, Ca, Mg, Fe, Zn, Cu and Mo in brown rice was evaluated, and the risk of malnutrition caused by rice consumption was assessed, based on DRIs of dietary nutrients for Chinese residents (NHC, 2018). As shown in Table 5, the average DIs of protein, Ca, Fe, and Zn was 34.4 ± 4.0 g·day^− 1, 61.1 ± 16.7, 6.6 ± 4.0 and 9.3 ± 1.6 mg·day^− 1, and the %DRIs was 53%, 8%, 55% and 74%, respectively. The above implies that sufficient intake of P, K, Mg, Cu, and Mo was guaranteed, however, the deficiency of protein, Ca, Fe, and Zn would occur by sole rice consumption. Nguyen et al. (2020b) reported that the average element intake for some nutrients including P, Mg, Cu, Mo from rice is higher as compared to the dietary reference intakes, whereas the supply of Ca and Fe by eating rice is far below people’s daily requirement in the main rice-producing areas in Vietnam, while Zn is abundant. Consequently, supplementation of these nutrients, such as protein, Ca, Fe and Zn, from other foods in daily diet needs to be emphasized to prevent potential malnutrition in South China.

Table 5

Mean daily intakes (*DIs*) of nutrients by eating rice from South China and the percent of *DIs* over dietary reference intakes (*DRIs*) for Chinese adult males
Population	Item	Protein (g·day^− 1)	P (mg·day^− 1)	K (mg·day^− 1)	Ca (mg·day^− 1)	Mg (mg·day^− 1)	Fe (mg·day^− 1)	Zn (mg·day^− 1)	Cu (mg·day^− 1)	Mo (mg·day^− 1)
Total (n = 208)	DIs	34.4 ± 4.0	1941 ± 843	2023 ± 323	61.1 ± 16.7	864 ± 178	6.6 ± 4.0	9.3 ± 1.6	1.6 ± 0.7	0.47 ± 0.41
Total (n = 208)	%DRIs (%)	53	270	101	8	262	55	74	200	470
Inbred Rice (n = 83)	DIs	34.4 ± 4.6a	2059 ± 1023a	1937 ± 373b	61 ± 19a	855 ± 184a	7.8 ± 4.5a	10.0 ± 1.3a	1.5 ± 0.8a	0.45 ± 0.46a
Inbred Rice (n = 83)	%DRIs (%)	53	286	97	7.6	259	65	80	188	450
Hybrid Rice (n = 125)	DIs	34.4 ± 3.5a	1884 ± 686a	2081 ± 273a	61 ± 15a	871 ± 174a	5.7 ± 3.3b	8.9 ± 1.7b	1.6 ± 0.7a	0.48 ± 0.37a
Hybrid Rice (n = 125)	%DRIs (%)	53	262	104	7.6	264	48	71	200	480
%DRIs represents the percent of DIs over DRIs, and is used to evaluate the risk of malnutrition caused by rice consumption. When %DRIs is low than 100%, it means that sole rice consumption poses a risk of malnutrition. The DRIs value of Chinese adult males (aged 18–50) is exemplified to calculate the DRIs percentage of mineral elements. DIs is expressed as mean ± standard deviation (SD). Different letters indicate significant differences between inbred and hybrid rice on the DIs of mineral nutrients (P < 0.05)

When both rice subspecies were compared, the possibility of insufficient Fe and Zn intake via consumption of the hybrid rice was significantly higher than that of the inbred rice (P < 0.05) (Table 5). As compared with the geographical variation of health risk via rice Cd and iAs intake, the regional discrepancy of malnutrition risk of mineral nutrients through rice eating was considerably lower (data not shown).

The survey on 208 rice cultivars from typical rice production regions in South China shows that iAs was the dominant As species (89.7%) in rice. Among these cultivars, 35.1% and 52.4% of them contained excessive Cd and iAs in reference to the Chinese Cd and iAs limits for rice. There was significant difference of subspecies and region for the accumulation of Cd, As and the uptake of mineral nutrient elements in rice. Inbred rice was significantly lower in As accumulation and higher in Fe and Zn buildup compared to hybrid rice. Significant and negative correlation between Cd and As versus a few of mineral elements suggests that contamination of Cd and As might reduce the mineral nutritional merits of rice. Health risk evaluation as measure by THQ indicates that Cd intake is higher than iAs intake via rice eating. Malnutrition susceptibility as measured by Chinese dietary reference intake, suggests that deficiencies of Ca, protein, Fe, and Zn associated with rice consumption needs to be concerned. Conclusively, the present study highlights the significance of reducing Cd and As buildup in rice plantation and supplementation of Ca, protein (N), Fe and Zn in human daily diet in southern China.

Author contributions

Qinghui Liu: Investigation, chemical analysis and writing of original draft

Weisheng Lu: Investigation assistance and resources

Cuihua Bai: Analysis method exploration and supervision

Congzhuo Xu, Maozhi Ye: Investigation assistance and chemical analysis

Yongcong Zhu: Chemical analysis

Lixian Yao: Funding acquisition, methodology, writing, review and editing.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgments

This research was supported primarily by Science and Technology Plan Project from Guangdong province (NO.2021B1212040008). Dr. Liu Kailou from National Rapeseed Industry Technical System of Jiangxi Province, and Professor Zhang Shihui from Hunan Academy of Agricultural Sciences were appreciated for their help in sample collection. We also thank Dr. Zhao Li from South China Agricultural University for his valuable suggestions in figure drawing.

Data availability statement

The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

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Cadmium, Arsenic and Mineral Nutrients in Rice, and Potential Risks for Human Health in South China

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