Full Terms & Conditions of access and use can be found at http://www.tandfonline.com/action/journalInformation?journalCode=tfab20 Download by: [China National Rice Research Institute] Date: 27 February 2017, At: 16:51 Food Additives & Contaminants: Part B Surveillance ISSN: 1939-3210 (Print) 1939-3229 (Online) Journal homepage: http://www.tandfonline.com/loi/tfab20 Nickel in milled rice (Oryza sativa L.) from the three main rice-producing regions in China Zhenzhen Cao, Renxiang Mou, Zhaoyun Cao, Xiaoyan Lin, Ping Xu, Zhijun Chen, Zhiwei Zhu & Mingxue Chen To cite this article: Zhenzhen Cao, Renxiang Mou, Zhaoyun Cao, Xiaoyan Lin, Ping Xu, Zhijun Chen, Zhiwei Zhu & Mingxue Chen (2017) Nickel in milled rice (Oryza sativa L.) from the three main rice-producing regions in China, Food Additives & Contaminants: Part B, 10:1, 69-77, DOI: 10.1080/19393210.2016.1250822 To link to this article: http://dx.doi.org/10.1080/19393210.2016.1250822 Accepted author version posted online: 26 Oct 2016. Published online: 04 Nov 2016. Submit your article to this journal Article views: 47 View related articles View Crossmark data
Transcript
Full Terms & Conditions of access and use can be found athttp://www.tandfonline.com/action/journalInformation?journalCode=tfab20
Download by: [China National Rice Research Institute] Date: 27 February 2017, At: 16:51
To cite this article: Zhenzhen Cao, Renxiang Mou, Zhaoyun Cao, Xiaoyan Lin, Ping Xu, ZhijunChen, Zhiwei Zhu & Mingxue Chen (2017) Nickel in milled rice (Oryza sativa L.) from the threemain rice-producing regions in China, Food Additives & Contaminants: Part B, 10:1, 69-77, DOI:10.1080/19393210.2016.1250822
To link to this article: http://dx.doi.org/10.1080/19393210.2016.1250822
Accepted author version posted online: 26Oct 2016.Published online: 04 Nov 2016.
Nickel in milled rice (Oryza sativa L.) from the three main rice-producing regionsin ChinaZhenzhen Caoa, Renxiang Moua, Zhaoyun Caoa, Xiaoyan Lina, Ping Xua, Zhijun Chenb, Zhiwei Zhua
and Mingxue Chena
aRice Product Quality Supervision and Inspection Center, China National Rice Research Institute, Hangzhou, China; bInstitute of QualityStandards and Testing Technology for Agro-Products, Chinese Academy of Agricultural Sciences, Beijing, China
ABSTRACTNickel (Ni) concentrations in milled rice obtained from China and their variations among differentprovinces and varieties, as well as associated health risks, were investigated. Results showed thatthe mean Ni concentration in milled rice was 0.49 ± 0.51 mg/kg, which was much higher thanreported in United Kingdom, French and Iranian cereals. There were significant variations(P < 0.05) of Ni concentrations in milled rice among different provinces and among varieties inthe same province. According to the dietary risk assessment, the mean values of the targethazard quotient for chronic risk ranged from 1.24 to 1.46 for 2–4, 4–7 and 7–11-year-old children,and all values of margin of exposure for hypersensitivity risk were considerably below 10 for allage groups, indicating that the current dietary exposure to Ni in rice is of concern for 2–11-year-old children and Ni-sensitised individuals. It is essential to establish a continuous monitoringprogramme to control Ni contamination in rice.
ARTICLE HISTORYReceived 29 June 2016Accepted 16 October 2016
Nickel (Ni) is a heavy metal and an essential microelementfor humans, which is a cofactor or structural componentof certain metalloenzymes and is involved in facilitatingferric iron absorption or metabolism in humans (Nielsen1984; Cempel & Nikel 2006; Wittsiepe et al. 2009).However, there are some adverse health effects whenhumans suffer from acute or long-term exposure(Barceloux 1999; Cempel & Nikel 2006; Foxall 2009). Ni isthe most common cause of sensitisation in the generalpopulation (Basketter et al. 1993; WHO 2005). Oral intakeof Ni can induce allergic contact dermatitis in Ni-sensitiveindividuals (D’Ambrosio et al. 1998; Nielsen et al. 1999;Jensen et al. 2006; Kazi et al. 2010). Besides, Ni and Nicompounds have been classified by the InternationalAgency for Research on Cancer as carcinogenic tohumans (group 1) causing cancers of the lung, nasal cavityand paranasal sinuses after inhalation (IARC 2012).
Food is the dominant source of Ni exposure for thenon-occupationally exposed population (Marzec 2004;Jensen et al. 2006). Cereal and cereal-based products, asthe most important food crop, are the major contribu-tors to the total dietary intake of Ni from food con-sumption for some Asian people. It was reported that43.3% of the daily intake of Ni for Lebanese adult wasfrom breads and cereals (Nasreddine et al. 2010). Wang
et al. (2014) also reported that cereal consumptioncontributed the most to the oral intake of Ni, account-ing for 43.5% of the daily Ni intake. China is one of thelargest consumers of rice in the world with an annualconsumption of about 190 million tons (China NationalGrain & Oils Information Center). The Northeast Plain,the Yangtze River basin and the Southeast Coastalregion are three main rice-producing regions, account-ing for 98% of the total national rice production inChina. However, Ni levels in the agricultural soils forsome localities of these regions have increased withthe growth of industrialisation and urbanisation in thepast two decades (Wei & Yang 2010; Li et al. 2014).According to a survey conducted in heavy metal con-taminations in agricultural soils from China, the meanconcentrations of Ni in agricultural soils of all 12 citieswere higher than their background values (Wei & Yang2010). The mean soil Ni concentrations in some miningareas were 2.1 times greater than the Grade II ofEnvironmental Quality Standard for soils (GB15618-1995) in China (Li et al. 2014). The uptake of Ni by riceplants is often highly correlated with the Ni concentra-tion in agricultural soils (Iyaka 2011; Sreekanth et al.2013). Thus, there is raising concern about Ni contam-ination in rice from these regions and the potentialhealth risk of Ni exposure from rice consumption.
In the past decades, several evaluations of the risksto human health related to the presence of Ni in foodhave been performed. THQ (target hazard quotient)values have been identified as the major parameterfor assessing non-carcinogenic risk from toxic elementalintake by consumption of contaminated food (U.S. EPA2000). THQ is the ratio of the estimated exposure to onecontaminant related to the reference dose without anyappreciable risk such as tolerance dietary intake (TDI). Ifthe THQ is below 1, the contamination is assumed to besafe. If the THQ exceeds 1, there is a chance of potentialhealth risk. The EFSA Panel on Contaminants in theFood Chain (CONTAM Panel) recommends a TDI of2.8 µg Ni/kg body weight (bw) as a reference dose forchronic effect in the general population, derived from alower 95% confidence limit for a benchmark dose at10% extra risk (BMDL10) of 0.28 mg/kg bw for post-implantation fetal loss in rats (EFSA CONTAM Panel2015). On the other hand, a margin of exposure (MOE)approach was recommended for estimating the hyper-sensitivity effect for Ni-sensitive humans after oral expo-sure to Ni, which is determined by the ratio of a lowestBMDL10 of 1.1 µg/kg bw to the Ni dietary exposure(EFSA CONTAM Panel 2015). An MOE of 10 or higherwould be indicative of a low health concern. Severalstudies have evaluated the chronic dietary exposure toNi in European populations in the past (Leblance et al.
2005; Turconi et al. 2009; Wittsiepe et al. 2009;Nasreddine et al. 2010; Rose et al. 2010; Arnich et al.2012; Domingo et al. 2012; Koch et al. 2016). The meanchronic dietary exposure to Ni, ranging from 1.49 to6.02 µg/kg bw per day, was close to the TDI or above it,especially for the young age classes, while the highdietary exposure (95th or 97.5th percentile) rangingfrom 3.01 to 12.7 µg/kg bw per day was above theTDI for all different age groups. With respect to thehypersensitivity effect, all the MOEs calculated fromthese exposure levels were considerably below 10 forall age groups both for the estimated mean and highdietary exposure levels. Therefore, it was concludedthat the current dietary exposure to Ni are of concernfor the general population. However, so far, there islittle information for nationwide dietary intake of Ni inthe Chinese population due to rice consumption. In thepresent study, the Ni concentrations in 1332 milled ricesamples obtained from the 11 provinces of the threemain rice-producing regions in China, as well as thevariations in Ni concentrations among the differentlocations and varieties were investigated. A probabilis-tic estimation of dietary exposure to Ni for different ageand gender groups was performed and the associatedhealth risk was assessed by the THQ and MOE methods.This study aimed to provide national-scale informationon the contamination levels and health risks of Ni in
Figure 1. The geographical locations of sampling provinces and sampling sites in China.
70 Z. CAO ET AL.
milled rice. The results can help to establish a contin-uous monitoring programme to control Ni contamina-tion in rice in China.
Materials and methods
Reagents and chemicals
Nitric acid (HNO3, 65%) and hydrogen peroxide (H2O2,30%) were obtained from Merck (Darmstadt, Germany).The Ni standard solution (1000 μg/ml) was obtainedfrom Sigma-Aldrich Co (St. Louis, MO, USA). Deionisedwater (18.2 MΩ) was produced by a Milli-Q water pur-ification system (Millipore Co., Bedford, MA, USA) andused throughout all analyses. The certified referencematerial (CRM) GBW 10010 rice flour, obtained fromthe Chinese Academy of Geographical Sciences(Beijing, China), was used for quality assurance.
Sample collection and preparation
1332 rice samples were collected from 94 sites in thethree main rice-production regions of China, covering 11provinces. Detailed information on the sample provinceand sample size was as follows: Liaoning (120 from 10counties), Jilin (36 from 7 counties), Heilongjiang (150from 5 counties), Hunan (309 from 12 counties), Sichuan(120 from 10 counties), Jiangxi (117 from 13 counties),Anhui (45 from 5 counties), Jiangsu (45 from 5 counties),Hubei (45 from 7 counties), Zhejiang (142 from 11 coun-ties) and Guangxi (203 from 9 counties). The geographicallocations of sampling provinces and sampling sites inChina were shown in Figure 1. Rice samples were col-lected from five random and well-distributed points ofone paddy field (>100 m2) during the harvest seasons.All five samples per field were combined to obtain onehomogenised sample per field. Then, 1 kg homogenisedrice sample was randomly chosen and transported to thelaboratory and oven-dried at 65°C for 3 days to constantweight. After removal of the outer hull and bran layers,the milled rice was ground into powder passing a 100-mesh sieve using a cyclone sample mill (UDY Corp., FortCollins, CO, USA) and then stored at 4°C for furtheranalysis.
Analytical procedure
Approximately 0.25 g of ground rice samples (accurate to1 mg) was weighed into polypropylene digestion tubes,steeped in 8 mL of concentrated HNO3 and predigestedfor 2 h at room temperature. Next, 3 mL of 30% H2O2 wasadded and heated to 120°C using a Digi-Block ED54
digestion system (LabTech, Inc., Hopkinton, MA, USA)until approximately 0.5 cm height of solutions. Finally,the cooling digest was diluted to 50 ml with deionisedwater (18.2 MΩ) for Ni determination. A Ni standardsolution and reagent blank followed the same procedure.For each sample, three replicate analyses were performedunder the same conditions. Measurement uncertaintywas calculated as the relative standard deviation (RSD).
An optimised analytical method of inductivelycoupled plasma-mass spectrometry (ICP-MS; X Series2, Thermo Fisher Corp., Waltham, MA, USA) in mixedmode was established to determine Ni concentrationsin rice. Main ICP-MS operating parameters were inci-dent RF power 1300 W, nebuliser Ar gas flow rate0.86 L/min, cooling Ar gas flow rate 13 L/min andauxiliary Ar gas flow rate 0.7 L/min. The ICP-MS wasused in a collision-reaction cell with kinetic energy dis-crimination (CCT-KED) mode using H2/He (v/v = 7:93) asthe collision cell gas (4 mL/min) and 50 μg/L In wasused as internal standard. The ion count was monitoredat m/z 60. The peristaltic pump rate was 30 rpm.
Method validation
The established method was validated by evaluation oflinearity, sensitivity, accuracy and precision. Linearity ofthe calibration curve was evaluated with the concentra-tions 0, 2, 10, 20 and 50 ng/mL. Sensitivity was determinedby evaluation of the limit of detection (LOD) and the limitof quantitation (LOQ). The LOD was defined as 3 times thestandard deviation of the blank (n = 10), while the LOQwas calculated as 3.3 times the LOD. Accuracy and intra-and inter-day precision (RSD) of the method were deter-mined by recovery experiments at low, medium and highconcentrations (n = 7) on 7 consecutive days.
Quality assurance
The CRM GBW 10010 rice flour (Chinese Academy ofGeographical Sciences, Beijing, China) was used to ver-ify the measurement of Ni in rice by applying one CRMmeasurement every 20 samples.
Dietary exposure assessment
The estimated daily intake (EDI) was calculated usingthe measured Ni concentrations in milled rice, com-bined with average daily rice consumption and averagebw for Chinese residents, by the equation
EDI ¼ C � EF � ED � FIRð ÞWAB � TA
FOOD ADDITIVES & CONTAMINANTS: PART B 71
where C is the Ni concentration in milled rice (mg/kg),EF is the exposure frequency (365 days/year), ED is theexposure duration (70 years), FIR is the rice ingestionrate (g/person/day), WAB is the average bw and TA is theaverage exposure time (EF × ED). FIR and WAB (shown inTable 1) were obtained from the National Nutrition andHealth Survey of Chinese residents (2002).
In order to obtain different distributions of Ni expo-sure, the probabilistic Monte Carlo method and boot-strap values were applied using the commerciallyavailable software package@Risk (PalisadeCorporation, Version 4.5, Ithaca, NY, USA). The simula-tion procedures were divided into U-step (for uncer-tainty) and V-step (for variability). First, at U-step,bootstrap samples with the same sample size weredrawn from an empirical distribution of 1332 ricesamples. Second, at V-step, Monte Carlo samplingwas operated n times from the bootstrap samplesabove. The mean values and percentiles (P50, P90,P97.5 and P99.9) of individual samples were obtainedafter repeating the U- and V-steps B times, at a 95%confidence interval (P2.5–P97.5) for each percentile,and n and B in the simulation procedures were set to100,000 and 2000, respectively, which resulted in100,000 × 2000 = 2 × 108 simulations to guaranteethe reliability of the results. For Ni concentrationsbelow LOD, data were handled as LOD/2, accordingto a previous report (Chen et al. 2009).
Dietary risk assessment
The chronic health risk of Ni consumption through ricewas assessed according to the THQ method (U.S. EPA2000), by the equation THQ = EDI/TDI, where TDI (toler-able daily intake) is 2.8 µg/kg bw/day, derived from alower 95% confidence limit for a benchmark dose at10% extra risk (BMDL10) of 0.28 mg Ni/kg bw as calcu-lated from the dose response analysis of the incidenceof litters with post-implantation loss in rats, applying
the default uncertainty factor of 100 to account forinterspecies differences and human variability (EFSACONTAM Panel 2015). A THQ below 1 is assumed tobe safe. If the THQ exceeds 1, there is a chance ofpotential health risk.
The hypersensitivity risk for Ni-sensitive humansthrough rice consumption was assessed by the MOEapproach (EFSA CONTAM Panel 2015) as followsMOE = BMDL10/EDI. Allergic contact dermatitis is themost prevalent effect of Ni in the general population,estimated prevalence in the general population to beup to 15%. A TDI of 2.8 µg/kg bw/day or above may notbe sufficiently protective of individuals sensitive to Ni.Thus, a lowest BMDL10 of 1.1 µg/kg bw/day derived forthe incidence of systemic contact dermatitis elicited inNi-sensitive humans after oral exposure was selected asthe reference point for hypersensitivity effect (EFSACONTAM Panel 2015). If the estimated value of MOEexceeds 10, it is believed to be safe for hypersensitivityeffect.
Statistics
Statistical analyses were done using the statistical soft-ware SPSS vs. 19.0 (SPSS Inc., Chicago, IL, USA). Thestatistical significance for Ni levels among differentareas and varieties were assessed using Duncan’s multi-ple comparison. All data were expressed as mean ± SD.A value of P < 0.05 was considered statisticallysignificant.
Results and discussion
Quality assurance
Good linearity was established in the concentrationrange 0–50 ng/mL, with a corresponding correlationcoefficient (r) higher than 0.9999. The recoveries atlow (15 ng/mL), middle (100 ng/mL) and high(1000 ng/mL) level were 85.2%, 90.3% and 98.6%,respectively, with the intra- and inter-day precision ran-ging from 1.7 to 5.2% and 5.6 to 8.5%, respectively,confirming that the applied ICP-MS method was suffi-ciently accurate and precise. LOD and LOQ were 4.5 and15 μg/kg, respectively, which met the quantificationrequirements. For the CRM, there was good agreementbetween certified (270 ± 20 μg/kg) and measured value(250.9 ± 4.3 μg/kg).
Frequency distribution
Table 2 shows the frequency distribution of Ni concen-trations in the investigated milled rice samples. The
Table 1. Average bw and rice daily intake for the Chinesepopulation.
levels ranged from 0.06 to 1.31 mg/kg, with an averageof 0.49 ± 0.51 mg/kg. Yang and Deng (2005) reportedmean Ni concentrations in rice from Sichuan (n = 97) of0.53 Fu et al. (2008) found an average concentration of0.76 mg/kg in rice from Taizhou (n = 13). Wang et al.(2014) revealed average contents in rice from Jiangxi(n = 50) and Jiangsu (n = 50) of 0.50 and 0.31 mg/kg,respectively. These data show that Ni values in rice inChina in this survey are within the range as reported inother literature. However, most of these studies havefocused on limited geographical areas and some werebased on far less samples. The present study provided amore nationwide data on Ni contamination in milledrice.
Ni content of cereals in other countries was reportedto range from 0.004 to 1.89 mg/kg, but with largevariations. Higher levels of Ni in cereals (up to1.47 mg/kg) were found in Nigeria (Onianwa et al.2000), whereas relatively lower levels (up to 0.16 mg/kg) were found in miscellaneous cereals in the UnitedKingdom (Rose et al. 2010), rice and semolina (up to0.02 mg/kg) in France (Leblanc et al. 2005) and rice (upto 0.004 mg/kg) in Iran (Pirsaheb et al. 2016). Therelatively higher Ni levels in milled rice samples inChina are possibly attributed to Ni enrichment in soil
and air as a result of the heavy use of fertilisers, waste-water irrigation and fossil fuels combustion.
Regional and variety differences
The regional distribution of Ni concentrations in ricesamples is shown in Table 3. These varied significantly(P < 0.01) among the three main rice-producingregions. The mean Ni concentration in the YangtzeRiver basin (0.54 ± 0.56 mg/kg) was significantly higher(P < 0.01) than those in the Northeast Plain(0.46 ± 0.54 mg/kg) and the Southeast Coastal region(0.35 ± 0.33 mg/kg). The reason for this phenomenonmay be due to heavy metal-rich wastewater irrigationon paddy land in the Yangtze River basin (Khan et al.2008), resulting in crop contamination.
Besides, there was a significant variation (P < 0.01) inthe Ni concentrations from the different sampling pro-vinces within the same rice-producing region (Table 3).For the Yangtze River basin, Hunan has the highestmean Ni concentration (0.70 ± 0.74 mg/kg) in milledrice samples, which was significantly (P < 0.01) higherthan those in Jiangxi (0.56 ± 0.31 mg/kg), Anhui(0.53 ± 0.30 mg/kg), Jiangsu (0.36 ± 0.24 mg/kg) and
Table 2. Frequency distribution of Ni concentrations in 1332milled rice samples from China’s three main rice-producingregions.Ni content (mg/kg) N Frequency (%)
Ni ≤ 0.1 111 8.30.1 < Ni ≤ 0.2 229 17.20.2 < Ni ≤ 0.3 236 17.70.3 < Ni ≤ 0.4 201 15.10.4 < Ni ≤ 0.5 126 9.50.5 < Ni ≤ 0.6 113 8.50.6 < Ni ≤ 0.7 72 5.40.7 < Ni ≤ 0.8 62 4.70.8 < Ni ≤ 0.9 39 2.90.9 < Ni ≤ 1.0 32 2.4Ni > 1.0 111 8.3
Table 3. Regional distributions of Ni concentrations (mg/kg) in milled rice samples from 11 provincesin China.Rice production area Province N Mean ± SD Maximum Minimum
Table 4. Ni concentration (mg/kg) variations in milled grains ofthe main rice varieties grown at the Hunan and Liaoningprovinces.Province Varieties N Mean ± SD
Sichuan (0.27 ± 0.20 mg/kg). Hunan province is rich inmineral deposition and well known as “the hometownof nonferrous metals”, where mining activities havecaused serious contamination of the agricultural envir-onment. High concentration of heavy metals in agricul-tural land has an adverse long-term effect on cropsafety, because they can be easily transferred by rootuptake and accumulation within the rice plant.Extensive reports demonstrated that paddy soils andrice from Hunan were severely contaminated withheavy metals. Liu et al. (2005) reported that the soilPb, Cd and Zn concentrations of Hunan mining areaswere 321.1–1088, 2.70–7.57 and 416.6–1000 mg/kg,respectively, which were by far exceeding the maxi-mum permissible concentrations for paddy soil qualityin China. Similarly, Lei et al. (2015) showed that Pb andCd levels in milled rice around mine areas were in therange 0.18–0.72 mg/kg and 0.10–1.32 mg/kg, respec-tively, which were much higher than the maximumlimits for rice as recommended by the Ministry ofHealth of China. However, so far, little attention waspaid on Ni contamination in Hunan province. In thepresent study, relatively high Ni concentrations in ricesamples from Hunan province indicated a possible Nicontamination in the paddy land of Hunan Province.With respect to the Northeast Plain, the mean Ni level inLiaoning (0.79 ± 0.72 mg/kg) was significantly higher(P < 0.01) than those in Jilin (0.45 ± 0.22 mg/kg) andHeilongjiang (0.21 ± 0.10 mg/kg). Liaoning, a traditionalindustrial and economic centre in northeastern China, isone of the highest Ni emitting provinces due to its largeamount of coal consumption and high Ni content ofraw coals (Tian et al. 2012). The airborne particles con-taining Ni eventually will be deposited on the surface ofsoils and subsequently be transferred into rice, leadingto relatively higher Ni concentrations in rice samples ofLiaoning province. Thus, monitoring efforts should beenhanced to assure food safety in the above-mentionedareas.
Rice variety showed large differences in existing Niconcentrations among the main rice varieties grown atthe same location (Table 4). Ni concentrations in eightmain rice varieties grown in Hunan ranged from0.18 ± 0.07 mg/kg in Wuyou308 to 1.45 ± 1.28 mg/kgin Xiangzaoxian6 and differences in mean Ni concentra-tions among the eight rice varieties were statisticallysignificant (P < 0.01). The Ni concentrations in Liaoningranged from 0.40 ± 0.25 mg/kg in Gangyu6 to1.01 ± 0.24 mg/kg in Xingyan1, while the differencesin Ni levels among the four varieties were also signifi-cant (P < 0.05). The coefficients of variation in differentvarieties were 49.3% for Hunan province and 37.7% forLiaoning province, respectively, suggesting that there
was genotypic variation in rice Ni concentrations withinthe same background value, which was in good agree-ment with previous studies (Zhang et al. 2006; Li et al.2012; Wu et al. 2015). Therefore, to select a rice geno-type with high tolerance to Ni toxicity is a reasonableapproach to minimise Ni contamination in rice.
Dietary exposure assessment
THQ and MOE have been identified as the major para-meters for assessing health risk from toxic elementintake by consumption of contaminated food (U.S.EPA 2000; EFSA 2009). For THQ, the EFSA CONTAMPanel recommends a TDI of 2.8 µg Ni/kg bw as areference dose for chronic effect for the population,derived from a lower 95% confidence limit for a bench-mark dose at 10% extra risk (BMDL10) of 0.28 mg/kg bwfor post-implantation fetal loss in rats (EFSA CONTAMPanel 2015). This guidance value is lower than thatderived by other institutional bodies (WHO 2005,2008) using the same studies (NOAEL of either 12 or22 µg/kg bw per day) due to the fact that a dose–response analysis of the complete data sets of thesestudies using the BMD approach was applied. As con-cluded by EFSA (2009), the BMD approach is a scienti-fically more advanced method to the NOAEL approachfor deriving a reference point, since it makes extendeduse of available dose–response data and provides aquantification of the uncertainties in the dose–responsedata. On the other hand, it has been reported thatindividuals can be sensitive to Ni through dermal con-tact and who have allergic contact dermatitis. Estimatedprevalence in the general population up to 15% maydevelop eczematous flare-up reactions in the skin (sys-temic contact dermatitis) from oral exposure to Ni salts.The TDI of 2.8 µg/kg bw/day may therefore not besufficiently protective of individuals sensitive to Ni.Thus, a lowest BMDL10 of 1.1 µg/kg bw/day derivedfor the incidence of systemic contact dermatitis elicitedin Ni-sensitive humans after oral exposure to Ni wasselected as the reference point for hypersensitivity anda MOE approach was adopted for risk characterisationby the EFSA CONTAM Panel (2015).
Percentiles of estimated intakes for different age andgender group’s exposure to Ni in China, as well as 95%confidence intervals for each percentile, are shown inTable 5. P50 values exhibit the median exposure ofconsumers to the distribution, whereas P97.5 data exhi-bit heavy exposure. For chronic risk assessment, theestimated mean and median dietary intakes for 2–11-year-old children ranged 2.55–4.09 μg/kg bw/day,accounting for 91.1–146.1% of the TDI of 2.8 µg/kgbw/day as set by EFSA. The 97.5th percentile dietary
74 Z. CAO ET AL.
intake ranged from 6.5 to 14.37 μg/kg bw/day, of whichall THQ values exceeded 1 in any age group. Withrespect to hypersensitivity, all MOEs calculated fromthese exposure levels were considerably below 10 forall age groups, both for estimated mean and high diet-ary exposure levels. The results suggest that the currentdietary exposure to Ni in rice is of concern for theChinese population, especially for children of2–11 years old and for Ni-sensitive individuals.Children of 2–11 years old in China had the highestestimated daily dietary exposure to Ni for rice con-sumption because of its higher intake per kg bw(Renwick et al. 2000; Chen et al. 2009). Some studieshave emphasised the potential risk of exposure of chil-dren to Ni contamination (Nasreddine et al. 2010).According to the 2006 UK Total Diet Study (Rose et al.2010), the highest estimated total dietary exposure toNi (7.54–8.32 μg/kg bw/day) was observed in childrenof 1.5–4.5 years old.
Ni daily intake obtained for rice consumption in thisstudy and similar foods in several countries were com-pared in Table 6. It can be concluded that the dietaryexposure risk to Ni for cereal consumption does notlead to a serious health risk for all reporting countries,except for United Kingdom and China. The highestdietary intake of Ni was observed in rice of China(Wang et al. 2014) and the lowest was found in riceand semolina in France (Leblanc et al. 2005). The dailyexposure to Ni in rice in the present study appearedsomewhat lower than that in the study reported byWang et al. (2014) but remarkably higher than thosein cereal and cereal products reported in other coun-tries. The relatively higher exposure to Ni for rice
consumption in China is possibly attributed to the dif-ference between dietary pattern of Chinese people andWestern European consumers, as Chinese generallyconsume more rice. On the other hand, the high dietaryexposure values obtained in this study could also bepossibly due to a few heavily contaminated rice sam-ples from areas with a high Ni background. Therefore, itis essential to strengthen monitoring for Ni contamina-tion in rice grains and its daily dietary intake. Besides,some measures could be taken to control Ni contam-ination in rice, especially in the more extensively con-taminated regions. These measures could includereducing industrial and mineral Ni emission to the agri-cultural area and select rice genotypes which areinclined to take up less Ni than other types.
Conclusions
Ni concentrations in 1332 milled rice samples obtainedfrom 11 provinces of the 3 main rice-producing regionsin China during 2015 ranged from 0.06 to 1.31 mg/kg,with an average of 0.49 ± 0.51 mg/kg, which was muchhigher than reported before in United Kingdom, Franceand Iran. The significant variations (P < 0.05) of Ni levelswere observed both among different provinces andamong varieties grown in the same location. MeanTHQs for chronic risk ranged from 1.24 to 1.46 forchildren of 2–11 years old and all MOEs for hypersensi-tivity risk were below 10 for all age groups, indicatingthat the current dietary exposure to Ni in rice is ofconcern for the Chinese population, especially for2–11-year-old children and Ni-sensitive individuals.
Table 5. Estimated dietary exposure of Ni (μg/kg bw/day) in milled rice samples for different age and gender groups of the Chinesepopulation.
The results indicate a need for regular monitoring of Nicontamination in rice, especially in more Ni-contami-nated regions, to control Ni intake by consumers.
Acknowledgments
We express our gratefulness and sincerest thanks to PhDXuefei Mao (Institute of Quality Standards and TestingTechnology for Agro-Products, Chinese Academy ofAgricultural Sciences) for effective advice in manuscriptwriting.
Disclosure statement
No potential conflict of interest was reported by the authors.
Funding
This work was supported by the National Agricultural ProductQuality and Safety Risk Assessment Major Project: [GrantNumber GJFP201500701]; the Central Public-interestScientific Institution Basal Research Fund: [Grant Number2014RG006-2]; the Special Agricultural Program for Scienceand Technology Project of Zhejiang Province [Grant Number2014C02002].
References
Arnich N, Sirot V, Rivière G, Jean J, Nöel L, Guérin T, LeblancJC. 2012. Dietary exposure to trace elements and health riskassessment in the 2nd French total diet study. Food ChemToxicol. 50:2432–2449.
Bontinck WJ. 1993. Nickel, cobalt and chromium in consu-mer products: a role in allergic contact dermatitis? ContactDermatitis. 28:15–25.
Cempel M, Nikel G. 2006. Nickel: a review of its sources andenvironmental toxicology. Pol J Environ Stud. 15:375–382.
Chen C, Li Y, Chen M, Chen Z, Qian Y. 2009.Organophosphorus pesticide residues in milled rice (Oryzasativa) on the Chinese market and dietary risk assessment.Food Addit Contam Part. 26:340–347.
D’Ambrosio FP, Bagnato GF, Guarneri B, Musarra A, LorenzoGD, Dugo G, Ricciardi L. 1998. The role of nickel in foodsexacerbating nickel contact dermatitis. Allergy. 53:143–145.
Domingo JL, Perelló G, Bordonaba JG. 2012. Dietary intake ofmetals by the population of Tarragona County (Catalonia,Spain): results from a duplicate diet study. Biol Trace ElemRes. 146:420–425.
[EFSA] European Food Safety Authority. 2009. Guidance of theScientific Committee on a request from EFSA on the use ofthe benchmark dose approach in risk assessment. EFSA J.2009:1–72.
[EFSA CONTAM Panel] EFSA Panel on Contaminants in theFood Chain. 2015. Scientific opinion on the risks to publichealth related to the presence of nickel in food and drink-ing water. EFSA J. 13:4002, 1–202.
Foxall K. 2009. Nickel toxicological overview. London: CHAPDHQ, Health Protection Agency.
Fu J, Zhou Q, Liu J, Liu W, Wang T, Zhang Q, Jiang G. 2008.High levels of heavy metals in rice (Oryza sativa L.) from atypical E-waste recycling area in southeast China and itspotential risk to human health. Chemosphere. 71:1269–1275.
[IARC] International Agency for Research on Cancer. 2012.Nickel and nickel compounds. IARC Monographs 100 C.Lyon: World Health Organization.
Iyaka YA. 2011. Nickel in soils: A review of its distribution andimpacts. Sci Res Essays. 6:6774–6777.
Jensen CS, Menné T, Duus Johansen J. 2006. Systemic contactdermatitis after oral exposure to nickel: a review with amodified meta-analysis. Contact Dermatitis. 54:79–86.
Kazi TG, Jalbani N, Baig JA, Arain MB, Afridi HI, Jamali MK,Shah AQ, Memon AN. 2010. Evaluation of toxic elements inbaby foods commercially available in Pakistan. Food Chem.119:1313–1317.
Khan S, Cao Q, Zheng YM, Huang YZ, Zhu YG. 2008. Healthrisks of heavy metals in contaminated soils and food cropsirrigated with wastewater in Beijing, China. Environ Pollut.152:686–692.
Table 6. Estimated mean daily dietary exposure (μg/kg bw/day) to Ni in cereal and cereal products from different countries.Country/Year Food type Exposure Population Reference
France/2000 Rice and semolina 0.006a >15 years Leblanc et al. (2005)UK/2006 Miscellaneous cereals 0.24–0.26b >18 years Rose et al. (2010)
0.67–0.78 1.5–4.5 years0.42–0.49 4–18 years
France/2006 Rice and wheat products 0.03 3–17 years Arnich et al. (2012)0.02 118–79 years
Lebanon /2010 Bread and cereals 0.91a Adult Nasreddine et al. (2010)Iran/2014 Rice 0.007 Adult Pirsaheb et al. (2016)China/2014 Rice 6.5 2–3 years Wang et al. (2014)
4.1 4–17 years3.15 18–70 years
China/2015 Rice 4.03 2–4 years Present study2.30–3.9 4–18 years1.86–2.30 18–80 years
aAssuming mean body weight of adults is 60 kg.bData derived from the estimated total dietary exposure.
76 Z. CAO ET AL.
Koch W, Karim MR, Marzec Z, Miyataka H, Himeno S, AsakawaY. 2016. Dietary intake of metals by the young adult popu-lation of Eastern Poland: results from a market basketstudy. J Trace Elem Med Bio. 35:36–42.
Leblanc JC, Guérin T, Noël L, Calamassi-Tran G, Volatier JL,Verger P. 2005. Dietary exposure estimates of 18 elementsfrom the 1st French total diet study. Food Addit Contam.22:624–641.
Lei M, Tie BQ, Song ZG, Liao BH, Lepo JE, Huang YZ. 2015.Heavy metal pollution and potential health risk assessmentof white rice around mine areas in Hunan Province, China.Food Secur. 7:45–54.
Li B, Wang X, Qi X, Huang L, Ye Z. 2012. Identification of ricecultivars with low brown rice mixed cadmium and lead con-tents and their interactions with the micronutrients iron, zinc,nickel and manganese. J Environ Sci. 24:1790–1798.
Li ZY, Ma ZW, van der Kuijp TJ, Yuan ZW, Huang L. 2014. A reviewof soil heavy metal pollution from mines in China: pollutionand health risk assessment. Sci Total Environ. 468:843–853.
Liu HY, Probst A, Liao BH. 2005. Metal contamination of soilsand crops affected by the Chenzhou lead/zinc mine spill(Hunan, China). Sci Total Environ. 339:153–166.
Marzec Z. 2004. Alimentary chromium, nickel, and seleniumintake of adults in Poland estimated by analysis and calcu-lations using the duplicate portion technique. Food/Nahrung. 48:47–52.
Nasreddine L, Nashalian O, Naja F, Itani L, Parent-Massin D,Nabhani-Zeidan M, Hwalla N. 2010. Dietary exposure toessential and toxic trace elements from a total diet studyin an adult Lebanese urban population. Food Chem Toxicol.48:1262–1269.
Nielson FH. 1984. Ultratrace elements in nutrition. Annu RevNutr. 4:21–41.
Nielsen GD, Søderberg U, Jørgensen PJ, Templeton DM,Rasmussen SN, Andersen KE, Grandjean P. 1999. Absorptionand retention of nickel from drinking water in relation to foodintake and nickel sensitivity. Toxicol Appl Pharm. 154:67–75.
Onianwa PC, Lawal JA, Ogunkeye AA, Orejimi BM. 2000.Cadmium and nickel composition of Nigerian foods. JFood Compos Anal. 13:961–969.
Pirsaheb M, Fattahi N, Sharafi K, Khamotian R, Atafar Z. 2016.Essential and toxic heavy metals in cereals and agriculturalproducts marketed in Kermanshah, Iran, and human healthrisk assessment. Food Addit Contam Part B. 9:15–20.
Renwick AG, Dorne JL, Walton K. 2000. An analysis of the needfor an additional uncertainty factor for infants and children.Regul Toxicol Pharm. 31:286–296.
Rose M, Baxter M, Brereton N, Baskaran C. 2010. Dietaryexposure to metals and other elements in the 2006 UKtotal diet study and some trends over the last 30 years.Food Addit Contam Part. 27:1380–1404.
Sreekanth TVM, Nagajyothi PC, Lee KD, Prasad TNVKV. 2013.Occurrence, physiological responses and toxicity of nickelin plants. Int J Environ Sci Te. 10:1129–1140.
Tian HZ, Lu L, Cheng K, Hao JM, Zhao D, Wang Y, Jia WX, QiuPP. 2012. Anthropogenic atmospheric nickel emissions andits distribution characteristics in China. Sci Total Environ.417:148–157.
Turconi G, Minoia C, Ronchi A, Roggi C. 2009. Dietary expo-sure estimates of twenty-one trace elements from a totaldiet study carried out in Pavia, Northern Italy. Brit J Nutr.101:1200–1208.
U.S. EPA. 2000. Risk-based concentration table. Philadelphia(PA): U.S. Environmental Protection Agency.
Wang W, Zhang ZH, Yang GL, Wang Q. 2014. Health riskassessment of Chinese consumers to nickel via dietary intakeof foodstuffs. Food Addit Contam Part A. 31:1861–1871.
Wei BG, Yang LS. 2010. A review of heavy metal contamina-tions in urban soils, urban road dusts and agricultural soilsfrom China. Microchem J. 94:99–107.
[WHO] World Health Organization. 2005. Nickel in drinking-water. Background document for development of WHOguidelines for drinking-water quality. Geneva: WorldHealth Organization (WHO/SDE/WSH/05.08/55).
[WHO] World Health Organization. 2008. Guidelines for drink-ing-water quality. Third edition incorporating the first andsecond addenda. Vol. 1. Geneva: World HealthOrganization.
Wittsiepe J, Schnell K, Hilbig A, Schrey P, Kersting M, WilhelmM. 2009. Dietary intake of nickel and zinc by young chil-dren–Results from food duplicate portion measurements incomparison to data calculated from dietary records andavailable data on levels in food groups. J Trace Elem MedBio. 23:183–194.
Wu M, Wang G, James B, Chen Y, Hu Z, Zheng C. 2015.Accumulation of soil nickel in the grains of differentIndica rice. Chin J Trop Crops. 9:006. Chinese.
Yang Y, Deng L. 2005. Effects of heavy metals in the paddysoil in Sichuan province on rice grain. J Agro-Environ Sci.24:174–177.
Zhang GP, Yao HG, Wu W, Xu M. 2006. Genotypic and envir-onmental variation in cadmium, chromium, arsenic, nickel,and lead concentrations in rice grains. J Zhejiang Univ SciB. 7:565–571.
