Concentrations of arsenic, cadmium and lead in human hair and typical foods in eleven Chinese cities

Environmental Toxicology and Pharmacology 48 (2016) 150–156

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Concentrations of arsenic, cadmium and lead in human hair and typical foods in eleven Chinese cities Tong Zhou a , Zhu Li a , Fan Zhang a , Xiaosan Jiang b , Weiming Shi a , Longhua Wu a,∗ , Peter Christie a a b

Key Laboratory of Soil Environment and Pollution Remediation, Institute of Soil Science, Chinese Academy of Sciences, Nanjing 210008, China College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing 210095, China

a r t i c l e

i n f o

Article history: Received 16 June 2016 Received in revised form 12 October 2016 Accepted 15 October 2016 Available online 19 October 2016 Keywords: Hair analysis Contaminants Food intake As Cd Pb

a b s t r a c t Concentrations of arsenic (As), cadmium (Cd) and lead (Pb) were determined in 384 human hair samples and 445 purchased food samples from 11 cities in China. The mean concentrations of hair As, Cd and Pb were 0.23, 0.062 and 2.45 mg kg−1 , respectively. The As, Cd and Pb concentrations in different foods were lower than the national maximum allowable contaminant levels. By comparison, males had higher hair As concentrations but lower Cd concentrations than females. When the interaction effects of gender and age were considered, males had the higher hair As, Cd and Pb concentrations in the 51–65 year-old age group. Residents of rural areas had higher hair As, Cd and Pb concentrations than people living in urban areas. Further analysis indicates that hair As, Cd and Pb concentrations and their changes with biological and environmental factors cannot be satisfactorily explained by the estimated intakes from purchased food. © 2016 Published by Elsevier B.V.

1. Introduction Arsenic (As), cadmium (Cd) and lead (Pb) are among the most important inorganic contaminants of plants, animals, and humans (Gochfeld, 2007; Vázquez et al., 2015). Continuous exposure to these contaminants may result in bioaccumulation and cause negative biological effects to human health depending upon the level and duration of exposure (Vahter et al., 2007). Determination of human risk from occupational and environmental exposure has usually been conducted during the past few decades through the measurement of contaminants in biological materials such as blood, serum, urine, hair, fingernails and saliva (Esteban and ˜ 2009; Gil et al., 2011). Blood and urine are the most comCastano, monly sampled biological materials but hair analysis has certain advantages as it is a painless and non-invasive method and hair is chemically inert with relatively high concentrations of contaminants, can be easily transported and stored, and reflects the status of the body over long time periods (Kempson and Lombi, 2011). Conversely, the disadvantages of hair analysis include the potential for external contamination and the fact that the kinetics of the biochemical mechanisms by which contaminants are incorporated

∗ Corresponding author. E-mail address: [email protected] (L. Wu). http://dx.doi.org/10.1016/j.etap.2016.10.010 1382-6689/© 2016 Published by Elsevier B.V.

into hair are not well known, and there is insufficient information ˜ to define reference ranges for contaminants (Esteban and Castano, 2009). The International Atomic Energy Agency (IAEA) accepts the use of mineral analysis of hair for measuring the levels of essential and toxic trace elements in living organisms including humans (Ryabukkin, 1978). Hair analysis has been widely used for the biological monitoring of human exposure to contaminants and for estimation of the nutritional status of individuals. Numerous studies confirm significant differences between exposed and non-exposed residents, and exposure to contaminants gives higher hair As, Cd and Pb concentrations (Wang et al., 2009; Gil et al., 2011; Hao et al., 2015; Massaquoi et al., 2015). In addition, the normal or reference ranges for contaminants in hair are important in the assessment of the health status of individuals (Kempson and Lombi, 2011). Hair analysis is now used as the tool for the diagnosis of reference ranges of As, Cd and Pb in Italy (Dongarrà et al., 2011), Poland (Chojnacka et al., 2010) and Russia (Skalny et al., 2015). By comparison, existing data vary widely in China and in other countries. These differences may be attributed to physiological variables such as hair colour, age, gender, body composition, and ethnicity which influence the incorporation of contaminants into hair (Chojnacka et al., 2006; Kempson and Lombi, 2011; Hao et al., 2015). Several studies in China have previously reported the concentrations of As, Cd and Pb in hair of residents (Huang et al., 2014; Li et al., 2014a; Luo et al.,

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2014). However, the results from one or two cities reported in these studies cannot adequately represent the reference status of hair contamination on a large scale due to differences in environmental conditions and lifestyles across the whole country. Although some individuals are primarily subjected to occupational exposure to many contaminants, food intake is the main route of entry of As, Cd and Pb into most humans through oral ingestion and the gastrointestinal tract (Vázquez et al., 2015). Consequently, information about concentrations and intakes of contaminants from foods is very important in the assessment of risk to human health by hair analysis. However, the absence of a significant correlation between contaminant intake and the corresponding concentration in hair of young students has been reported in Spain (Gonzalez-Munoz et al., 2008). Therefore, the relationships between hair As, Cd and Pb concentrations and the corresponding intakes from food need detailed characterisation in China. The two main purposes of the present study were therefore to evaluate the overall concentrations of As, Cd and Pb in the hair of residents of different Chinese cities and determine the effects of gender, age and residential area on contaminant concentrations in hair, and to assess the As, Cd and Pb concentrations in different groups of food purchased in these cities and analyse the contribution of food intake to the accumulation of As, Cd and Pb in human hair.

2. Materials and methods 2.1. Sample collection and preparation Hair and food samples were collected from 11 cities (Graphical abstract), namely Harbin (HRB) in Heilongjiang province, Fuxin (FX) in Liaoning province, Tangshan (TS) in Hebei province, Xi’an (XA) in Shaanxi province, Zhengzhou (ZZ) in He’nan province, Nanjing (NJ) in Jiangsu province, Wuhan (WH) in Hubei province, Fuzhou (FZ) in Fujian province, Nanning (NN) in Guangxi autonomous region, Chengdu (CD) in Sichuan province and the municipality of Shanghai (SH). These selected cities constituted the areas sampled in the Fourth China Total Diet Study of 2007 (Wu and Li, 2015). They represent the major densely populated regions in China with populations of over one million inhabitants and have strong agriculture-driven economies. Ideally, hair and food samples would be collected randomly from both urban and rural areas. However, samples were collected only from rural areas in NJ city and urban areas in SH and WH cities due to some factors outside our control. Hair samples from each participant weighing approximately 2.0 g were cut with stainless steel scissors between 1 and 3 cm as close as possible to the scalp from the occipital region of the head and sealed in plastic bags. During sample collection some basic personal information such as gender, age and health status were recorded. A total of 384 hair samples were collected from local healthy people of ages 13 to 65 years across the 11 cities, 218 from males and 166 from females. A total of 445 food samples comprising vegetables (351), cereals (39), meat (39) and fish (16) were also purchased from three local major supermarkets in each city. The vegetables included leafy vegetables, fruit vegetables, root and stem vegetables and edible fungi and the cereals included primary products from the grains of rice, wheat, maize and beans. Meat samples included pork, beef, mutton, chicken and duck and the fish samples included both freshwater and marine species. The hair samples were prepared for digestion and elemental analysis by washing five times with acetone and deionized water (Milli-Q Millipore 18.2 M cm−1 ) following the sequence acetonewater-water-water-acetone according to the method proposed by the IAEA (Ryabukkin, 1978). The samples were then air-dried, cut into 5-mm pieces and stored in plastic bags before digestion. The

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food samples were washed with deionized water three times, oven dried at 80 ◦ C and ground prior to chemical digestion. 2.2. Sample digestion and analysis The procedures for the digestion of hair and food samples have been described in detail previously (Li et al., 2014b). Samples (0.5 g) were placed in 50-ml high-pressure polytetrafluoroethylene (PTFE) digestion containers with 2 ml 30% H2 O2 and 6 ml 65% HNO3 and the sealed containers were placed in a digestion vessel at 160 ◦ C for 8 h. After digestion the sample solutions were then evaporated at 130 ◦ C on an electric evaporation block until about 2 ml solution remained. The remaining solution was transferred to a clean 15-ml polycarbonate tube and made up to final volume with deionized water for the elemental analysis. At least duplicate digestions of all hair and food samples were prepared. Both H2 O2 and HNO3 (Guaranteed Reagent grade) were obtained from Nanjing Chemical Reagent Co. Ltd. (Nanjing, China). The concentration of As in the digests was determined by atomic fluorescence spectrometry (AFS-610D2, Rayleigh, Beijing, China) and the concentrations of Cd and Pb in solution were determined by inductively coupled plasma-mass spectrometry (ICP-MS, Agilent 7700×, Santa Clara, CA). Certified reference materials comprising human hair (GBW07601), rice (GBW10045), meat (GBW08552) and cabbage (GBW10014) were used (National Research Centre for Standards, China) for quality control. The recovery rates of elements in the certified reference materials ranged between 88.7 and 108% and the limits of detection (LODs) obtained for As, Cd and Pb were 0.002, 0.001 and 0.003 mg kg−1 , respectively. When the concentration of an element was below the LOD the values were set at half the LOD and treated as real values in the statistical analysis. Blanks were included in every batch of samples to check for possible contamination and procedural blanks were analysed every two hours to monitor variations in blank levels. The toxicity of contaminants, especially As, varies considerably depending on their chemical forms. However, we analysed only the total As concentrations in food and hair. 2.3. Intake estimates The daily intakes of As, Cd and Pb from the cereals, vegetables, meat and fish were estimated by the following equation: Intake(gkg bw−1 d−1 =

Cc × Ac + Cv × Av + Cm × Am + Cf × Af (1) BW

where Cc , Cv , Cm and Cf are the mean concentrations of contaminants (mg kg−1 ) and Ac , Av , Am and Af are the amounts consumed (g d−1 ) in cereals, vegetables, meat and fish, respectively. The BW is the average human body weight. The concentrations of contaminants in different foodstuffs were obtained by analysis. The amounts of different foodstuffs for Chinese consumers were obtained from the Fourth China Total Diet Study (Wu and Li, 2015) and were classified by gender, age and province (Tables S1, S2). However, food consumption in Jiangsu province where NJ city is located was not reported in the Fourth China Total Diet Study. Accordingly, the food consumption in NJ was assigned the mean levels from SH city because NJ is very close to SH geographically and the residents of the two cities have similar eating habits. The BW values for people of different gender and age were obtained from the Fourth China Total Diet Study (Table S1) but the BW values in the individual cities were not given (Wu and Li, 2015). 2.4. Statistical analysis Data analysis was performed using the SPSS version 20.0 for Windows software package. Data with a skewed distribution were

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normalised by transformation to natural logarithms (ln) prior to statistical analysis. After ln-transformation, Student’s t-test or one-way analysis of variance followed by LSD (least significant difference) post hoc test were used for group comparisons of mean values of hair As, Cd and Pb concentrations by gender, residential area and city. Pearson correlation analysis was used to study the relationships between hair As, Cd and Pb concentrations and their corresponding intakes from foods in the different cities. The statistical significance level was set at p < 0.05. To facilitate data interpretation and compare studies across a wide range of experimental conditions, an antilogarithmic function was used to transform the ln-transformed data back to the original scale to obtain the values of confidence interval (CI) and mean (Zhou and Guo, 1997). Finally, the 95% CI and mean values of food and hair contaminant concentrations and food contaminant intakes were calculated for each subgroup.

Table 1 Mean concentrations (in mg kg−1 fresh weight) and 95% CI (confidence intervals) of As, Cd and Pb in different foods. Contaminant

Food

n

Mean

95% CI

As

Vegetables Cereals Meat Fish

350 39 39 16

0.11 0.054 0.064 0.080

0.099–0.13 0.038–0.077 0.049–0.083 0.057–0.11

Cd

Vegetables Cereals Meat Fish

347 39 39 16

0.24 0.068 0.003 0.007

0.20–0.28 0.039–0.12 0.002–0.003 0.004–0.013

Pb

Vegetables Cereals Meat Fish

351 39 39 16

0.61 0.32 0.21 0.22

0.58–0.65 0.31–0.33 0.18–0.23 0.18–0.27

3. Results 3.1. Concentrations and estimated intakes of As, Cd and Pb in foods The concentrations of As, Cd and Pb in the different foodstuffs are shown in Table 1. Vegetables had the highest mean concentrations of As, Cd and Pb compared with other foodstuffs (p < 0.05). Based on the daily consumption of the selected foods, human body weights (Table S1), and the corresponding contaminant concentrations, we estimated the daily intakes of As, Cd and Pb from different foods of males and females from different age groups (Fig. 1a–c). The total mean intakes of As, Cd and Pb estimated from vegetables, cereals, meat and fish consumption from the 11 cities were 1.44, 2.31 and 7.62 ␮g kg bw−1 d−1 , respectively. The mean intakes of As, Cd and Pb for adults (20–65 years) were 1.36–1.44, 2.24–2.34 and 7.28–7.65 ␮g kg bw−1 d−1 , respectively. We observed that humans in the 13–19 year-old age group had slightly high intakes of As, Cd and Pb (both males and females) compared with the 20–65 yearold groups. The estimated intakes of As, Cd and Pb from vegetables,

cereals, meat and fish were not significantly different between males and females in each age group. Overall, vegetables and cereals were the main contributors to food As (55.0 and 34.6%), Cd (72.5 and 27.1%) and Pb (55.8 and 38.2%) intakes in the present study. In the Fourth China Total Diet Study (Wu and Li, 2015), however, the consumption rates of vegetables, cereals, meat and fish are given only for males but not for female adults and the body weight of humans are not given within these selected cities (Table S2). As shown in Fig. 1 (d–f), the daily As, Cd and Pb intakes (␮g d−1 ) from foods of male adults varied greatly within the cities sampled and no consistent trends were observed. Based on the annual consumption of the selected foods (Fig. S1) from the Chinese Statistical Yearbook (NBSPRC, 2012), the daily intakes of As, Cd and Pb were also estimated for residents of urban and rural areas in the present study (Fig. 2). The results show that intakes of As, Cd and Pb from foods by residents were 5.31, 25.8 and 21.0% higher in rural areas than that in urban areas.

Fig. 1. Intakes of As, Cd and Pb from vegetables, cereals, meat and fish in different cities and their overall mean values (a, b, c) and in different age groups and genders (d, e, f). The units of intakes are presented as ␮g kg bw−1 d−1 in figures a, b and c but are presented as ␮g d−1 kg−1 in figures d, e and f.

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Table 2 Mean concentrations and 95% CI of As, Cd and Pb in hair classified by gender and age (mg kg−1 ). Age

Males

Females

Total

Mean

95% CI

n

Mean

95% CI

N

Mean

95% CI

n

As 13–19 20–50 51–65 Total

0.25 0.17 0.59 0.20

0.14–0.45 0.14–0.21 0.17–2.06 0.17–0.24

28 172 18 218

0.13 0.097 0.15 0.11

0.037–0.45 0.063–0.15 0.071–0.30 0.074–0.16

12 137 17 166

0.22 0.17 0.30 0.23

0.12–0.40 0.13–0.22 0.15–0.62 0.18–0.29

40 309 35 384

Cd 13–19 20–50 51–65 Total

0.035 0.038 0.084 0.041

0.021–0.057 0.032–0.045 0.045–0.16 0.034–0.048

28 172 18 218

0.062 0.059 0.051 0.058

0.047–0.082 0.050–0.068 0.036–0.073 0.051–0.066

12 137 17 166

0.046 0.048 0.066 0.062

0.031–0.068 0.042–0.054 0.046–0.093 0.055–0.069

40 309 35 384

Pb 13–19 20–50 51–65 Total

2.19 2.35 4.46 2.47

1.50–3.19 2.04–2.69 2.70–7.38 2.17–2.81

28 172 18 218

2.87 2.55 3.24 2.63

2.04–4.04 2.26–2.87 2.03–5.18 2.35–2.93

12 137 17 166

2.42 2.44 3.81 2.45

1.81–3.23 2.23–2.68 2.71–5.36 2.25–2.68

40 309 35 384

Fig. 2. Intakes (␮g d−1 ) of As, Cd and Pb from vegetables, cereals, meat and fish in urban and rural areas.

The As, Cd and Pb concentrations in hair of residents of rural areas were 39.4, 91.8 and 74.1% higher (p < 0.05) than those of urban areas (Table 3). Great variations in hair As, Cd and Pb concentrations among the 11 cities were also observed. The mean concentrations of hair Cd and Pb were consistently lower in the cities FX, SH, TS and HRB but higher in NJ, ZZ and XA. Hair with As concentrations <0.10 mg kg−1 was collected from FZ, HRB, TS and FX, and hair with As concentrations >0.25 mg kg−1 was collected from NN, XA and ZZ. As stated above, hair samples were collected only from rural areas in NJ and from urban areas in SH and WH. In Table S4 it can be seen that the hair As, Cd and Pb concentrations were affected significantly by the interaction between residential areas and cities. If we combine the results from urban and rural areas (Table S5), mean hair As, Cd and Pb concentrations were consistently low in HRB and FX but high in XA and ZZ. Correlation analysis results further show that there were no significant relationships between hair concentration and food intake in terms of As, Cd and Pb for male adults in the cities sampled (Fig. S3). 4. Discussion

3.2. Concentrations of As, Cd and Pb in hair 4.1. Total As, Cd and Pb concentrations in foods and their intakes After logarithmic transformation the concentrations of hair As, Cd and Pb approximated to a normal distribution (Fig. S2). The overall mean concentrations of As, Cd and Pb in hair were 0.23, 0.062 and 2.45 mg kg−1 with 95% CI of 0.18–0.29, 0.055–0.069 and 2.25–2.68 mg kg−1 , respectively (Table 2). The t-test shows that the hair As concentration of males were higher than females at each age group (p < 0.05). In contrast, males had lower hair Cd concentrations than did females (p < 0.05). However, the lower hair Cd concentrations of males than females occurred only at age groups 13–19 and 20–50 years. At age group 51–65 years, males still had higher Cd concentration in hair than females (p < 0.05). Although the total hair Pb concentrations were not significantly different between males and females, the males also showed higher Pb concentrations in hair than females at age group 51–65 years (p < 0.05). Among the three age groups, people in the 51–65 year-old age group had higher hair As, Cd and Pb concentrations than those in the other two age groups, especially in the case of males. However, the hair As, Cd and Pb concentrations were not significantly different between the 13–19 and 20–50 year-old groups. We observed that there were interaction effects of gender and age on hair contaminant concentrations (Table S3). When the factors of gender and age were considered simultaneously we found that males had the highest (p < 0.05) hair As, Cd and Pb concentrations in the 51–65 year-old age group.

In the recommendations of the Chinese National Food Safety standard (MHPRC, 2012), the maximum allowable concentrations in vegetables, cereals, meat and fish are 0.5, 0.2, 0.5 and 0.5 (inorganic) mg kg−1 for As; 0.5, 0.2, 0.1 and 0.1 mg kg−1 for Cd; and 1.0, 0.5, 0.2 and 0.5 mg kg−1 for Pb, respectively. In the present study, the mean concentrations of As, Cd and Pb in the different types of food were below the maximum allowable concentrations of contaminants in foods recommended by the MHPRC (2012) except for the Pb concentration in meat which was slightly above the limit. However, Cd and Pb concentrations in vegetables and Pb concentrations in cereals and meat were higher than the maximum levels set for Cd (0.2 mg kg−1 in vegetables) and Pb (0.3, 0.2 and 0.1 mg kg−1 in vegetables, cereals and meat) in foodstuffs by the European Union (EC, 2006) and the Food and Agricultural Organisation of the United Nations (CAC, 1995). In 2006 the French Food Safety Agency conducted a second French Total Diet Study to estimate dietary exposures to trace elements from 1319 samples of food habitually consumed by the French population (Arnich et al., 2012). Most of the food samples in France had lower As, Cd and Pb concentrations than we found in the present study. The concentrations of As, Cd and Pb in selected foodstuffs (114 samples) of vegetables, cereals, meat and fish from Serbian market baskets were also lower than the results found in foods in the present study

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Table 3 Mean concentrations and 95% CI of As, Cd, Pb in hair in different residential areas and cities (mg kg−1 ). Variable

Area City

n

Urban Rural NJ SH WH FZ NN CD HRB FX TS XA ZZ

203 181 24 21 18 38 50 34 29 48 35 44 43

As

Cd

Pb

Mean

95% CI

Mean

95% CI

Mean

95% CI

0.16 0.22 0.20 0.16 0.21 0.061 0.44 0.13 0.099 0.094 0.074 0.27 0.27

0.12–0.22 0.16–0.31 0.14–0.30 0.11–0.24 0.11–0.39 0.027–0.14 0.20–0.97 0.087–0.21 0.035–0.28 0.067–0.13 0.060–0.093 0.15–0.51 0.11–0.70

0.035 0.067 0.13 0.025 0.038 0.044 0.050 0.046 0.034 0.017 0.033 0.072 0.083

0.030–0.040 0.057–0.079 0.079–0.21 0.018–0.035 0.024–0.062 0.031–0.064 0.039–0.064 0.035–0.061 0.026–0.044 0.013–0.021 0.025–0.044 0.050–0.10 0.059–0.12

1.91 3.33 4.88 1.11 2.48 2.42 2.53 2.44 1.46 1.45 2.44 2.79 4.61

1.73–2.12 2.92–3.79 3.55–6.73 0.77–1.62 1.93–3.17 1.99–2.94 2.10–3.04 1.84–3.24 1.21–1.77 1.21–1.74 1.91–3.12 2.15–3.62 3.34–6.37

with the exceptions of As (0.43 mg kg−1 ) and Cd (0.029 mg kg−1 ) in canned fish (Skrbic´ et al., 2013). In the present study, the estimated intakes of As, Cd and Pb from purchased foods for adults (20–65 years) were higher than the dietary intakes of As, Cd and Pb for adults in France (Arnich et al., 2012) and Serbia (Skrbic´ et al., 2013). The higher estimated As, Cd and Pb intakes from foods in the present study were not only determined by the high food contaminant concentrations but also by the relatively large amounts of food consumed. According to the International Statistical Yearbook issued by the National Bureau of Statistics of the People’s Republic of China (NBSPRC, 2007), residents of China have the second largest daily consumption of vegetables, cereals, meat and fish among the 43 countries compared. In 2007 the Fourth China Total Diet Study reported that the intakes of Cd and Pb from foods were 0.54–0.91 and 1.36–1.76 ␮g kg bw−1 d−1 for residents of ages between 13 and 65 years, respectively (Wu and Li, 2015). In the present study the estimated intakes of Cd and Pb (2.31 and 7.62 ␮g kg bw−1 d−1 ) were also higher than the results published in the Fourth China Total Diet Study.

4.2. Hair As, Cd and Pb concentrations and related factors 4.2.1. Comparison with other studies of hair As, Cd and Pb concentrations At the similar ranges of age, a comparison of the mean concentrations of As and Cd in the hair of residents in different countries (Table 4) reveals that hair As and Cd concentrations in the present study were much lower than in most other countries investigated except for Italy and Russia (Varrica et al., 2014; Skalny et al., 2015; Zaitseva et al., 2015). Hair Pb concentrations were slightly lower than in Pakistan, Poland and other parts of China (Anwar, 2005; Wang et al., 2009; Chojnacka et al., 2010; Huang et al., 2014) but ˜ et al., were higher than in Italy, Russia and Spain (Pena-Fernández 2014; Varrica et al., 2014; Skalny et al., 2015; Zaitseva et al., 2015). Hair As, Cd and Pb concentrations in the Chinese cities sampled were at low levels within Asia but were still at slightly higher levels than in Italy, Russia or Spain. On a global basis, trace elements in the human body vary with the intrinsic nature of diet and physiological variables that influence the availability of trace elements for digestion, absorption and utilization (Freeland-Graves et al., 2014). We observed higher intakes of As, Cd and Pb from food in the current study than in some European countries. In addition, blood Cd and Pb concentrations are higher in humans of Asian ethnic background than those of European ethnic background (Muennig et al., 2012), and Cd and Pb concentrations in dark hair are higher than in blond hair (Chojnacka et al., 2006; Kempson and Lombi, 2011).

This indicates that Chinese residents will have higher absorption rates of contaminants than Europeans. The higher food intakes and absorption rates of contaminants by residents might therefore be the most important factors contributing to the higher hair As, Cd and Pb concentrations in China than in European counties.

4.2.2. Gender and age differences in hair As, Cd and Pb concentrations We found that males had higher As concentrations in hair than did females at each age group. A review carried out by Vahter et al. (2007) also found that males seem to be more susceptible to exposure to As than females. In contrast, males had lower Cd concentrations in hair than did females. In comparison to males, females have proportionately more body fat but lower rates of renal clearance, and hence females might store relatively more lipophilic metal ions to increase the contaminant concentration even when they have been metabolized and conjugated (Blaak, 2001; Gochfeld, 2007). In addition, deficiencies of Fe2+ in foods will enhance the absorption of other ingested divalent cations in the blood of females than of males, including Cd (Sudo et al., 2006; Gochfeld, 2007). In China the Fourth Total Diet Study reported that females had very low intakes of Fe from food consumption (Wu and Li, 2015). Contaminants in fat and blood can accumulate in hair shafts through the blood stream in the hair roots as the hair grows (Kempson and Lombi, 2011). Thus, more Cd accumulates in hair of females compared with males. However, the higher As and lower Cd concentrations in the hair of males than females cannot be explained solely by the absence of statistically significant differences in food Cd and Pb intakes. Previous studies have indicated gender related differences in hair As, Cd and Pb concentrations (Wang et al., 2009; Hao et al., 2015; Zaitseva et al., 2015). In the present study the differences in hair Pb concentration were not significant between males and females in the cities sampled. Humans in the 51–65 year-old age group had higher hair As, Cd and Pb concentrations than those in the other two age groups, especially in males. However, these results cannot be explained by the slightly low intakes of As, Cd and Pb in the 51–65 yearold age group compared with those of 13–19 and 20–50 year-olds. Although food requirements decrease with age, the need for essential trace elements of elderly persons generally remains the same as that of young adults (Ekmekcioglu, 2001). Elderly persons are therefore prone to develop trace element deficiencies (such as Fe) after weight loss (Ekmekcioglu, 2001). The deficiencies of Fe2+ intakes from food will result in greater rates of absorption and accumulation of other ingested divalent cations in the internal organs and hair (Sudo et al., 2006; Gochfeld, 2007; Vázquez et al., 2015). By comparison, we assumed that the absorption and accumulation

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Table 4 Mean concentrations and ranges of As, Cd and Pb in hair (mg kg−1 ) reported in different countries. Country

China China China China China Italy Japan Pakistan Pakistan Poland Russia Russia Spain

n

20 88 40 190 50 144 100 100 165 160 117 5908 59 54 96

As

Cd

Pb

Mean

Range

Mean

Range

Mean

Range

0.43 0.83 0.94 0.18 0.75 0.039 0.54 0.43 0.66 0.31 0.83 0.045 0.042 0.042 /

0.21–1.08 / 0.2–1.6 0.00–1.32 0.00–21.0 0.002–0.32 / / 0.21–1.48 / 0.65–3.96 0.01–0.08 0.02–0.17 0.02–0.26 /

0.21 0.11 0.09 0.028 0.46 0.019 0.11 0.086 / 0.08 0.09 0.034 0.016 0.033 /

0.12–0.34 / 0.01–0.40 0.00–0.81 0.00–8.91 0.00–1.9 / / / / 0.054–0.49 0.006–0.056 0.002–0.068 0.002–0.37 /

5.29 4.24 2.9 1.11 0.69 0.59 1.88 1.93 / 3.53 3.08 1.05 0.49 0.98 0.70

1.09–15.9 / 0.00–5.4 0.04–20.7 0.00–8.06 0.07–15 / / / / 0.00–10.9 0.19–1.39 0.047–6.5 0.084–4.8 0.11–2.65

Age

Reference

>1 15–65 / 20–98 >18 11–13 1–84 1–87 18–60 / 21–22 20–60 17–22 17–22 13–16

Wang et al. (2009) Huang et al. (2014) Massaquoi et al. (2015) Luo et al. (2014) Li et al. (2014a) Varrica et al. (2014) Schopfer and Schrauzer (2011) Shah et al. (2011) Anwar (2005) Chojnacka et al. (2010) Skalny et al. (2015) Zaitseva et al. (2015) ˜ Pena-Fernández et al. (2014)

“/” information not reported.

rates of As, Cd and Pb in hair by elderly males (51–65 years old) may be accelerated in certain conditions. Overall, the males in the 51–65 age group had the highest hair As, Cd and Pb concentrations in the cities sampled.

4.2.3. Hair As, Cd and Pb concentrations in different residential areas and cities The higher As, Cd and Pb concentrations of residents of rural areas than those of urban areas can also be partly explained by the higher intakes of contaminants from food consumption in the present study. However, the percentage increases in total As (5.31%), Cd (25.8%) and Pb (21.0%) intakes from foods were lower than the percentage increases in hair As (39.4%), Cd (91.8%) and Pb (74.1%) concentrations. A possible explanation might be that residents also eat vegetables and cereals grown by themselves instead of produce purchased in the market in rural areas. Taken together with the food intakes, there are also some other environmental or biological factors influencing the exposure opportunity, metabolism, toxicity kinetics, toxicity dynamics and modulation of As, Cd and Pb into the tissues or organs of the human body (Gochfeld, 2007). Due to the limited number of studies so far conducted, the mechanisms by which these uncertain factors increase the As, Cd and Pb concentrations in the hair of residents of rural areas compared with urban areas require further investigation. Among the 11 cities there were non-significant relationships between hair concentration and food intake in terms of As, Cd and Pb for male adults in the present study. Including food intake as a factor, the differences in hair As, Cd and Pb concentrations in these cities might also be determined by other, as yet unknown, factors. According to published statistics on atmospheric As and heavy metal concentrations of 44 major cities over the past decade in China, contamination with As, Cd and Pb varied significantly among cities and Zhengzhou city had the highest atmospheric Cd and Pb concentrations (Duan and Tan, 2013). In addition to the major exposure from food consumption, atmospheric particles were found to be an important source of endogenous deposition of Cd to human hair in the Pearl River Delta region in south China (Huang et al., 2014). On the North China Plain heavy metal concentrations in 139 groundwater samples collected from rural wells were also significantly different in five cities due to variations in natural and anthropogenic sources (Li et al., 2015). These differences in atmospheric sources and drinking water exposure might change the influence of food Cd and Pb intakes on their corresponding concentrations in the hair of residents of the 11 Chinese cities studied.

5. Conclusions This study reports the concentrations of As, Cd and Pb in the hair of residents and their corresponding concentrations in the foods consumed in different Chinese cities. Compared to other studies worldwide the hair As, Cd and Pb concentrations of residents of the 11 cities sampled were at normal levels. Human hair As, Cd and Pb concentrations varied according to gender, age and residential area. Hair of males seems to be more susceptible to As exposure while females seem to be more susceptible to Cd exposure. Hair As, Cd and Pb concentrations were higher in the 51–65 year-old age group than in the 13–19 and 20–50 year-old groups, especially in males. Residents of rural areas usually had higher As, Cd and Pb concentrations in hair than those of urban areas. Hair As, Cd and Pb concentrations varied significantly among the 11 cities. Taking into account the influencing factors of gender, age, residential area and city, the status of hair As, Cd and Pb concentrations may be not fully explained by the estimated intakes from the purchased foods in the cities sampled. Conflict of interest None. Acknowledgement This research was supported by the National Natural Science Foundation of China (No. 41325003). Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.etap.2016.10.010. References Anwar, M., 2005. Arsenic, cadmium and lead levels in hair and toenail samples in Pakistan. Environ. Sci. 12, 71–86. Arnich, N., Sirot, V., Rivière, G., Jean, J., Noël, L., Guérin, T., Leblanc, J.C., 2012. Dietary exposure to trace elements and health risk assessment in the 2nd French Total Diet Study. Food Chem. Toxicol. 50, 2432–2449. Blaak, E., 2001. Gender differences in fat metabolism. Curr. Opin. Clin. Nutr. Metab. Care 4, 499–502. CAC (Codex Alimentarius Commission), 1995. Codex general standard for contaminants and toxins in food and feed. CODEX STAN, 193–1995.

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