Abstract
The object of this study is to analyze the levels of seven toxic elements residues in raw bovine milk in China and assess the potential health risk of those residues. The 178 raw bovine milk samples were collected from eight main milk-producing provinces and from three types of milk stations in China, and were analyzed for arsenic (As), lead (Pb), cadmium (Cd), chromium (Cr), mercury (Hg), aluminum (Al), and nickel (Ni) using inductively coupled plasma-mass spectrometry (ICP-MS). Al, Pb, Hg, Ni, Cr, and As were detected in 47.8, 29.2, 28.1, 23.6, 12.4, and 9.0% of total milk samples, respectively, and Cd were not detected in all samples. The raw bovine milk samples with high levels of toxic elements were found in industrial areas, such as Heilongjiang and Shanxi. Nemerow pollution index analysis showed that the levels were lower in the samples from the processing plants than that from the large-scale farms and small farm cooperatives. The margin of exposure (MOE) values suggest that the levels of As, Pb, Hg, Cr, Al, and Ni in the raw milk samples are not causing a health risk for Chinese consumers, including adults and children. Nevertheless, the risk of Pb for infant and young children was more serious than adult.
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Introduction
Milk has been served as a main nutrition food for infants and also for adults. It is known as an excellent source of protein, and rich in minerals such as calcium, magnesium, iron, manganese, and zinc [1]. With the rapid increase of urbanization in China, great concerns have been raised regarding the potential impacts on the food by the contaminations of environment. Toxic elements are particularly important to environment contaminations, because excessive accumulation of dietary and non-dietary toxic elements in human body may cause some serious systemic health problems [2, 3]. Milk may also be contaminated with toxic elements due to environmental pollution [4], such as water, atmosphere, and soil, and from feed into cow milk [5,6,7]. Furthermore, the presence of toxic elements in milk could be an indicator of the environmental pollution [1, 8].
Many countries and international organizations have set the maximum residue levels (MRLs) of toxic elements in raw milk to guarantee the quality and safety of milk. The MRL of Pb is set as 0.02 mg/kg in European Union (EU) and Codex Alimentarius Commission (CAC). The MRLs of Pb, Cr, Hg, and As are set in China as 0.05, 0.3, 0.01, and 0.10 mg/kg, respectively [9,10,11]. Some researchers have paid close attention to toxic element levels in milk [1, 12,13,14,15,16]. Therefore, determination of the residual levels of toxic elements in milk and performing related risk assessment becomes necessary.
In China, the industrial type of the main milk-producing provinces as Heilongjiang, Hebei, Shandong, and Shanxi, are all heavy industries, include mining, smelting, and processing industry. In a previous study, we observed significantly higher concentrations of toxic elements in raw milk of a Chinese industry city [17]. For the past few years, the consumption of milk has been increased remarkably in China [3]. Despite the study of toxic elements in milk being reported commonly, the concentration and the risk for human health regarding toxic elements in Chinese milk is still lacking. Therefore, the purposes of this study were (1) to determine the heavy metals (As, Pb, Cd, Cr, Hg, Al, and Ni) in raw bovine milk from eight main milk-producing provinces; (2) to identify the contamination situation of different producing areas and milk stations; and (3) to conduct a health risk assessment of toxic elements attributed to the adult and child consumption.
Experimental and Methods
Reagents and Standards
High purity water was obtained by a Milli-Q water purification system (Millipore, Bedford, MA, USA). Nitric acid (65%, Sigma, Germany) was used for cleaning glassware and also for digesting milk samples along with 30% hydrogen peroxide (Merck, Germany). Multi-element standard solutions were used at the concentration of 10 mg/L for external calibration (SPEX CertiPrep, USA). One percent nitric acid was used to dilute the standard to 100 μg/L. Five standards with weighed linear regression were prepared at concentrations ranging from 0 to 4 μg/L for As, Pb, Cd, Cr, Al, and Ni. The Hg calibration curve was drawn from 5 points with the range from 0 to 2 μg/L.
The tuning solution which contains Li, Y, Co, Ce, and Ti was used to optimize the instrument (SPEX CertiPrep, USA), and an online internal standard solution containing 100 mg/L of each of Bi, Ge, In, Li, Lu, Rh, Sc, and Tb was prepared to calibrate data (SPEX CertiPrep, USA).
Sample Collection and Preparation
Sample Collection
A total of 178 raw bovine milk samples were collected from eight main milk-producing provinces in China during the period from May to August 2012. The raw milk samples were collected from three types of milk stations in China, including 80 raw milk samples from small farm cooperatives, 83 from large-scale farms, 15 from milk-processing plants, with the sample proportions of 5:5:1. The sample numbers and associated areas were given in Fig. 1.
After stirring the milk in each holding tank, 100 mL of raw milk sample was taken from the upper third, 100 mL from the middle third, and 100 mL from the lower third. A total of 300 mL milk from each tank was mixed and 100 mL of it was taken out and stored at −20 °C for further analysis.
Sample Preparation and Determinations
The milk samples were digested by the MARS 5 microwave digestion system (CEM Corporation, USA). One milliliter of milk sample was added into each polytef vessel, followed by 5 mL of 65% nitric acid and 2 mL 30% hydrogen peroxide. The digestion program was as follows: (1) 4 min ramp to 90 °C, hold 0 min; (2) 5 min ramp to 120 °C, hold 5 min; (3) 5 min ramp to 185 °C, hold 25 min, and 100% power (1600 W). A blank solution was prepared with 5 mL of 65% nitric acid and 2 mL of 30% hydrogen peroxide using the same digestion procedure. Both digested samples and reagent blank were diluted to 50 mL with deionized water. All digested samples were prepared in duplicate.
Instrumentation and Analysis
The quadrupole inductively coupled plasma-mass spectrometer (ICP-MS) used in this work was Agilent 7700× (Agilent, Japan), equipped with an Agilent integrated auto-sampler model (Agilent, Germany). The instrument was tuned for the optimal performance, using the tune multi-element mix solution of Li, Y, Co, Ce, and Ti (SPEX CertiPrep, USA). The sensitivity of 7Li, 89Y, and 205Ti were no less than 3000, 12,000, and 6000 counts, respectively. The level of oxide species (CeO/Ce) was below 1.5%, and doubly charged (Ce2+/Ce) was below 3%. The operating conditions are summarized in Table 1.
Method Validation
Instrumental/Method Detection Limits
In order to calculate the instrument detection limits (IDLs) and method detection limits (MDLs), the standard deviation (SD) of reagents blanks was employed. A number of 20 pool reagents blanks/digested milk (diluted with water to 50 mL) and 20 pool reagents blanks/digested milk (diluted with water to 50 mL) spiked with 0.2 μg/L of all elements were prepared and analyzed. The reagent blanks were used for the calculation of IDLs, while digested milk was used for the MDLs [5, 18].
The following formula was used:
where C is the concentration of reagent blank with 0.2 μg/L, SD is the standard deviation of blank reagent, and I is the signal intensity of the element of spike and blank reagent.
where C is the concentration of digested milk with 0.2 μg/L, SD is the standard deviation of blank milk, and I is the signal intensity of the element of spike and blank milk.
Quality Control Performance
For controlling the accuracy of the detection with the samples, the method was verified by the recovery experiments for the seven elements. The recovery (%) was performed by spiking the milk digested solutions with 0.01, 0.05, 0.1, and 0.3 mg/L, which were set in according to Chinese MRLs of Pb, As, and Cr. The recovery (%) was calculated as follows:
Risk Assessment of Toxic Elements for Children and Adult
Margin of Exposure
The margin of exposure (MOE) is the ratio of the reference point (RP) for a compound to the estimated or measured level of exposure to that compound in humans [19]. The magnitude of MOE could be used as advice to support the risk priority of management [20, 21]. The benchmark dose lower confidence limit (BMDL) was considered the most suitable appropriate reference point, which was the lower 95% confidence limit on the benchmark dose (BMD), it accommodates uncertainty in the data. Therefore, the World Health Organization (WHO) defined MOE as the ratio of the no-observed-adverse effect level (NOAEL) or benchmark dose lower confidence limit (BMDL) for the critical effect to the theoretical, predicted, or estimated exposure dose or concentration [22].
Derivation of Toxicity Benchmark Values
Inorganic arsenic (iAs) is more toxic than organic arsenic compounds [23]. Hence, in the present study, we assumed As concentration in positive samples was iAs. The Joint FAO/WHO Expert Committee on Food Additives (JECFA) identified a benchmark dose lower confidence limit of 3 μg/kg b.w./day based on an observed effect level for a 0.5% increased incidence of lung cancer (BMDL0.5) [23, 24]. Similarly, the toxicity of hexavalent chromium (Cr IV) is more than trivalent chromium (Cr III). The BMDL10 of 1 mg/kg b.w./day of Cr IV was used to estimate the risk of total Cr in raw milk [25]. For estimated daily exposure to Pb with infant and child consumers, BMDL01 of 0.5 μg/kg b.w./day for the neurodevelopmental toxicity was used. For adults, a BMDL10 dietary lead intake value of 0.63 μg/kg b.w./day for nephrotoxicity was derived [26]. The BMDL10 was used as the reference point of Cr (1 mg/kg b.w./day), Hg (0.06 mg/kg b.w./day) and Ni (0.28 mg/kg b.w./day), respectively [27, 28]. For Al, the NOAEL of 1 mg/kg b.w. per day was used for effect on neurodevelopmental toxicity [29].
Milk Consumption Data
Dietary exposures for children (ages 1–5) and adults (ages 18 or over) were estimated using the arithmetic mean concentrations of toxic elements found in raw milk. The ingestion rates for children of fluid milk as published by Child-Specific Exposure Factors Handbook of EPA [30]. For adults, 300 mL is a suitable level, which was advised by the Dietary Guidelines for Chinese Residents [31]. Children’s body weight for age and sex groups were as published by WHO [32]. And the adult’s body weight is adopted 60 kg which evaluated tolerance daily intake (TDI) by WHO [33].
Analysis and Statistical Methods
Contamination Index Method
Single-factor index method was used to reflect the contamination of single element. It used the actual pollution level compared with the maximum residue limit. Nemerow multifactor index method, combined with the maximum and the average contamination index, was used to reflect the comprehensive pollution levels. The MRLs of Pb of 0.05 mg/kg, Cr of 0.3 mg/kg, Hg of 0.01 mg/kg, As of 0.1 mg/kg [10], Ni of 0.1 mg/kg, and Al of 0.2 mg/L [34], are used as reference values to calculate the single-factor index and the Nemerow multifactor index. These two indexes were used to compare the region’s pollutions and to distinguish the differences of the milk contamination levels of the three types of milk stations.
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1.
Single-factor index method
Single-factor index method was compared the measured value and the limited value.
where P i is single-factor index, C i is measured value, and S i is limited value.
-
2.
Nemerow multifactor index method
Nemerow multifactor index method was a comprehensive assessment method that combined the maximum single factor index and the average single factor index.
where P is the nemerow multifactor index, (C i /S i )max is the maximum single factor index, and (C i /S i)ave. is the average single-factor index.
Box and whisker plot was used to estimate the level of outlier degree by the SPSS Statistics Software Version 20 (IBM, New York, USA). Highly significant correlation (p < 0.01), significant correlation (p < 0.05), and not significant correlation were analyzed by one-way ANOVA.
Results and Discussion
Detection of Toxic Elements in Samples
The overall performance of the method and the levels of As, Pb, Cr, Cd, Hg, Al, and Ni in 178 raw milk samples are summarized in Table 2. The New Zealand National Chemical Contaminants Programme (NCCP) has an IDL of 10, 5, 10, and 2 μg/L for As, Hg, Pb, and Cd, respectively. The present method could detect as low as 0.1 μg/L for As, 0.05 μg/L for Hg, 0.01 μg/L for Pb, and 0.01 μg/L for Cd, respectively. The recoveries were between 82.9 and 108.4% which were in accordance to an acceptance limits between 80 and 110% set by the standard of GB/T 27404-2008 [35]. A relatively high detection rate of 47.8% was shown for Al, with the residue level range between 10.81 and 1517.67 μg/L. The detection rates were 29.2, 28.1, and 23.6% for Pb, Hg, and Ni, respectively, with the concentration ranges of 2.01–33.37, 1.02–7.57, and 3.03–68.61 μg/L, respectively. The detection rates were 12.4 and 9.0% for Cr and As, respectively, with concentration ranges of 8.01–84.66 and 1.03–2.30 μg/L. The Cd was not detected in all samples.
A comparison of toxic elements concentrations in raw milk with those reported by many authors is shown in Table 3. The detected concentrations of Al (10.81 ~ 1519.67 μg/L), Cd (lower than detection limit), Ni (3.03 ~ 68.61 μg/L) in this study were lower than those reported in literatures [4, 13, 18, 36, 37]. In all survey of these studies, the concentration of Al in milk is relatively higher than other elements. Al occurs naturally in the environment and is also released due to anthropogenic activities such as mining and industrial uses, in the production of Al metal and other Al compounds [29]. Most unprocessed foods typically contain less than 5 mg/kg [29]. The As and Cr levels were lower than that reported by Herwig N. et al. [38]. The detected concentration of Hg was lower than that reported by Bilandzic N. et al. [36]. The mean concentrations of Pb (8.50 ± 7.42 μg/L) in this study were lower than that reported by Kazi et al. and Bilandzic et al. [4, 36], while higher than that reported by Licata et al. and Sola-Laranaga et al. [1, 18]. Pb is always found in milk not only in great industrial area. It exist in environment normally, the contamination of fodder and water were all the reasons to influence the levels in raw milk [1].
The detected concentrations of Pb, Cr, Hg, and As in the milk samples were all below China’s regulated limits (Pb of 0.05 mg/kg, Cr of 0.3 mg/kg, Hg of 0.01 mg/kg, and As of 0.1 mg/kg) [10].
Toxic Element Pollution Analysis
Table 4 shows the levels of toxic elements in the raw bovine milk and the contamination indexes of eight provinces. As and Pb were not detected in the samples from Tianjin and Inner Mongolia. Anhui showed higher As pollution with the maximum (2.30 μg/L) and mean value (1.42 ± 0.44 μg/L). The numbers of detected samples of As and Pb in Anhui were more than that of the other provinces. Pb level was the highest in the samples from Heilongjiang province, with the maximum level of 33.37 μg/L and the mean values of 18.24 ± 12.28 μg/L. In accordance to the single-factor index for Pb, Heilongjiang was the most polluted, followed by Hebei and Shanxi. Cr level was the highest in the samples form Anhui province, with the maximum levels of 84.66 μg/L and the mean values of 60.23 ± 24.55 μg/L, while Cr was not detected in the samples from Hebei province. The single-factor index of Cr indicated that Anhui was the most polluted, followed by Heilongjiang and Sichuan. Hg level was the highest in the samples form Shanxi province with the level of 3.20 ± 3.00 μg/L and the lowest in the samples from Tianjin province, with the level of 1.38 ± 0.01 μg/L. Correspondingly, Shanxi province showed the highest-single factor index value (0.320) and Tianjin showed the lowest single-factor index value (0.138). The highest Al level of 1519.00 μg/L was found in Shanxi’s samples, whereas the highest mean value of 763.00 ± 957.42 μg/L and the highest-single factor index value of 3.815 were found for Heilongjiang’s samples. The Ni residue was not detected in the samples from Tianjin and Inner Mongolia. There was only one sample that detected Ni but with the highest level of 68.61 μg/L in Shanxi. The sample numbers with detected Ni was more in Sichuan than the others. Taken together, As, Pb and Ni were not detected in the samples from Tianjin and Inner Mongolia, Cr was not detected in the samples from Hebei.
In accordance to the Nemerow multifactor index, the samples from Heilongjiang were most polluted, and Shandong, followed by Shanxi and Anhui. The toxic element accumulations are significantly related to the degree of soil ingestion during grazing. One of the most important source is water, which could transfer through food chain to animals [4, 39, 40]. The raw milk samples with high levels of toxic elements were found in industrial areas, such as Heilongjiang and Shanxi. These results could provide the references for regulators to control toxic element residues pollution in industrial areas.
The maximum, mean, minimum, and contamination index method was used to analyze region differences and make comparison of the element levels in detected samples from different province. The Environmental Protection Agency (EPA) established the contamination factor index method for water pollution assessment [41]. Yu used the contamination index method and evaluated toxic element levels in the raw milk samples from different regions and milk stations [42].
Six toxic element levels were detected in the milk samples, from large-scale farms, small farm cooperatives, and milk-processing plants and are shown in Table 5. Cd was undetected in the milk samples. The detection rates of As, Pb, Cr, and Ni were higher in the milk samples from large-scale farms than small farm cooperatives and milk-processing plants. The relative high detection rates of Hg and Al were shown in the samples from dairy cooperative. The lowest detection rates of all six elements were found in the milk-processing plants. The Nemerow multifactor index analysis showed that milk-processing plants were the lowest and large-scale farms were the highest.
There are three main types of milk stations, large-scale farms, small farm cooperatives, and milk-processing plants, in China [43]. The management mode of milk-processing plant is dairy products enterprise, and the large-scale farm is private owner. The small farm cooperative’s management mode is the combination of milk producers. This result could be related to good manufacturing practices operated by the professionals in the milk processing plants. This measure could control the residue contaminations effectively. Significant difference existed among three milk stations in the Cr levels. The detectable mean value was higher (74.17 ± 10.13 μg/L) in the samples, from dairy company farms than that (25.49 ± 17.77 and 31.09 ± 20.67 μg/L) from other two. There was no significant difference in As, Pb, Hg, Al, and Ni levels among three types of milk stations.
Estimation of Daily Intake of Toxic Elements with Children and Adult
The average of milk exposure concentration for As, Pb, Cr, Hg, Al, and Ni is 1.35, 8.50, 34.58, 2.31, 284.16, and 10.78 μg/L, respectively. Based on the exposure mean concentration, the MOE of toxic elements for male and female children from age 1 to 5 and adults are listed in Table 6. Because the element of Cd was not detectable, Cd was not considered as a risk factor. The value of MOE is not a precise quantification of risk, but it should be a support prioritization of risk management action. The magnitude of MOE is large, on communication of a low level of human health concern [3, 21]. Based on the data of Table 6, the values of MOE for children were smaller than adults and showed an increasing trend between the ages from 1 to 5. The contribution of the differences to children and adult is revealed by their consumption of dairy products, with level for infant group greater than older infant and young children group. In addition, children generally have higher food intake than adults when expressed on a body weight basis, and therefore represent the group with the higher potential exposure [29]. By the same token, the MOE values for male children showed a lower level of health concern than male children.
Children and adult have a lower MOE of Pb, when compared to the other toxic elements. Because the reference point of BMDL01 (0.5 μg/kg b.w./day) and BMDL10 (0.63 μg/kg b.w./day) is lower than the other, that concerning the sensibility of neurotoxicity in infant, children, and adult health [27]. In adults, the lead-associated neurotoxicity was found to affect central information processing and short-term verbal memory, to cause psychiatric symptoms and to impair manual dexterity. The developing brain is more vulnerable to the neurotoxicity of lead than the mature brain [27]. Therefore, the risk of Pb for infant and young children was more serious than adult. The MOE value of As is higher than Pb, but lower than the other elements. For children, the MOE estimations of exposure to iAs were, in general, 4–10 times higher than adult. Though the value of MOE, the potential toxic element exposures are displayed as an arrangement of Pb > As > Ni > Hg > Cr > Al. Although Al shows a relatively high level, the MOE value display a large value, compared with the other elements for more safety. Pb should pay more attention than the other toxic elements, which is the reason why EU and CAC only set the maximum residue limit for Pb [9, 11].
Chen et al. used MOE method to evaluate potential exposure of estrogens in milk products and Benford et al. calculated MOE of 12 genotoxic and carcinogenic chemicals in food and estimated of human dietary exposure [3, 21]. The combined MOE is determined by taking the reciprocal of the sum of individual MOEs, compared with a threshold value to concern the acceptability of potential exposure risk [19]. However, there is no certain threshold value of infant and child with exposure of toxic elements; therefore, the MOE in this analysis is used to support prioritization of risk management action on communication of a low level of human health concern if the MOE is large [21].
Conclusion
In this study, the seven toxic elements were determined by ICP-MS. The raw bovine milk samples with relative high toxic metal levels were found from provinces with the heavy industry; special attention should be paid to industrial areas. The levels of toxic elements in raw milk from milk-processing plants were lower than large-scale farms and small-farm cooperatives. Management practices associated with the levels of toxic element, suggesting targeted supervision needs to reduce the toxic element levels.
In conclusion, the toxic element levels were all below Chinese MRLs. The MOE result of toxic elements in these milk samples are large; thus, the consumption of milk does not present a problem for adult and children health. But Pb should be paid more attention to than the other toxic elements in milk, especially for infant and child consumers.
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This study was supported by special fund for agro-scientific research in the public interest (201403071), The Agriculture Science and Technology Innovation Program (ASTIP-IAS12).
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Qu, XY., Zheng, N., Zhou, XW. et al. Analysis and Risk Assessment of Seven Toxic Element Residues in Raw Bovine Milk in China. Biol Trace Elem Res 183, 92–101 (2018). https://doi.org/10.1007/s12011-017-1116-x
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DOI: https://doi.org/10.1007/s12011-017-1116-x