Health Risk Assessment of Heavy Metal in Moso Bamboo Shoots from Farm Markets, China

Abstract

The contents of 6 kinds of heavy metals (Pb, Cr, Cd, As, Cu, Ni) in moso bamboo shoot were measured by inductively coupled plasma-mass spectroscopy (ICP-MS). The health risk of the 6 kinds of heavy metals was assessed by the target hazard quotients (THQ). The mean contents of Pb, Cr, Cd, As, Cu and Ni in all analyzed bamboo shoots were 6.19 ∼ 92.8, 1.38 ∼ 137, 1.22 ∼ 35.5, 1.14 ∼ 7.48, 224 ∼ 1266 and 31.4 ∼ 381 µg kg⁻¹, respectively. The contents of these heavy metals in all samples were below the corresponding maximum limits established by Ministry of Health P. R China. It is observed that each heavy metal THQ value was below 1.0. The TTHQs of the heavy metals for adults and children were 0.116 ∼ 0.152 and 0.165 ∼ 0.216, the results indicate that the ingestion of moso bamboo shoots will not bring risks to residents.

Introduction

Bamboo shoots are the edible shoots emerging from the rhizome of bamboo. The moso bamboo (Phyllostachys heterocycla cv. Pubescens) are the most widely planted bamboo species with the highest economic and ecological benefit in China. The moso bamboo shoots are usually harvested in two seasons, winter and spring, and are called winter bamboo shoots and spring bamboo shoots, respectively (Choudhury et al., 2012). Nowadays, moso bamboo shoots have become an essential part of daily diet in many areas of China, and are also exported to other countries in large quantities. As a vegetable, it is rich in nutrients, such as proteins, minerals, vitamins, phenols, phytosterols and dietary fibres (Nirmala et al., 2014; Singhal et al., 2013). Bamboo shoots have also been regarded as a traditional Chinese medicinal material for more than 2000 years (Chongtham et al., 2011).

In recent decades, food safety has been a constant concern worldwide (Toth et al., 2016). One of the greatest threats to food safety may be the heavy metal pollution due to mineral exploitation and abuse of pesticides and chemical fertilizers (Lu et al., 2015). Heavy metals, including lead (Pb), chromium (Cr), cadmium (Cd) and arsenic (As), which has been shown to be harmful to human body (Li et al., 2014; Zeng, et al., 2015). Heavy metal contamination of bamboo shoots may occur during process of growth. As previously reported, the concentrations of total arsenic in bamboo shoots ranged from 27.7 to 94.0 µg kg⁻¹ (dry weight), of which As (III) presented 10.1% to 35.9% (Zhao et al., 2006). The values of Pb, Cd, Zn, Cr, Cu and Mn in rhizomes of moso bamboo shoots were 0.262, 0.024, 3.592, 0.038, 0.567 and 2.751 mg kg⁻¹, respectively (Yan et al., 2015). A survey on consumer's perception of vegetable safety indicated that people tend to be more concerned about “freshness”, “pesticide residues” and “heavy metal contamination” (Cheng et al., 2016). So, it is important to evaluate the bamboo shoots' health risks level to ensure the food safety and rebuild consumers' trusts with it.

Health risk assessment is the process to estimate the probability of harmful effects on human health resulting from exposure to chemicals in contaminated environmental media. The non-carcinogenic effects of heavy metals can be estimated by Target Hazard Quotient (THQ), which on the basis of relationship between exposure and effects time, exposure frequency, and levels (USEPA 2007). This method has been widely used to assess the health risk of food consumption. (Ahmed et al., 2015; Alipour et al., 2015; Fu et al., 2014; Li et al., 2015; Shaheen et al., 2016). However, there is little research about the heavy metal contents and health risk of edible moso bamboo shoots. Winter bamboo shoots and spring bamboo shoots are the most widely consumed bamboo species in China. The aim of the present study was to measure the concentration of Pb, Cr, Cd, As, Cu, Ni and evaluate the health risks level in winter bamboo shoots and spring bamboo shoots from the farm market.

Materials and Methods

(1)Sample collection    Thirty-two samples were collected from farm markets in Zhejiang and Jiangxi province, one of the largest bamboo shoots producing areas in China. Sixteen winter bamboo shoots (WBS) samples were collected in January 2016, eight samples were collected from each province. Sixteen spring bamboo shoots (SBS) were collected in March 2016, eight samples were collected from each province. The fresh moso bamboo shoots samples were manually removed from the shell and the lower edges, the edible portion was ground, placed in polyethylene bottles, and stored at −18°C prior to analysis.

(2)Reagents, standards and apparatus    Hydrogen peroxide (Guaranteed reagent, 30%, Guanghua Sci-Tech, Tianjin) and nitric acid (Trace metal grade, 69%, Fisher, Canada) were used to digest the moso bamboo shoot samples. The samples were first digested using a Mars 6 microwave system (CEM, Matthews, NC, USA). Deionized water used in this study was generated with a Milli-Q system (Millipore, Bedford, MA, USA). Multielement standard solutions containing 100 mg L⁻¹ of each element (Pb, Cd, Cr, As and Cu) were supplied by the National Analysis Center of Iron and Steel (NCS, Beijing, China). A certified reference material (CRM Rice, GBW10045, National Research Center for Certified Reference Materials, Beijing, China) was used to verify the accuracy of the results. The heavy metal content was measured by ICP-MS instrument (NexIon 300D, Perkin Elmer, Shelton, CT, USA). Ultra-pure grade argon (99.999% pure) was used as the carrier gas.

(3)Sample preparation and digestion    Approximately 1.0 g ground sample was weighed and 5 mL of nitric acid was added into a Teflon tube. Samples were pre-digested at 160°C for 20 mins. After cooling, 2 mL hydrogen peroxide was added, and the teflon tubes were transferred into the Mars 6 microwave system. The temperature was increased to 130°C in 5 min, and after 10 min the temperature increased to 180°C in 5 min and was held for 30 min. After cooling, the solution was transferred in a Teflon beaker, which was then heated at 200°C to remove hydrogen peroxide and nitric acid, then carefully diluted to 25 mL in polypropylene tubes. Each sample was analyzed in triplicate, and one blank and one reference material was added as controls on each batch.

(4)ICP-MS analysis    The parameters of the ICP-MS are shown in Table 1. Dynamic reaction cell (DRC) mode with ammonia gas (NH₃) was used to eliminate the potential mass interference from ArC to Cr. A solution containing 1 µg L⁻¹ Li, Be, Mg, Fe, In, Ce, Pb, U was used to optimize the instrumental parameters before sample measurement by ICP-MS. According to the performance of ICP-MS instrument and concentration levels in bamboo shoots, the linearity range was found to be 0.1 ∼ 10 µg L⁻¹ for Pb, Cd, Cr and As, and 1.0 ∼ 100 µg L⁻¹ for Cu and Ni.

Table 1. Operation parameters of ICP-MS (NexIon 300D)

Parameters	Setting parameters
RF power	1100 W
Nebulizer (carrier gas) flow rate	0.98 L min−1
Coolant gas flow	15 L min−1
Sweeps	20
reading	1
Number of replicates	3
Scanning mode	Peak hopping
Sampling cone orifice (Ni)	1.2 mm
Skimmer cone orifice (Ni)	1.0 mm
DRC gas flow (NH3)	0.6 mL min−1
Isotopes of selected	52Cr+, 60Ni+, 63Cu+, 75As+, 111Cd+ and 208Pb+

(5)Quality control    The limits of detection (LOD) were defined as 3 times the standard deviations of the 10 consecutive measurements from the independent digestion blank. The precision of the method, expressed as the relative standard deviation (RSD, %) at 1 µg L⁻¹ concentration level for the Pb, Cd, Cr and As and 10 µg L⁻¹ Cu and Ni were all <3%. A certified reference material (CRM rice, GBW10045) was analyzed to ensure accuracy of the ICP-MS procedure. The results were in good agreement with the reference values. The limits of detection and contents of certified reference material is shown in Table 2.

Table 2. The limits of detection and concentrations of certified reference material (GBW10045) (mg kg⁻¹)

Element	The limits of detection	Reference value	Found value
Pb	0.005	0.070±0.023	0.061±0.003
Cr	0.01	(0.14)	0.12±0.02
Cd	0.005	0.19±0.02	0.21±0.02
As	0.002	0.11±0.02	0.11±0.01
Cu	0.006	2.4±0.2	2.2±0.1
Ni	0.01	0.31±0.04	0.29±0.02

(6)Human health risk assessment    The individual heavy metal health risk of consumption of food can be assessed by Target hazard quotient (THQ). The estimated daily intake (EDI) of heavy metal is an essential part of health risk assessment. The THQ was calculated as:   

Where F_IR is the food ingestion rate (g person⁻¹ day⁻¹, fresh weight, 150 and 100 g day⁻¹ for adults and children, respectively); E_D is the exposure duration (70 years); E_F is the exposure frequency (365 day year⁻¹); C_f is the heavy metal concentration in bamboo shoots (µg kg⁻¹); W_AB is the average body weight (61.8 kg for adults, 28.9 kg for children); T_A is the average exposure time(365 days × 70 years) (Zheng et al., 2007); RfDo is the oral reference dose, and the RfDo values of Pb, Cr, Cd, As, Cu and Ni are set to be 3.6, 1500, 1, 0.3, 40 and 20 µg kg⁻¹ d⁻¹, respectively (JECFA, 2003; USEPA, 2015).

Results and Discussion

(1)The content of heavy metal in moso bamboo shoots    The results of Pb, Cr, Cd, As, Cu, Ni in bamboo shoots from different farm markets are shown in Table 3. The contents of each metal in bamboo shoots from various farm markets decreased in the order of Cu > Ni > Cr > Pb > Cd > As. The contents of Pb, Cr, Cd, As, Cu, Ni in all analyzed bamboo shoots varied widely, indicating remarkable differences of the source of products (Su et al., 2013). The contents of Cr had the highest coefficient of variation (CV) in measured elements, while Cu had the lowest CV in measured elements. For Pb, Cr, Cd and As, there were no significant difference (p > 0.05) between spring moso bamboo shoots and winter moso bamboo shoots. The contents of Cu and Ni in two species of bamboo shoots were significantly different (p < 0.01). The maximum limits of Pb, Cr, Cd, As for bamboo shoots established by Ministry of Health P.R. China (Standards, 2012) was 200, 500, 50 and 500 µg/kg, respectively. The concentrations of these heavy metals in all samples were below the corresponding maximum limits, while for Cu and Ni, the maximum limits standard in bamboo shoots have not yet been established in China.

Table 3. Heavy metal contents (µg kg⁻¹) in spring bamboo shoots (SBS) and winter bamboo shoots (WBS)

Samples		Pb	Cr	Cd	As	Cu	Ni
SBS (n=16)	Mean ± SD	29.7±19.6	41.6±47.8	11.7±5.01	2.84±1.74	915±210	204±110
	Range	6.19∼92.8	1.38∼137	4.16∼21.0	1.14∼7.48	578∼1266	63.0∼381
	CV	66.0%	115%	42.9%	61.1%	23.0%	54.0%
WBS (n=16)	Mean ± SD	27.6±11.6	31.4±24.5	14.1±12.8	2.77±1.13	481±159	92.0±52.9
	Range	14.7∼50.8	8.61∼103	1.22∼35.5	1.66∼6.12	224∼691	31.4∼188
	CV	42.2%	78.0%	90.8%	40.9%	33.1%	57.5%
All samples (n=32)	Mean ± SD	28.7±15.9	36.5±37.7	12.9±9.63	2.81±1.44	698±287	148±102
	Range	6.19∼92.8	1.38∼137	1.22∼35.5	1.14∼7.48	224∼1266	31.4∼381
	CV	55.5%	103%	74.8%	51.4%	41.1%	69.1%

(2)The content of heavy metal in bamboo shoots compared with previous studies    The content of heavy metals in this study were comparable to previous studies (Table 4). The content of Cr, Cd ranges were reported to be 17.0 to 312.0 µg kg⁻¹ and 1.00 to 50.0 µg kg⁻¹ (Yan et al., 2015), which covered the values measured in this study. Average Cu content in winter bamboo shoots was similar to the result reported by Yan et al. (Yan et al., 2015). The content of Pb, Cr, Cd and As were reported to be 64.63, 158.5, 10.27 and 12.69 in Shaoxing (Feng, 2015). While, the Pb value in bamboo shoots around lead-zinc mine in Quzhou, southeastern China was reported to be within 1.00 ∼ 561.0 µg kg⁻¹ (Yan et al., 2015), which was much higher than that in this study. Similar results were observed in Dendrocalamus asper (D.asper) and Dendrocalamus giganteus (D. giganteus) samples, which were collected from India (Nirmala et al., 2007).

Table 4. Previous studies on heavy metal contents (µg kg⁻¹) in bamboo shoots

Species	Pb	Cr	Cd	As	Cu	Ni	Site	Source
P. Pubescensa	28.7	36.5	12.9	2.81	698	148	Zhejiang, Jiangxic	Present study
P. Pubescens	64.63	158.5	10.27	12.69	—	—	Shaoxing	(Feng, 2015)
P. Pubescens	262	38	24	—	567	—	Quzhou	(Yan et al., 2015)
P. Pubescens	178	44	19	—	1961	—	Quzhouc	(Yan et al., 2015)
D. asperb	33.2	—	49.2	—	32	106	Chandigarh	(Nirmala et al., 2007)
D. giganteusb	50.2	—	35.4	—	56	122	Chandigarh	(Nirmala et al., 2007)

^a  Phyllostachys heterocycla cv. Pubescens (P. Pubescens) samples were collected from China.

^b  Dendrocalamus asper (D.asper) and Dendrocalamus giganteus (D. giganteus) samples were collected from India.

^c  Those samples were collected from local farm markets.

(3)Human potential health risk of individual heavy metals    The human potential health risk of individual heavy metal can be expressed by THQ. If the value of THQ is smaller than 1.00, it indicates no obvious risk. The potential health risks of heavy metals for adults and children were considered separately because of their differences in body weight and dietary composition. The detailed data of individual heavy metal THQ and total heavy metal THQ (TTHQ) through consumption of bamboo shoots for both adults and children are listed in Table 5. The THQ of each metal decreased in the order of Cu > Cd > As > Pb > Ni > Cr, and all the THQ values were below 1.00, indicating that people would not experience any obvious risk. It's worth noting that THQ of individual heavy metal for children was higher than that of adults, and similar results were also found in vegetables and seafood from China and Turkey, respectively (Ozden and Erkan, 2016; Zheng et al., 2007).

Table 5. Health risk of heavy metals (THQ) for different residents through consumption of bamboo shoots

Heavy metal	Residents	THQ
		WBS	SBS	All Samples
Pb	Adults	1.86×10−2	2.01×10−2	1.93×10−2
	Child	2.65×10−2	2.86×10−2	2.75×10−2
Cr	Adults	5.08×10−5	6.72×10−5	5.90×10−5
	Child	7.24×10−5	9.59×10−5	8.41×10−5
Cd	Adults	3.42×10−2	2.83×10−2	3.13×10−2
	Child	4.87×10−2	4.04×10−2	4.46×10−2
As	Adults	2.24×10−2	2.30×10−2	2.27×10−2
	Child	3.19×10−2	3.28×10−2	3.24×10−2
Cu	Adults	2.92×10−2	5.55×10−2	4.23×10−2
	Child	4.16×10−2	7.91×10−2	6.04×10−2
Ni	Adults	1.12×10−2	2.48×10−2	1.80×10−2
	Child	1.59×10−2	3.53×10−2	2.56×10−2
TTHQ	Adults	0.116	0.152	0.134
	Child	0.165	0.216	0.191

The THQ of Cr was the lowest, and it should be associated with its low content and high RfDo (oral reference dose). It should be noted that the THQ of Cr was calculated according to Cr³⁺, for its low toxicity, and the potential health risks were also negligible in fruits and vegetables as reported by Shaheen et. al. (Shaheen et al., 2016). The THQ of Cu was the highest, and the mean value of all bamboo shoots reached 4.23×10⁻² and 6.04×10⁻² for adults and children, respectively. Although copper is an essential element for humans, large and acute doses can be harmful (Kafaoglu et al., 2016). Although Pb, Cd and As have higher toxicity than the rest of measured metals, the results suggested that the consumption of bamboo shoots should not result in significant health risks derived from those toxic substances.

(4)Human potential health risk of multi-heavy metals (TTHQ)    Actually, a variety of toxic heavy metals exist in foodstuffs, and the synergistic or antagonistic effects between the various metals would increase or decrease the health risk (Muthusamy et al., 2016; Zeng et al., 2015). In present research, the potential health risk of multi-heavy metal was evaluated by the total THQ (TTHQ) , the calculation formula is as follows:

  

As shown in Table 5, the TTHQ of spring moso bamboo shoots was higher than winter moso bamboo shoots. The difference in essence of spring shoots and winter shoots is insignificant, but spring shoots have as longer growth period. The TTHQs of these heavy metals for adults and children were 0.116 ∼ 0.152 and 0.165 ∼ 0.216, respectively. Neither children nor adults are under the risk of heavy metals. As shown in Figure 1, Cu has contributed up to 31.6% of TTHQ, followed by Cd, As, Pb and Ni, while Cr contributes little to the potential health risk value.

Fig. 1.

Health risk of heavy metals (THQ) for different residents through consumption of bamboo shoots

The TTHQs have been reported to assess the multi-heavy metal health risk on various kinds of foodstuff. The TTHQs of the toxic metals (Hg, Cd, Pb and As) through the consumption of different fish and shellfish ranged from 0.09 ∼ 0.95 (Ozden & Erkan, 2016). The TTHQs of heavy metals (As, Cd, Pb, Cr, Mn, Ni, Cu and Zn) from consuming fruits and vegetables were ranged from 0.078 ∼ 0.418 and 0.084 ∼ 1.194 (Shaheen et al., 2016). Moreover, the TTHQs (Cd, As, Pb, Cr, Ni, Zn, Se, Cu, Mo, Mn, Sb, Ba, V, Ag) of rice and wheat from Bangladesh were reported to be 10.548 and 0.601. The health risk of arsenic even reached 7.419 (Ahmed etal., 2015). By comparison, the results of this study showed that the average TTHQ of bamboo shoots was generally lower than that of fish, shellfish, vegetables, rice and wheat.

Conclusion

This study assessed the health risk of 6 heavy metals (Pb, Cr, Cd, As, Cu, Ni) in moso bamboo shoots from Zhejiang and Jiangxi farm markets in China. The content of Pb, Cr, Cd, As, Cu, Ni in all analyzed bamboo shoots were 6.19 ∼ 92.8, 1.38 ∼ 137, 1.22 ∼ 35.5, 1.14 ∼ 7.48, 224 ∼ 1266, 31.4 ∼ 381 µg kg⁻¹, respectively. The content of these heavy metals in all samples were below the corresponding maximum limits established by Ministry of Health P.R. China. The THQ value of each heavy metal was below 1.00, and the TTHQs of the 6 heavy metals for adults and children were 0.116 ∼ 0.152 and 0.165 ∼ 0.216, which indicated that the ingestion of moso bamboo shoots will not pose health risks to consumers.

Acknowledgements    This work was supported by The Fundamental Research Funds for Centra Public-interest Scientific Institution (CAFYBB2017SZ002).

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