Title Metal contamination in low-cost jewelry and toys in Cambodia

Background
The existence of lead-contaminated consumer products is a global issue. Toys and low-cost jewelry may contain toxic metals and Cambodia is known to have consumer products with toxic metals.


Objectives
It is important to inform Cambodians about sources of toxic metals so that they can reduce their exposure risk, particularly for children.


Methods
Student volunteers purchased, or brought from home, low-cost jewelry and toys to either the University of Health Science or a Don Bosco Institute in Phnom Penh, Cambodia, where they were analyzed using X-ray fluorescence (XRF). The initial analysis was performed in 2011. A subset of the 2011 samples was re-analyzed in 2015 using new preparation techniques and a new x-ray fluorescence (XRF) unit.


Discussion
The analysis of low-cost jewelry in Phnom Penh in 2015 indicated that lead in jewelry clasps is a more serious health concern than was first perceived in 2011. Mercury, nickel, cadmium and copper were also found in toys, and occasionally these toys had been produced by well-known companies. Sources of jewelry production of samples in the present study are unknown. Lead in clasps in low-cost jewelry appeared to be the greatest risk to children in our sampling.


Conclusion
One-third of toys and low-cost jewelry exceeded the United States and European Union guidelines for heavy metals. XRF analysis allows for rapid screening of lead and other toxic metals and could be used to reduce the sales of low-cost jewelry and toys containing toxic metals.


Introduction
Cambodia imports most of its consumer products from nearby countries and the rate of economic growth of Cambodia has produced a high demand for consumer products. 1his influx of consumer products requires a more rapid, effective system of quality control.Consumer products that are imported and sold in Cambodia can contain chemical contaminants that pose serious adverse health effects to consumers. Ninety percent of the enamel paints sampled in Cambodia exceeded a voluntary standard of 100 μg/g lead (Pb) of the producing country, Thailand. 4The problem is not limited to Cambodia, as studies in the US, India, and China have found elevated Pb in children's toys, low-cost jewelry, and paints. 5,6,7 Sources of metals used to make low-cost jewelry include recycling facilities for lead acid batteries and electronic wastes. 5,9,10Such recycled metals lower the cost of manufacturing and imitate shiny, better quality jewelry.
Blood lead levels (BLL) as low as 3 µg/dl were associated with neurobehavioral deficits in visual Zinc motor integration, attention, reaction time and off-task behaviors. 16Bellinger 17 found that adverse outcomes such as reduced IQ performance and academic deficits occurred at BLL <10 µg/dl, and at prolonged exposure there was association with attention deficit hyperactivity disorder (ADHD).Similarly, children aged 2 through 5 years had an 18-point increase in the Total Behavior Problem Score (TBPS) if their BLLs were higher than >15 µg/dL. 18

Lead in Inexpensive Jewelry
In the United States, there are at least 4 million households with children who have been exposed to Pb, and approximately half a million US children one to five years old with BLLs above 5 µg/dL. 19Recognizing that Pb exposure can affect every system in the body, the United States (US) Centers for Disease Control and Prevention (CDC) initiated a Childhood Lead Poisoning Prevention Program which is committed to eliminating BLLs > 10 µg/dL by 2020. 19owever, despite efforts to eliminate Pb exposure in children, there have been numerous cases reported in which workers and children have been the victims of Pb exposure.One of the lead exposure pathways is low-cost jewelry items, which are imported into the US from developing countries such as China. 6study conducted by Weidenhamer and Clement 6 found that 77 out of 130 inexpensive jewelry samples imported from China to the US exceeded the former United States Consumer Product Safety Commission (USCPSC) guideline of 0.06% (600 µg/g). 20Moreover, out of 311 inexpensive jewelry samples purchased, Maas et al. 21found more than 50% of samples contained more than 3.0% Pb in at least one portion of the jewelry piece, while 39.5% of the samples contained more than 50% Pb and 29.2% contained more than 75% Pb.
The above findings were highlighted by the death of a four-year old child in Minnesota after ingesting a charm composed of 99.0%Pb and stress the need to improve monitoring and regulation of imported Pb-containing products in the US. 22In 2011, the Consumer Product Safety Commission (CSPC) 23 issued a recall of 150 million pieces of metallic toy jewelry due to concerns over Pb levels.
A similar, serious incident was reported in 2009 when an Americanborn child of Cambodia-born parents was found to have been wearing an amulet obtained from a monk in Cambodia that contained more than 45% Pb.The level of Pb in his blood was 20 µg/dL. 24Subsequently, the CDC 24 advised parents who had traveled to foreign countries and may have had their children wearing amulets or inexpensive jewelry items obtained from these countries to register for a BLL test out of concern over potential Pb contamination.
A recent analysis of low-cost jewelry in China found items with 65% Pb, 71% copper (Cu) and 37% cadmium (Cd), and 3-7 other samples had high levels of metals. 25A survey in Seattle of children's jewelry in 2015 indicated that lead was still present in 23% of samples; the highest Pb concentration of 50,100 µg/g was lower than found in some earlier surveys, probably reflecting improved monitoring and management. 26

Lead in Plastic Toys
In plastic toys, Pb is used as a pigment for color or as a stabilizer to provide rigidity and high heat stability. 9Toys are an integral of part of a child's development. 10Children with their hand-to-mouth habits can chip off parts of the surface of the contaminated toy, or leach the toxic element in their mouths.Because  Prior to and after the analysis, jewelry pieces were kept in plastic bags to prevent cross contamination.
Because the jewelry pieces were different from one another in terms of length, composition and style, the jewelry part analyzed varied from one sample to another.Because we were concerned the jewelry clasps might be richer in lead (soft and dense) than the XRF results indicated, the 2011 clasps were stored for further analysis.In 2015, prior to XRF analysis, the clasps were flattened with a hammer into disks 7 mm to 10 mm in diameter.Subsequently, they were analyzed using the new model XRF in Cambodia and in Bangkok, using the "small spot" unit.

Lead Concentration in Toys
Seventy-one children's toys were purchased by students from local markets, and some by the senior author in Thailand.After the toys were tested on Plastic or General Metals mode for 30 seconds, they were kept in plastic bags in the laboratory or returned to the donor.All were collected in 2011.

Lead Concentration in Low-cost Jewelry
Of the 89 jewelry pieces tested, 35% failed the EU guidelines for heavy metals.Of these, 18% were found with more than 160 µg/g Pb, the EU guideline for lead in scraped-off materials.Of concern is that 11% of these 88 samples contained 100 times the EU guidelines for lead. 31hese results, presented in Table 3, illustrate the lead content as measured directly with the Niton XL3T970 in 2015.In 2011, the concentration of lead measured with a XRF XL3t in the same 10 jewelry clasps was significantly less (Figure 1).It appears that the older analyzer was not as accurate in measuring small pieces, i.e. 4 mm in diameter or 10 mm by 4 mm.Furthermore, the analysis showed higher Pb levels in the clasps when they were flattened into a thin sheet and measured with the Niton XL3T970 in 2015 (Figure 1).2, a relatively strong relationship between the lead and copper content of the clasps can be seen.The three outlying data points in Figure 2 are samples with about 40% nickel, which is considerably higher than the other clasps.These three outlying data points pull the line down from the rest of the data set.Excluding these outliers is one option, but an equivalent response is formed when the copper and nickel content are combined and plotted against the lead content, showing a strong relationship (r 2 =.994) (Figure 3).When the clasps were flattened, sometimes the sides of the clasp looked quite different, with one side being much richer in lead and containing less copper and nickel.One flattened clasp was very different, with the lead content of one side at 39.3% and the other at 83%.Because of the high metal content, the analytical error was small.Prior to flattening, the 10 clasps processed in 2015 in triplicate had an average relative standard deviation of 10.2%.Further analysis supported this interpretation.We used another Niton XRF analyzer with "small spot" capability that can measure pieces 3 mm in diameter.For three jewelry clasps, in the "small spot" analysis, the lead content of the initial analysis and the flattened clasp was 61.9±26.9% and 84.0±5.3%, respectively.It is not possible to compare the results of the earlier analysis in 2015 to the "small spot" analysis, as flattening the clasp is a oneway destructive process.Furthermore, flattening removes any uncertainty about small size weakening the analysis.
Lead most commonly seriously exceeded the EU guidelines, but Ni, Cu, Cd and antimony (Sb) also commonly exceeded the EU guidelines (13% to 18% of samples).Only zinc and chromium did not exceed the guidelines.

Metal Contamination in Toys
Out of 71 toy samples tested, four toys (6%) contained more than 100-fold the EU Hg guideline, i.e. >1% Hg, and 26% of toys failed the EU guidelines due to mercury.In two toy cars, the mercurycontaining paint (1-2%) readily chipped off (Figure 4).Nickel and lead were

Discussion
The greatest health risk in low-cost jewelry is associated with lead, particularly in the clasps.Newer model XRF analyzers are very effective for screening lead, even with small pieces.At times, a surface coating can partially mask the actual lead content, but by flattening the item, a better estimate of the total lead content can be made.These coating interferences have been reviewed by Maas et al. 21Our limited analysis of the small spot feature indicated that this feature would not resolve an underestimation of lead, as often there are surface coatings.It is possible that higher energy XRF analyzers using radioactive sources of X-rays, such as is used to measure leaded paint under layers of paint, might do a better job of detecting high levels of lead under surface coatings.In university environments, particularly when the XRF analyzer is used in educational clinics, the use of more powerful XRF analyzers might create restrictions.For example, licensing of more powerful XRF analyzers is more difficult.
Students can learn a lot about toxic metals in educational clinics. 33tudents can also educate their families and friends, and thus reduce the general exposure to toxic metals.This is a very effective way to get important information to the people most at risk.Moreover, having students collect items for analysis can remove the bias associated with purchasing of consumer goods; vendors often detect professionals and avoid selling bootleg items.
Handheld XRF analyzers with x-ray tubes and lower energy x-rays are sufficient for educational clinics and adequate for any review of toxic metals in such products.There is a great deal of variation in the coating on the clasps, including relatively pure lead, lead coated with a mixture of lead and copper, and primarily lead plated with nickel.It is possible that the nickel and copper might reduce the extraction of lead in gastric solutions, and this question should be resolved, but this would not make these clasps safe.There is still a high lead content on the surface of many clasps.Jewelry vendors at times admit to selling jewelry that can initiate skin irritations, and point out better quality jewelry that is a lot less likely to cause skin irritations.About 10-15% of women are known to be allergic to nickel 34 , and individuals can commonly be sensitive to cadmium, copper, etc.However, some jewelry vendors are not so honest.In educational clinics at universities in Phnom Penh, we processed four "gold" rings that were sold as high quality gold, but were mostly copper.In our analysis of jewelry bought by students, we had very little opportunity to process expensive jewelry.No amount of Pb is considered safe for children, and there is a possibility they might chew and ingest the surface of a toy coated with Pb, contributing to elevated BLLs.Maas et al. 21cited two studies that showed handling of Pb-contaminated items with lower Pb weight percent than the jewelry pieces in this study can result in significant transfer of Pb to the skin.Additionally, up to 4 µg of Pb could be transferred from the skin to the surface of food items after a single handling of items contaminated with Pb. 20 Like the jewelry items, the Pb content of toys could not be determined by visual inspection.Different parts of the toy may or may not possess Pb or may contain uneven concentrations.The toys appeared in different colors and designs to which children are attracted.
Only after using an XRF analyzer could the metals concentrations be determined quickly.Thus, XRF analyzers are reliable, robust tools for screening environmental samples and consumable goods.

Conclusion
Because there is a lack of treatment facilities and experience with Pb poisoning in Cambodia, it is important to implement prevention measures and make the public aware of the health risks.Processing consumer goods in educational clinics in schools can be an effective method of education.Labeling of certified consumer goods could help inform parents whether toys or jewelry are suitable for children.Increased monitoring in the US, the EU and in the developing world with XRF analyzers could increase consumer protection.

Table 1 -Toys Recalled Due to Lead Contamination-US Consumer Safety Product Commission 2004
31008 are examples of recalls, whereas 2010-2016 are inclusive of recalls by CPPCResearchUS Pb guideline has been reduced to 90 µg/g.30TheEuropeanUnion(EU) has three categories for heavy metals in toys with the scraped-off category (160 µg/g for Pb) (Table3) being the most relevant to toys in our study.Although significant, the concentrations of Pb in plastic toys in the literature are generally much less than that found in low-cost jewelry.The purpose of this study was to use a handheld X-ray fluorescence analyzer (XRF) to evaluate the lead content in inexpensive jewelry and plastic toys that are sold in markets in Phnom Penh, Cambodia and compare the findings with the European Standard EU EN 71-3:2013 for scraped-off materials.31Murphy,Lim,Kim, Irvine, Chaiwat, WilsonMetal Contamination in Low-Cost Jewelry and Toys in Cambodia

Table 2 -Calibration of XRF XL3t and LPA-1 XRF with a Certified Reference Material
Note: Values are in µg/g *NIST Certified Reference Material, RMD Inc. Colors refer to paint reference materials.Max detected is the maximum detected concentration of metal.% EU Guide is the percentage of samples that exceeded the EU guideline for scraped-off metals.% 100x EU is the percentage of samples that exceeded the EU guideline for scraped-off metals by 100x.

Table 3 -Heavy Metal Content of Low-Cost Jewelry and Toys
4y far the most common cause for a CSPC recall of lead in the toy in the United States was associated with lead in paint (Table1).Since much of the developing world still uses enamel paint with lead,4painted toys in such countries should be expected to be occasionally contaminated with lead or even mercury.Although the four largest recalls of toys in the USA because of lead occurred between 2004 and 2008, the problem of lead contamination remains serious (Table1).