Environ Sci Pollut Res DOI 10.1007/s11356-014-2596-2

RESEARCH ARTICLE

ALAD genotypes and blood lead levels of neonates and children from e-waste exposure in Guiyu, China Xia Huo & Lin Peng & Bo Qiu & Liangkai Zheng & Taofeek Akangbe Yekeen & Xijin Xu

Received: 24 November 2013 / Accepted: 23 January 2014 # Springer-Verlag Berlin Heidelberg 2014

Abstract Extensive e-waste recycling activity in Guiyu, China, has been conducted using primitive techniques for the last 20 years, resulting in serious heavy metal environmental contamination. A polymorphic variant of the δaminolevulinic acid dehydratase (ALAD) gene has been found to influence lead uptake and, thus, may influence an individual’s susceptibility to lead toxicity. We therefore explored whether the ALAD gene polymorphism affects blood lead levels of newborns and children in Guiyu. A total of 273 newborns and 504 children, and a combination of 2004/2005 and 2006 independent recruitments were used for this study. Umbilical cord blood from newborns (Guiyu/exposed group 189 vs. Chaonan/reference group 84) and venous blood from children (exposed group, 319 vs. Chendian/reference group 185) were collected. Blood lead levels (BLLs) were measured via graphite furnace atomic absorption spectrometry (GFAAS) for all samples, while ALAD genotyping was performed using PCR-RFLP for 273 neonate cord blood and 246 children’s blood. The median BBLs of neonates in exposed group vs. the reference group were 10.50 (2.36–40.78) vs. 7.79 (0.8–19.51) for 2004/2005 and 9.41 (9.28–47.60) vs. 5.49 (0.35–18.68) for 2006, while child mean BLLs were 15.31±5.79 vs. 9.94±4.05 for 2004/2005 and 13.17±5.98 vs. 10.04 ± 4.85 for 2006. The genotype frequencies in

Responsible editor: Philippe Garrigues X. Huo : L. Peng : B. Qiu : L. Zheng : T. A. Yekeen : X. Xu (*) Laboratory of Environmental Medicine and Developmental Toxicology, and Provincial Key Laboratory of Infectious Diseases and Molecular Immunopathology, Shantou University Medical College, 22 Xinling Rd., Shantou 515041, Guangdong, People’s Republic of China e-mail: [email protected] X. Xu Department of Cell Biology and Genetics, Shantou University Medical College, Shantou 515041, Guangdong, China

newborns were 98.90 % for the ALAD-1/ALAD-1 homozygote and 1.10 % for the ALAD-1/ALAD-2 heterozygotes, while the values were 95.93 and 4.07 %, respectively, in children. The allele frequencies of the ALAD-1 and ALAD2 were 99.45 and 0.55 % for newborns, but 97.97 and 2.03 % for children, respectively. No significant differences in blood lead levels were found between ALAD-1/ALAD-1 and ALAD-1/ALAD-2 either in newborns or in children. The frequency distribution of the ALAD-2 allele in newborns from the exposed group was lower than that of the reference group. There were no significant differences, between the two different ALAD genotypes in the lead load of newborns and children. The frequency distribution of ALAD gene does not influence the blood lead levels of newborns and children in this case, which means that the higher lead burden in the exposed children was possibly influenced by e-waste recycling, but not ALAD genotypes. Keywords Lead . Newborn . Children . E-waste . Delta-aminolevulinic acid dehydratase . Polymorphism

Introduction The rapid development of modern science and technology has accelerated the updating and upgrading of new electronic products. Obsolete electronic products are increasing at an astonishing rate and have become the world’s largest source of electronic waste (e-waste). Guiyu has a nearly 20-year history of e-waste recycling. Recycling is often performed by uncontrolled methods that damage the environment and threaten health (Huo et al. 2007; Samarasekera 2005; Wu et al. 2010). Several studies have shown that Guiyu residents and the Guiyu environment have soaring levels of toxic heavy metals, as well as the highest documented levels of atmospheric polychlorodibenzo-pdioxins (PCDDs), polychlorodibenzofurans (PCDFs), and

Environ Sci Pollut Res

polybrominated diphenyl ether (DE) in the world (Bi et al. 2007; Li et al. 2007; Wang and Guo 2006; Wong et al. 2007a, b, c; Leung et al. 2008). Our previous study found that people employed in e-waste recycling companies in Guiyu had a high incidence of skin damage, headaches, vertigo, nausea, chronic gastritis, and gastric and duodenal ulcers (Qiu et al. 2004) and that Guiyu children and newborns had significantly higher blood lead, cadmium, and meconium lead levels (Huo et al. 2007; Li et al. 2008a, b; Zheng et al. 2008; Guo et al. 2010; Liu et al. 2011; Yang et al. 2013; Zheng et al. 2013). Lead is a toxic heavy metal of which exposure results in significant adverse effects to multiple organ systems such as nervous, hematologic, renal, and reproductive systems (Ahamed and Siddiqui 2007; Hu et al. 2007; Telisman et al. 2007; Aseervatham et al. 2013). Although the half-life of blood lead is approximately 30 days (Menke et al. 2006; Yakub and Iqbal 2010) and evaluation of Pb from mothers blood could only reflect primarily recent external exposure, long-term exposures through efflux of lead from bone stores and continuous exposure of the pregnant mothers to lead sources coupled with no placental-fetal barrier to lead transport (Goyer 1990) may increase possible toxic effects of lead on the child while in utero. Fetal blood lead levels are nearly equal to maternal blood lead levels. The primary mechanism for transplacental lead transport is probably simple diffusion and is probably related to fetal blood flow rate (Goyer 1990). Previous reports have shown that the δ-aminolevulinic acid dehydratase (ALAD) genotype influences the distribution and accumulation of lead in the blood and target organs (Zhao et al. 2007). The ALAD gene is located on chromosome 9q34 and is approximately 16 kilobases long (Wetmur et al. 1986). This gene codes for the ALAD enzyme which catalyzes the second step in heme synthesis involving the asymmetric addition of two molecules of aminolevulinic acid to form the monopyrrole porphobilinogen, which is the precursor of heme (Kelada et al. 2001). The ALAD gene shows a polymorphism (G-to-C transversion at position 177) leading to two alleles (ALAD-1 and ALAD-2) and three phenotypes (ALAD 1-1, ALAD 1-2, and ALAD 2-2) (Montenegro et al. 2006). ALAD-2 codes for a more electronegative enzyme, and the ALAD-2 protein is thought to be able to bind positively charged lead ion more tightly than the ALAD-1 protein. Carriers of the ALAD-2 allele who are exposed to lead might then retain lead in their blood and tissues longer, increasing the chance of an adverse effect due to inhibition of ALAD and consequent buildup of aminolevulinic acid or perhaps due to lead itself, which can initiate oxidative damage and change the structure of cellular components (Kelada et al. 2001). To analyze whether ALAD gene polymorphism affects the blood lead levels of newborns and children, we examined the frequency distribution of ALAD genotypes and the relationship between ALAD genotype and lead levels of newborns and children in an e-waste recycling town, and analyzed whether

this hereditary factor is a major factor in governing the lead exposure of newborns and children in Guiyu.

Materials and methods Study subjects All pregnant women on delivery from December 2004 to June 2005 and July to October 2006 at two hospitals in Guiyu (exposed group) and Chaonan (a town 11.6 km from Guiyu, used here as the reference group) were recruited to participate in this study. The site locations are as shown in Fig. 1. A total of 273 pregnant women agreed to participate, out of which 189 were from the exposed group and 84 were from reference group. Exclusion criteria for enrolling mothers and newborns were as follows: prenatal hypoxic-ischemic history, severe psychiatric disorders requiring medication, diabetes, or cancer. Also recruited were 165 and 61 children for the exposed group and reference group (Chendian, about 10 km from Guiyu), respectively, for 2004/2005 (Huo et al. 2007), while 154 children from the exposed group and 124 children from the reference group were recruited in 2006 (Zheng et al. 2008) to participate in this study. A questionnaire was administered to obtain demographic information of the mothers/neonates as well as children. With consent from parents or guardians, umbilical cord blood samples and venous blood samples were respectively collected from the newborns and children. After cutting the umbilical cord of the newborns, 5 mL of umbilical cord blood was collected from the placenta into metal-free EDTAcontaining sealed glass automatic hemostix. Similarly, 2 mL of venous blood was collected from the children into metalfree EDTA-containing sealed glass automatic hemostix. Samples were stored in the refrigerator at −20 °C. This study was approved by the Human Ethics Committee of Shantou University Medical College. Laboratory analysis Lead levels in umbilical cord blood (CBPb) were determined in the Central Laboratory of Shantou University Medical College by graphite furnace atomic absorption spectrometry, which consisted of a Shimadzu AA-660 AAS, a GFA-4B graphite furnace atomizer and a 1 ASC-60G autosampler (Shimadzu Corporation, Kyoto, Japan), with injection volume set at 10 μL. The main parameters used for lead determination were a 283.3-nm wavelength, 8-mA current, 1.00-nm slit width, 150 °C drying temperature, ashing at 325 °C, and atomization at 1,400 °C (Koreckova-Sysalova 1997). The accuracy of the methods was controlled by recoveries of 95 and 107 % from the spiked blood samples. The detection limit for lead was 0.21 μg/L.

Environ Sci Pollut Res Fig. 1 Map of the sampling sites. The locations of Guiyu, Chaonan, and Chendian are shown

Identification of ALAD polymorphisms The ALAD polymorphism was determined by polymerase chain reaction (PCR) with restriction fragment length polymorphism as previously described (Schwartz et al. 1995). We performed PCR reactions in duplicate, with blank controls included in each set. Briefly, amplifications were performed on 0.5 μL of whole blood using a primer set specific for a portion of the ALAD gene. Primer sequences for amplification were 5′-GGTCAGGAGGACCGTTGCCT-3′ and 5′ATTTTTTGTAGAGATGGGTTTTGCC-3′, which generated a 307-nucleotide base-pair fragment. Amplified DNA was then restricted using MspI and electrophoresed through 2.0 % agarose. ALAD alleles were differentiated based on the existence of an MspI endonuclease restriction site specific for ALAD-2, which yielded a diagnostic restriction band. Heterozygotes exhibiting both the ALAD-1 and ALAD-2 fragments could, in this way, be differentiated from homozygotes of either type. All neonate cord blood and only 2006 children blood samples were evaluated for ALAD gene polymorphisms due to insufficient samples. Statistical analysis Independent-sample t tests were used to determine differences between groups, and nonparametric analyses were used for data with skewed distribution. χ2 values were calculated by use of the chi-square test for categorical data. The HardyWeinberg equilibrium test was used to compare the theoretical frequency distribution and actual frequency distribution. All

analyses involved use of SPSS version 13.0 software (SPSS, Inc., Chicago, IL, USA). A P0.05 >0.05 >0.05 >0.05

72 (72.0 %) 28 (28.0 %) 39.41±1.50 9.77±0.45 0.50±0.02 3.12±0.40

28 (53.85 %) 22 (46.15 %) 38.98±1.54 9.79±0.50 0.50±0.01 3.29±0.52

>0.05

62 (62.00) 38 (38.00)

25 (48.08) 27 (51.92)

>0.05

0.05 >0.05 >0.05 >0.05

0.05). The

frequency distribution of ALAD-1 and ALAD-2 were 99.45 and 0.55 % for neonates, but 97.97 and 2.03 % for children, respectively. No significant deviation from the HardyWeinberg equilibrium was detected from study subjects (P>0.05, Table 2). Average blood lead concentrations were correlated with ALAD genotype in each residence area. There were no significant differences between blood lead levels and either of ALAD-1/ALAD-1 or ALAD-1/ALAD-2 both in newborns and children (all, P>0.05, Fig. 3). However, there were significant differences in Pb levels between the exposed group and the reference group, except for ALAD-2 in children (P0.05

* *

P25 Max Min

ALAD1-2

R

E R E Children

ALAD1-2

ALAD1-1

R E Neonates

ALAD1-1

E

ALAD1-2

R

ALAD1-2

P50 ALAD1-1

50 45 40 35 30 25 20 15 10 5 0

ALAD1-1

Pb level(µg/dL)

have a prevalence of 96.70 and 3.30 %, respectively, in Chinese Han population (Zheng et al. 2001). Our study subjects were Chinese Han population, and the frequency distribution of ALAD-1 allele was 99.21 % and ALAD-2 allele was 0.79 % in Guiyu. Compared with other populations, frequency distribution of ALAD-2 allele in Guiyu was very low, and there were no significant differences in lead load between homozygous ALAD-1/ALAD-1 and heterozygous ALAD-1/ ALAD-2 children in Guiyu, which means that the lead load of the subjects was influenced by other factors. E-waste recycling in Guiyu had led to high Pb values reported for neonates and children in 2004/2005. Reduction was observed compared to 2006, and this trend continues over the years as shown by our previous studies on neonates (Xu et al. 2012) and children (Liu et al. 2011, 2014; Yang et al. 2013). This reduction was attributed to government efforts, increase in health awareness of local people (Zheng et al. 2008), and the economy recession of 2009 which affected ewaste business greatly. Nevertheless, the Pb values of neonates and children in Guiyu are still higher than 5.0 μg/dL which was considered as elevated blood lead levels (BLLs) (NCEH-CDC 2013). The differences observed with Pb

P75

Fig. 3 Comparison of the lead levels in blood of neonates and children based on ALAD genotypes between the reference and exposed groups (*significant difference in Pb between groups (P0.05) in Pb concentration between genotypes within group)

concentrations in children higher than that of neonates may be due to the involuntary or direct ingestion of contaminated dust particles via the “hand-to-mouth” pathway (Zhu et al. 2012). In addition, the increased Pb accumulation in children could be via inhalation, as a report had shown that a high level of Pb was observed in TSP (Pb 444±228) and PM2.5 (392± 244) evaluated for samples collected in Guiyu in 2004 (Deng et al. 2006). Children have been reported to be sensitive to heavy metal and metalloid poisoning (Fowler 1993). The ALAD gene can modify lead toxicokinetics and ultimately influence individual susceptibility to lead poisoning (Garcia-Leston et al. 2012). Lead protein binding tests suggest that ALAD is the most important lead-binding protein in blood (Gonick 2011). Prior studies have reported that compared to ALAD-1/ALAD-1 individuals, ALAD-1/ALAD-2 and ALAD-2/ALAD-2 individuals have a more negatively charged enzyme, with greater affinity for lead and increased blood lead levels (Gao et al. 2010). Furthermore, studies of lead protein binding showed that 84 % of protein-bound lead was bound to ALAD in ALAD-2 carriers, while 81 % was bound to this enzyme in the ALAD-1 homozygotes (Sobin et al. 2011). These suggest that although both forms of the enzyme bind great quantities of lead, ALAD-2 may bind the metal with the highest affinity. Wetmur et al. (1991b) found that the ALAD-2 allele contains G-C transversion at position 177 of the coding region, generating a new MspI restricted enzyme site, resulting in the substitution at amino acid 59 of asparagine for lysine. It appears that this substitution changes the electrical charge of the molecule resulting in ALAD-2 having a higher affinity for lead than ALAD-1. So we studied ALAD gene polymorphism to analyze whether ALAD is a major factor governing lead accumulation in newborns and children due to lead exposure from e-waste recycling. We found that the frequency of the ALAD-2 allele in newborns and children of Guiyu was lower than that of other areas. There were no significant differences in lead load of newborns and children among different ALAD genotypes in Guiyu vs. the reference group. Our results indicate that the ALAD allele does not influence the blood lead levels of

Environ Sci Pollut Res

newborns and children in Guiyu. This study provides the first analysis of the frequency distribution of the ALAD allele and the impact of the ALAD allele on blood lead levels in an ewaste recycling town. The relatively high levels of blood lead of newborns and children from Guiyu were not associated with their ALAD genotypes, but probably influenced by the primitive e-waste recycling activities.

Acknowledgments This work was supported by the National Natural Science Foundation of China (21177080) and Guangdong University Project for International Cooperation and Innovation Platform (2013gjhz0007). We wish to thank Dr. Stanley Li Lin for his constructive comments. Conflict of interest The authors declare that there are no conflicts of interest.

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ALAD genotypes and blood lead levels of neonates and children from e-waste exposure in Guiyu, China.

Extensive e-waste recycling activity in Guiyu, China, has been conducted using primitive techniques for the last 20 years, resulting in serious heavy ...
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