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We conducted a human monitoring survey in Dong Mai, a battery recycling village in Vietnam, to assess exposure status to Pb.. Lead level was measured in hair, blood and urine samples of

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S P E C I A L F E A T U R E : O R I G I N A L A R T I C L E End-of-Life Vehicle (ELV) Recycling

Exposure assessment of lead to workers and children

in the battery recycling craft village, Dong Mai, Vietnam

Takako Noguchi•Takaaki Itai•Nguyen Minh Tue•Tetsuro Agusa•

Nguyen Ngoc Ha•Sawako Horai •Pham Thi Kim Trang•Pham Hung Viet•

Shin Takahashi•Shinsuke Tanabe

Received: 19 January 2013 / Accepted: 19 June 2013

Ó Springer Japan 2013

Abstract Human exposure to lead (Pb) due to

uncon-trolled Pb-acid battery recycling has been an environmental

health issue in newly developed industrial regions We

conducted a human monitoring survey in Dong Mai, a

battery recycling village in Vietnam, to assess exposure

status to Pb Lead level was measured in hair, blood and

urine samples of residents in Dong Mai and two reference

sites during 4 years spanning 2007–2011 In Dong Mai, Pb

levels in three matrixes were significantly higher than those

in reference sites Blood Pb levels of all adults and children

exceeded 10 lg/dL, the Centers for Disease Control and

Prevention definition of an elevated blood Pb level Clear

increase of urinary d-aminolevulinic acid (ALA) level with

increasing blood Pb level indicated disruption of heme

synthesis One adult exceeded 100 lg/dL of blood Pb,

where encephalopathy is of concern The blood Pb levels

achieved various toxic effect threshold values, and elevated

blood Pb was not limited to recycling workers, but was also

in children and women of reproductive age Serious

pollution status of Dong Mai village suggests an impor-tance of further monitoring surveys in various developing Asian countries

Keywords Pb battery  Recycling  Vietnam  Risk assessment Lead

Introduction Lead poisoning remains one of the serious environmental problems in the world, due to prevalent environmental and occupational exposures Lead-acid battery recycling has become a widespread activity in many developing coun-tries [1], and it is an important source of Pb releasing into the environment The hazards of battery recycling have been reported in a series of studies on workers, their families and the environment of various developing coun-tries [2] Vietnam recorded the eighth highest economic growth in Asia [3], and has high resource demands In Vietnam, so called ‘‘craft village’’, which is defined as rural villages with existing craft and non-farming activities drawing the participation of at least 30 % of all households and making at least 50 % of the village’s total income, have greatly contributed to increased income and reduced pov-erty in rural areas It was estimated that ninety waste recycling craft villages are distributed across the country, mainly in the Northern part [4] Although establishment of craft village is an efficient solution to rural economic development, environmental problems are arising because

of the rapidly increasing craft production despite invest-ment for infrastructure being still poor Production in some craft villages, such as plastic, lead and metal recycling craft villages, typically leads to dangerous chronic diseases such

as cancer and heavy metal intoxication, due to manual

T Noguchi  T Itai ( &)  N M Tue  T Agusa 

N N Ha  S Takahashi  S Tanabe

Center for Marine Environmental Studies (CMES),

Ehime University, 2-5 Bunkyo-cho, Matsuyama,

Ehime 790-8577, Japan

e-mail: itai@sci.ehime-u.ac.jp

N M Tue  P T K Trang  P H Viet

Centre for Environmental Technology and Sustainable

Development (CETASD), Hanoi University of Science,

Vietnam National University, T3 Building, 334 Nguyen Trai

Street, Thanh Xuan District, Hanoi, Vietnam

S Horai

Recycling-oriented Environmental Science, Department

of Regional Environment, Faculty of Regional Sciences,

Tottori University, 4-101 Koyama-cho Minami, Tottori,

Tottori 680-0945, Japan

DOI 10.1007/s10163-013-0159-0

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procedures of recycling and poor understanding of workers

about environmental impacts [5] Dong Mai is such a

vil-lage in the Northern part of Vietnam, and has been

recy-cling Pb-acid battery for the past 40 years A local news

report suggested that of 259 households in the village, at

least 61 were involved in Pb recycling, totaling more than

500 workers [6] The General Department of

Environ-ment’s report in 2008 warned that Dong Mai villagers can

lose up to 10 years of their lifespan due to environmental

pollution Another report estimated that 71.1 % of residents

have mental diseases and 65.6 % have respiratory diseases,

and 100 % of workers suffer from chronic Pb poisoning

[7] Considering the situation in Dong Mai, quantitative

assessment of exposure status in the village residents is

necessary

In this study, human exposure to Pb was assessed in a

Pb-acid battery recycling site in Dong Mai We have

car-ried out sampling surveys in Dong Mai and two reference

sites since 2007 Screening of Pb levels in residents was

conducted via analysis of scalp hair, blood and urine

Health risk for residents was assessed by comparing blood

Pb level to the epidemiologically suggested threshold

val-ues of Pb intoxication Urinary d-aminolevulinic acid

(ALA) was measured as a biomarker of Pb-induced

ane-mia These surveys aim to elucidate exposure status and

health risk, as well as toxicological implications related to

battery recycling

Materials and methods

Study sites

Dong Mai village (hereafter DM) in Van Lam district,

Hung Yen province, Vietnam was chosen as a study site

DM is a small Pb-acid battery recycling craft village with

approximately 2300 residents Several hundred tons of

waste batteries were transported to DM every month, and

the estimated monthly production volume of Pb ingots was

250 tons Most business was family-based and batteries

were recycled in the backyard of each house

Urban control samples were collected from Hanoi city

(hereafter HN), the capital city of Vietnam, in 2008,

whereas rural control samples were collected from Duong

Quang village (hereafter DQ) in 2010 and 2011 Distances

to the reference sites from DM were ca 26 km and 9 km,

respectively

Sample collection

The primary screening surveys were conducted in DM and

HN in September 2007 and 2008 (hereafter ‘‘first survey’’),

whereas continued monitoring were conducted in DM and

DQ in January 2010 and 2011 (hereafter ‘‘second survey’’)

In both surveys, scalp hair, blood and urine were collected from the residents Cumulative participants of the first survey were 49 and 20 in DM and HN, respectively In the second survey, cumulative participants were 93 (including

23 children from 4 to 18 years old) and 71 (including 5 children) in DM and DQ, respectively (Table1) Sex, age, height and weight measurements, occupation, smoking and drinking habitats, hair length and residents time were recorded, and informed consents were obtained from all donors All samples were kept in gel ice immediately after collection and then sent to our laboratory in Centre for Environmental Technology and Sustainable Development (CETASD), Hanoi University of Science, and frozen at

-20°C The frozen samples were air transported with gel ice

to the Environmental Specimen Bank (es-Bank) at Center for Marine Environmental Studies (CMES), Ehime Uni-versity, Japan and stored at -25°C until analysis [8]

Chemical analysis of elements Human hair samples were washed in an ultrasonic bath with 0.3 % of polyoxyethylene lauryl ether and subse-quently dried for 12 h at 80 °C [9] Hair samples were digested in a mixture of concentrated HNO3and 50 % HF (5:1) in Teflon vials using a microwave system (Ethos D, Milestone S.r.l., Sorisole, BG, Italy) Human blood and urine samples were digested in HNO3with the microwave system Hot plate digestion was also employed for blood analyses at 200 °C for 3 h in Teflon vials The level of Pb was measured using an inductively coupled plasma mass spectrometer (ICP-MS; Agilent 7500cx, Agilent Technol-ogies, Tokyo, Japan) Rhodium was used for internal standards for correction of matrix effects and instrumental drift in ICP-MS measurements Accuracy and precision of measurements was assessed by analyzing standard refer-ence materials: NIES No 5 human hair and NIES No 18 human urine provided by National Institute for Environ-mental Studies (NIES), Japan and IAEA A-13 bovine blood provided by International Atomic Energy Agency (IAEA), Austria The recoveries of elements were in the range of 87–106 % of certified value

Urinary d-aminolevulinic acid analysis Determination of urinary d-aminolevulinic acid (ALA) was carried out by SRL Inc., Tokyo, Japan A brief procedure

of analysis was as follows The urine sample was mixed with in acetyl acetone, ethanol and formaldehyde solution and boiled The fluorescent derivative of ALA was ana-lyzed by high performance liquid chromatography coupled with a fluorometer

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Statistical analysis

All statistical analysis was performed with Statcel 2 (Seiun

Inc., Tokyo, Japan) and R software (version 2.14.0) The

Mann–Whitney U test was employed to verify significant

differences between DM and HN or DQ The Steel–

Dwass’s test was used to determine the difference in blood

Pb levels among six groups, i.e., adult male in DM, adult

female in DM, male children in DM, female children in

DM, adult male in DQ, and adult female in DQ A p value

of less than 0.05 was considered as an indication of

sta-tistical significance, unless otherwise mentioned The data

below the limit of detection were included in the statistical

evaluation as an estimated 50 % of the detection limit

value

Results

Pb levels in hair, blood, and urine

The Pb levels in hair were determined only in the first

survey population The Pb level in hair was extremely high

in DM compared to HN (Table1) The median value ratio

of Pb between DM and HN were 27

The Pb level in blood was determined in both the first

and the second surveys Among the first survey population,

the Pb levels in DM were higher than HN (p \ 0.001)

(Table1), with the median value ratio of Pb being 6.1

Among the second survey population, blood Pb levels of 93

residents in DM were statistically higher than in DQ

(p \ 0.001) (Fig.1) The median value ratio of blood Pb

between DM and DQ was 11 In DM, blood Pb levels in the

second survey population were significantly higher than

that of first survey population (p \ 0.001)

Among the second survey population, blood Pb levels of

adult males were higher than those of females in DM

(p \ 0.01), whereas gender difference was insignificant among residents in DQ (Fig.1) Blood Pb levels of 23 children in DM were also higher than for residents in DQ (p \ 0.01) (Fig.1) In DM, blood Pb levels of children were comparable to those in females The median value ratio of blood Pb between children in DM and residents in

DQ was 9

The trace element levels in urine were determined only

in the first survey population In urine, the levels of Pb were significantly higher in DM than in HN (p \ 0.001), with the ratio of median values of Pb being 8.7

Table 1 Median and range of Pb concentration in hair (lg/g), blood (lg/dL) and urine (ng/g) in residents of DM and reference sites in first and second surveys

Hair (first survey) Blood (first survey) Blood

(Second survey)

Urine (first survey)

Dong Mai 51 (2.5–2300) n = 49 20 (5.5–110) n = 49 34 (14–122) n = 93 24 (3.1–200) n = 49 Adult male 120 (2.5–2300) n = 16 35 (14–110) n = 16 43 (23–122) n = 30 56 (12–200) n = 16 Adult female (n = 16) 48 (19–220) n = 33 20 (5.5–71) n = 33 36 (14–87) n = 40 20 (3.1–150) n = 33 Child (n = 16) N.A N.A 29 (17–48) n = 23 N.A.

Hanoi (first survey) and

Duong Quang (second survey)

1.9 (0.80–5.5) n = 20 3.3 (1.9–6.3) n = 20 3.3 (1.0–11) n = 71 2.7 (0.79–6.0) n = 20

Adult male (n = 16) 3.0 (0.96–4.3) n = 9 4.1 (2.3–6.3) n = 9 4.2 (2.3–10) n = 24 2.7 (1.5–6.0) n = 9 Adult female (n = 16) 1.7 (0.80–5.5) n = 11 2.8 (1.9–4.5) n = 11 2.7 (1.0–11) n = 42 2.8 (0.79–5.8) n = 11 Child (n = 16) N.A N.A 2.9 (2.0–5.0) n = 5 N.A.

N.A not available

Fig 1 The box-whisker plot of blood Pb levels among six groups Only the data obtained from the second survey were used The horizontal line indicates the median, the box covers the 25th–75th percentiles and the maximum length of each whisker is 1.5 times the interquartile range Points outside this show up as outliers Groups with the same letters do not have significantly different levels in Steel–Dwass’s test for multiple comparisons

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Relationship between blood Pb and urinary ALA

The ALA analysis was conducted for the second survey

population Urinary ALA levels in DM varied from 0.3 to

71 mg/L in DM, and were significantly higher (p \ 0.001)

than those of DQ (0.1–3.0 mg/L) The ALA levels

posi-tively correlated with blood Pb levels in DM (p \ 0.001,

r = 0.47), whereas these were not correlated in DQ

(p [ 0.05, r = -0.19) (Fig.2)

Discussion

Exposure level

The human monitoring data of this study demonstrated

serious contamination by Pb in DM residents The Pb

levels of scalp hair in DM were comparable to other

seri-ously contaminated sites, e.g., Singapore (mean 640, range

0.93–3500 lg/g) [10], Poland (mean 150, range

35–290 lg/g) [11] and the West Indies (mean 590, range

51–1500 lg/g) [12]

Similar to the scalp hair, blood Pb levels also indicated

serious exposure status Because blood Pb levels are a more

direct signature of Pb burden in the body than hair,

com-parison to the other sites is useful to evaluate potential of

health effect The blood Pb levels of this study were

comparable to those reported in other studies where some

health effects are observed, i.e., children in a backyard

battery repair shop in Jamaica, where 22 children were

hospitalized for Pb poisoning (mean 32, range 31–170 lg/

dL) [13]; hormone disruption of Taiwanese battery workers

(mean ± SD: 24 ± 12 lg/dL) [14]; and residents in a

Senegalese battery recycling area where 18 children died (mean 56, range 38–81 lg/dL) [1] Gender differences of blood Pb levels provided some information for exposure pathway Males showed higher blood Pb levels than females since they often are more likely to engage in the Pb smelting work, whereas females only dismantled waste batteries

It is worth noting that children also have higher level of blood Pb than those found at the reference site Therefore, environmental Pb contamination in DM was not limited to workers, but also local residents like children

Risk assessment for human exposure to Pb among second survey population

Health risk of Pb exposure was evaluated by comparing the blood Pb levels to the epidemiologically defined toxic effect thresholds Of the 93 residents, including 23 chil-dren, from DM, all had blood Pb levels exceeding the minimum toxic threshold values (10 lg/dL) recommended

by The Agency for Toxic Substances and Disease Registry [15] Blood Pb levels greater than this value may induce decreasing activity of heme biosynthesis enzymes and elevating blood pressure Since Pb is a cumulative toxicant that affects multiple body systems, such as neurological, hematological, gastrointestinal, cardiovascular and renal systems, continuous Pb-acid battery recycling could lead to serious health risk among residents Blood Pb levels greater than 100 lg/dL raise concern of encephalopathy [15] One adult corresponded to this blood Pb level, with it as high as

122 lg/dL Actually, this level is comparable to those reported in a serious Pb pollution site in Dakar, Senegal, where 18 children have died, possibly due to Pb exposure [1]

The urinary ALA levels supported possible manifesta-tion of toxic effect by the Pb exposure ALA level is an initial compound in the heme synthesis pathway, and its level in urine can be used as the signature of anemia, which

is the initial manifestation associated with Pb exposure The inhibition of ALA dehydratase (ALAD) by Pb causes

an increase in ALA in plasma, and consequently excretion

of ALA in urine [16, 17] Urinary ALA levels increased with blood Pb levels, suggesting that inhibition of ALAD occurred due to high Pb in blood (Fig.2) This clear rising trend, stated from around blood level [ 50 lg/dL, was almost consistent with the trend observed in a previous study [18]

Since Pb exposure was not limited to the adults but also children in DM, adverse effects for children are of partic-ular concern Children, with their nervous system in active development, are generally vulnerable to the neurotoxico-logical affects of Pb Higher gastrointestinal tract uptake ratio and hand-to-mouth behavior enhances risk for

0

10

20

30

40

50

60

70

80

Blood Pb (µg/dL)

: DM

p < 0.001, r = 0.47

: DQ

p > 0.05

Fig 2 Relationships between urinary ALA and blood Pb levels of

the participants in the second survey

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children [19] The minimum threshold blood Pb level

corresponding to adverse health effects are lower than

adults [20] The Center for Disease Control and Prevention

(CDC) recommends that children’s blood Pb levels greater

than 10 lg/dL require further monitoring [21] All 23

children surveyed in DM had levels greater than 10 lg/dL,

with a maximum of 48 lg/dL According to the field

observation and questionnaire survey, children were not

directly involved in the recycling activity in both smelting

factory and backyard recycling site Hence, this result

suggests two possibilities: 1) the extent of Pb

contamina-tion is already widely spread in the village; or 2) children

are actually involved in the recycling activity In either

case, the situation is serious

The current situation in DM is serious, and a more

severe situation may probably occur if urgent mitigation

activity is not taken up soon Lead is a well-known

cumulative toxicant and prenatal Pb exposure can occur not

only through current maternal environmental exposures,

but also through the mobilization of cumulative maternal

bone Pb stocks during pregnancy and lactation [22, 23]

Additionally, maternal Pb burden causes risk for the

fol-lowing generation, even after improvement of the

con-taminated environment [24] Seventy-two percent of the

women in DM were in reproductive age, and their median

blood Pb level was 36 lg/dL, which may be associated

with adverse birth outcomes [25–27] All the facts strongly

suggest that medical treatment such as chelating therapy is

urgently needed in the village, DM [28]

Conclusion

Serious contamination of Pb was confirmed in the Pb-acid

battery recycling site in Dong Mai village, Northern part of

Vietnam The blood Pb levels achieved various toxic effect

threshold values, and apparent enrichment in blood was not

limited to recycling workers, but was also in children and

women of reproductive age The manifestation of Pb

poi-soning was apparent by clear elevation of urinary ALA

levels

Considering the widespread Pb contamination in the

village scale, not only should further monitoring be

con-tinued, but providing a pollution control solution is also

needed Since the major exposure pathway is likely

inha-lation and/or ingestion of heavily contaminated soil and

dust in suspension, soil removal is an important solution to

prevent residents from further exposure A preliminary

screening using field portable X-ray fluorescence

spec-troscopy indicated that Pb level in soil is highest around a

smelting plant (up to 15 wt%), then decreases

exponen-tially with distance (unpublished) In the case of the battery

recycling site in Senegal, the Senegalese government and a

non-government organization (Blacksmith Institute) suc-ceeded in reducing symptoms of Pb poisoning in humans

by removal of soil from the high Pb region that exceeded

Pb content [1,000 mg/kg [29] We assume that the same treatment may be also effective in DM The estimated area

in which the soil Pb level exceeds 1000 mg/kg in Dong Mai is ca 10,000 m2 Hence, ca 2,000 m3of soil should be removed, assuming that effective removal depth is 20 cm

In the Senegal case, the budget to complete soil removal was USD 200,000 to remove 3,700 m3soil in 2 years In order to achieve such a mitigation program, establishment

of a cooperative framework by national and local govern-ments and non-government organizations is urgently needed

Finally, the result of this study is an alarm that similar situations may occur in other craft villages in Vietnam, and also in other Asian developing countries Since transport of waste material is not limited to national scale, the help of developed countries is important to improve the material recycling system in developing Asian countries

Acknowledgments This study was supported by Grants-in-Aid for Scientific Research (A) (No 25257403), ‘‘Global COE Program’’ and

‘‘Project for the Encouragement of Science/Math-Oriented University Students’’ from the Ministry of Education, Culture, Sports, Science and Technology, Japan (MEXT) and Japan Society for the Promotion

of Science (JSPS) and Waste Management Research Grant (K123001) from the Ministry of Environment, Japan We also acknowledge the approval of the Photon Factory Program Advisory Committee (Pro-posal No 2009G632) The success of this investigation was thanks to the support and collaboration of donors and member of the health authorities in Dong Mai and Duong Quang village.

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