Abstract
The Seo-Cheon Janghang Smelter in South Korea closed in 1989 owing to its contribution to environmental pollution. The emissions from the smelter likely affect various environmental media and also pose significant health risks to nearby residents, particularly in relation to exposure to heavy metals such as lead, cadmium, and arsenic. Although the environmental impacts of the smelter are known, long-term follow-up studies on heavy metal exposure in nearby residents remain limited, especially after remediation. This study aimed to assess the levels of heavy metal exposure and associated health effects, particularly on renal and bone health. We analyzed blood and urine samples from 37 volunteers, collecting demographic, lifestyle, and exposure-related data through interviews. Renal function tests and bone mineral density measurements were conducted. The geometric means for blood lead (bPb) and blood cadmium (bCd) were 1.95 μg/dL and 2.68 μg/L, respectively. The mean urinary cadmium (uCd) concentration was 3.74 μg/g cr. Urinary total and harmful arsenic concentrations were 165.7 μg/L and 1.00 μg/L, respectively. The bPb levels significantly decreased from 2008 to 2020, whereas cadmium levels did not show significant change overall. Among 28 participants tested in both years, bCd levels decreased for individuals living > 2 km from the smelter, while remaining stable for those closer. The uCd levels significantly decreased only in individuals who had relocated > 2 km away from the smelter. Despite remediation efforts, uCd levels remain persistently elevated. These findings underscore the need for continuous exposure monitoring and longitudinal health assessments of residents living near the former smelter.
Keywords: Follow-up, Health effect, Heavy metal exposure, Smelter
Introduction
Although smelters have been essential to industrialization, they emit heavy metals into the surrounding environment [1]. These heavy metals—including lead (Pb), cadmium (Cd), arsenic (As), copper (Cu), and zinc (Zn)—are often found in base metal ores. During the smelting process, they may be released through chimneys, disposed of in landfills alongside other waste products, or dispersed as ore dust, thereby contaminating nearby soil and water sources [2].
In Korea, rapid industrialization led to the widespread and often unregulated establishment of pollutant-emitting facilities, which often negatively influenced the health and property of nearby residents. Consequently, residents living near smelters exhibit significantly higher levels of heavy metal exposure than those residing farther away [3, 4].
As, Pb and Cd are among the most hazardous substances, ranking first, second, and seventh, respectively, on the National Priority List (NPL) of the U.S. Agency for Toxic Substances and Disease Registry (ATSDR) [5]. Arsenic (As) is a well-established human carcinogen, with dietary exposure identified as the primary route of entry for the general population [6, 7]. Inorganic arsenic and its compounds are classified as Group 1 human carcinogens, indicating sufficient evidence for carcinogenicity in humans [8]. Moreover, arsenic exposure has been associated with cardiovascular disorders, reproductive toxicity, developmental delays in children, and immunosuppression [9]. Lead (Pb) is a potent neurotoxin, particularly in children, where it has been linked to reduced IQ, behavioral disorders, and impaired cognitive development—even at blood lead levels below 5 µg/dL [10, 11]. In adults, chronic lead exposure is associated with hypertension, kidney dysfunction, and reproductive toxicity, including reduced sperm count and increased risk of miscarriage [10–12]. Inorganic lead compounds are classified as “probably carcinogenic to humans” (Group 2A) [13]. Cadmium (Cd) is primarily transmitted through the consumption of contaminated food and water, inhalation of contaminated air, and, less frequently, through skin contact. Individuals residing near mining or industrial areas are at an increased risk of cadmium exposure due to environmental accumulation [14]. Upon entering the body, cadmium binds to proteins and circulates through the bloodstream, accumulating predominantly in organs such as the kidneys and liver. Notably, cadmium has an exceptionally long biological half-life, often exceeding a decade, leading to gradual accumulation over time [15]. Due to its persistence in the environment and bioaccumulate nature, Cd, remains a significant public health concern worldwide, necessitating continued monitoring and mitigation efforts, especially in communities near industrial or mining activities.
In 2008, following environmental pollution complaints from local residents, a detailed investigation of heavy metal contamination was conducted near the former Janghang Smelter in Seocheon-gun, Chungcheongnam-do, South Korea. The study found that soils within a 500-m radius of the smelter exceeded contamination standards for Cu, Zn, Pb, Cd, As, and Ni [16]. A subsequent health assessment showed that residents had significantly higher Cd and Pb exposure levels compared to a control group from a rural area approximately 15 km away. These findings confirmed the former smelter as a major source of heavy metal exposure [17, 18].
Following the 2008 findings, the Ministry of Environment implemented a series of measures, including acquiring heavily contaminated land and relocating residents between 2009 and 2012. These actions were followed by full-scale soil remediation projects that began in 2013. However, whether these policies effectively reduced heavy metal exposure among residents remains unclear.
Therefore, this study aims to evaluate the current levels of heavy metal exposure and associated health risks among residents living near the former smelter site and to assess the effectiveness of government intervention policies by comparing present data with those from the 2008 survey.
Materials and methods
Study participants
The participants in this study were 11 males and 26 females who resided near the former Seo-Cheon Janghang Smelter and had applied for damage relief through the Korea Institute of Environmental Science and Technology. All had lived within 4 km of the smelter for > 5 years and had no occupational exposure to heavy metals. Of these participants, 28 had taken part in the 2008 health impact survey of residents near the smelter. Prior to participation, all individuals were informed about the purpose of the study and provided written consent to participate in structured interviews. The survey covered their demographic and socioeconomic characteristics, smoking, drinking, dietary habits, and medical history. Physical measurements, blood pressure, and bone density were assessed, and blood and urine samples were collected. The study protocol was approved by the Institutional Review Board (IRB) of Chung-Ang University, South Korea (No. 1041078–202007-HRBR-137–01).
To compare current heavy metal exposure levels with those from 2008, data from a previous survey conducted by researchers were retrieved and analyzed. Blood Cd and lead concentrations were measured utilizing the same analytical methods as in this study. Urinary Cd and As concentrations were determined by atomic absorption spectrophotometry (AAs).
Determination of metal levels in blood and urine
To evaluate heavy metal exposure, ~ 4 mL of blood and 40 mL of urine were collected from each participant and stored at − 70 °C until analysis. Blood Pb and Cd concentrations were measured using graphite furnace atomic absorption spectrometry with Zeeman background correction (GFAAS; Model No. PinAAcle 900Z, PerkinElmer, Shelton, CT, USA). Whole blood samples were diluted to 0.2% in Triton X-100 containing 1% nitric acid and 0.2% diammonium hydrogen phosphate. Urinary Cd and As concentrations were analyzed using inductively coupled plasma mass spectrometry with a dynamic reaction cell (DRC) (ICP-MS; Agilent 7700 Series ICP-MS, Agilent Technologies, Santa Clara, CA, USA). Urine samples were diluted 1:10 with 1% nitric acid, and indium (115In) was used as the internal standard.
The urinary creatinine concentrations were measured using the colorimetric Jaffe reaction, based on the reaction with picric acid and NaOH, and analyzed with a microplate reader (Spectra 340) [19]. The urinary Cd concentrations were normalized to creatinine levels (μg/g creatinine) to control the effects of urine dilution.
The As species were analyzed using an ICP-MS coupled with high-performance liquid chromatography (HPLC; Agilent 1260 Infinity, Agilent Technologies). The measured species included As3⁺, As5⁺, monomethylarsonic acid (MMA), and dimethylarsinic acid (DMA). Hazardous As concentrations were defined as the sum of the As3⁺, As5⁺, and MMA. Urine samples were filtered through a 0.22-μm membrane filter (Sterile syringe filter, cellulose acetate N.A., PN: 28,145–477 supplied by VWR), then transferred into chromatographic vials and loaded onto autosampler trays.
Kidney injury biomarker measurements
The urinary N-acetyl-β-D-glucosaminidase (NAG) activity and β2-microglobulin (β2-MG) levels were measured as biomarkers of renal tubular damage. The NAG activity was determined using a NAG Quantitative Kit (Shionogi, Osaka, Japan), following the procedures of the manufacturer. The β2-MG levels were measured using a β2-MG Enzyme-Linked Immunosorbent Assay (ELISA) Kit (Immundiagnostik AG, Bensheim, Germany), following the instruction of the manufacturer. The estimated glomerular filtration rate (eGFR) was calculated using the serum creatinine and cystatin C levels based on the Chronic Kidney Disease-Epidemiology Collaboration (CKD-EPI) creatinine-cystatin Eq. (2012) [20].
Bone mineral density measurements
During participant health examinations at Chung-Ang University Hospital, the mineral density of the calcaneus (heel bone) was measured using high-accuracy dual-energy x-ray absorptiometry (DXA) to evaluate bone damage associated with Cd exposure.
Statistical analysis
All data were analyzed using IBM SPSS Statistics for Windows Version 26.0 (IBM Corp., Armonk, NY, USA). Heavy metal concentrations were log-transformed prior to analysis. Group means were compared using Student’s t-tests and analysis of variance (ANOVA). The change in heavy metal concentrations between 2008 and 2020 was assessed with a paired t-test. Analysis of covariance (ANCOVA) was performed to adjust for age and sex when comparing heavy metal concentrations. The chi-square test was applied to examine differences in frequency distributions between groups. Statistical significance was set at p < 0.05 and p < 0.001.
Results
Table 1 presents the demographic characteristics of the participants. The cohort included 26 females and 11 males, with a mean age of 79.6 years. Their mean residence duration was 62.9 years, and they all lived in the area for > 20 years. Thirteen participants (35.1%) resided within 2 km of the smelter, while 24 (64.9%) lived > 2 km away. Twenty-eight (75.7%) participants were non-smokers, 17 individuals (45.9%) were current alcohol consumers, and 20 (54.1%) had no history of alcohol consumption. The proportions of residents who obtained ≥ 50% and < 50% of their total rice intake from local sources were 67.6% and 32.4%, respectively. The participants consumed either tap water or purified water. Overall, 37.8% of the participants had previously worked at the smelter (Table 1). Table 2 presents the heavy metal concentrations in the blood and urine of participants. The geometric mean blood Pb concentration was 1.95 µg/dL, with 2.18 µg/dL in males and 1.86 µg/dL in females. In contrast, the mean blood Pb concentration was 4.14 µg/dL in 2008. The geometric mean blood Cd concentration was 2.68 µg/L, with 3.12 µg/L and 1.90 µg/L in females and males, respectively. The geometric mean blood Cd concentration was 2.64 µg/L in 2008. The geometric mean urinary Cd levels were 3.66 µg/g creatinine, with higher means observed in females (4.55 µg/g creatinine) than in males (2.18 µg/g creatinine). The geometric urinary Cd level was 2.72 µg/g creatinine in 2008. The geometric mean total urinary As concentration was 166.7 µg/L, with 186.8 µg/L and 157.5 µg/L in males and females, respectively. No significant difference was observed between the sexes. The geometric mean harmful As concentration (inorganic As + MMA) was 0.99 µg/L, with 1.11 µg/L and 0.94 µg/L in males and females, respectively. Table 3 presents heavy metal exposure stratified by smoking history, alcohol consumption, local rice intake, and residential area. Total urinary As concentration was higher in smokers (318.3 µg/L) than in non-smokers (134.3 µg/L) (p = 0.029). However, after adjusting for age and sex, the difference was no longer statistically significant. Blood and urinary Cd levels were higher in non-drinkers than in drinkers (p = 0.040 for bCd; p = 0.005 for uCd). After adjusting for age and sex, this difference also lost statistical significance (p = 0.729 for bCd; p = 0.539 for uCd). Urinary Cd concentrations were significantly higher among individuals who obtained > 50% of their rice from local sources (5.32 µg/g cr) than in those who did not (3.13 µg/g cr) (p = 0.017). However, this difference was not statistically significant after adjusting for age and sex (p = 0.285). Individuals residing within 2 km of the former smelter had significantly higher urinary Cd levels (5.49 µg/g cr) than those living > 2 km away (3.01 µg/g cr) (p = 0.005). However, this difference also lost statistical significance after age and sex adjustment (p = 0.138). Blood Pb and urinary iAs + MMA concentrations did not significantly differ by smoking status, alcohol consumption history, residential distance from the smelter, or local rice intake. Table 4 presents changes in heavy metal exposure by residential area and migration status among participants tested in both 2008 and 2020. Blood Pb levels were lower in 2020 than in 2008, regardless of residential area or migration status. Blood Cd levels were significantly lower in 2020 than in 2008 among residents living > 2 km from the smelter (p = 0.009), independent of migration status. In contrast, urinary Cd levels did not significantly differ by residential area. However, urinary Cd levels were significantly lower among residents who had migrated (p = 0.014) but not significantly different among those who remained in the same residence (p = 0.379). Tables 5 and 6 present the results of kidney function and bone density assessments evaluating the health effects of Cd exposure. Among participants assessed for Cd-related kidney damage, high NAG, high β2-MG, and low eGFR were observed in 16.2%, 29.7%, and 32.3%, respectively (Table 5). Osteoporosis was observed in 22.9% of participants evaluated for Cd-related bone demineralization (Table 6). However, the prevalence of abnormal findings did not significantly differ between individuals with urinary Cd levels above and below the reference standard.
Table 1.
Participant distribution in communities near former smelter sites based on epidemiological characteristics
| Characteristics | Total (N = 37) | |
|---|---|---|
| Age | < 69 | 3 (8.1) |
| 70–79 | 11 (29.7) | |
| ≥ 80 | 23 (62.2) | |
| Mean ± SD | 79.6 ± 8.35 | |
| Sex | Male | 11 (29.7) |
| Female | 26 (70.3) | |
| Duration of residence (years) | < 49 | 6 (16.2) |
| 50–69 | 18 (48.6) | |
| ≥ 70 | 13 (35.1) | |
| Mean ± SD | 62.9 ± 13.5 | |
| Distance from smelter, (km) | < 2.0 | 13 (35.1) |
| ≥ 2.0 | 24 (64.9) | |
| Smoking status | Non-smoker | 28 (75.7) |
| Smoker | 9 (24.3) | |
| Alcohol consumption | Non-drinker | 20 (54.1) |
| Drinker | 17 (45.9) | |
| Local rice consumption (%) | < 50 | 25 (67.6) |
| ≥ 50 | 12 (32.4) | |
| Drinking water source | Tap water/filter water | 37 (100) |
| Underground water | – | |
| Occupational smelter exposure | Yes | 14 (37.8) |
| No | 23 (62.2) |
Mean arithmetic mean, SD standard deviation
Table 2.
Mean metal concentrations among study participants
| Heavy metal | Sex | GM (GSD) | Range (min–max) | 95th percentile | *2008 survey | **KoNEHS IV |
|---|---|---|---|---|---|---|
| GM(GSD) | GM | |||||
| Blood Pb (µg/dL) | Male | 2.18 (1.56) | 1.12–3.76 | 3.26 | – | – |
| Female | 1.86 (1.76) | 0.50–3.73 | 2.83 | – | – | |
| Total | 1.95 (1.69) | 0.50–3.76 | 2.93 | 4.14 (1.54) | 1.51* | |
| Blood Cd (µg/L) | Male | 1.90 (1.62) | 0.59–3.46 | 2.43 | – | – |
| Female | 3.12 (1.66) | 1.36–7.85 | 4.05 | – | – | |
| Total | 2.68 (1.72) | 0.59–7.85 | 3.68 | 2.72 (1.95) | 0.39* | |
| Urine Cd (µg/L) | Male | 2.18 (1.92) | 0.82–5.14 | 3.89 | – | – |
| Female | 4.55 (1.66) | 1.66–12.66 | 6.22 | – | – | |
| Total | 3.66 (1.90) | 0.82–12.66 | 5.31 | 2.64 (1.77) | 0.71** | |
| Urinary Total As (µg/L) | Male | 186.8 (3.73) | 5.1–725.0 | 318.3 | – | – |
| Female | 157.5 (2.55) | 20.0–1,755.3 | 240.8 | – | – | |
| Total | 166.7 (2.84) | 5.1–1,755.3 | 285.0 | – | – | |
| iAs + MMA (µg/L) | Male | 1.11 (5.90) | 0.11–12.95 | 4.08 | – | – |
| Female | 0.94 (5.91) | 0.11–10.51 | 4.10 | – | – | |
| Total | 0.99 (6.10) | 0.11–12.95 | 4.08 | – |
GM geometric mean, GSD geometric standard deviation
*2008 survey (blood Pb, N = 562; urine Cd, N = 437; blood Cd, N = 557; urine As, N = 441)
*KoNEHS IV, Korean National Environmental Health Survey, 2018–2020
**KNHANES, Korea National Health and Nutrition Examination Survey. 2016–2018
Table 3.
Heavy metal concentrations in blood and urine stratified by smoking status, alcohol consumption, occupation smelter exposure, local rice consumption, and residential proximity to smelter
| Heavy metal | Smoking status | Alcohol consumption | Occupation smelter exposure | Local rice consumption | Residential proximity to smelter | ||||||
|---|---|---|---|---|---|---|---|---|---|---|---|
| Yes | No | Yes | No | Yes | No | Yes | No | < 2.0 km | ≥ 2.0 km | ||
| Blood Pb (µg/dL) | GM (GSD) | 2.24 (1.50) | 1.80 (1.65) | 1.80 (1.65) | 1.91 (1.72) | 2.07 (1.58) | 1.88 (1.78) | 1.80 (1.65) | 2.03 (1.73) | 2.10 (1.49) | 1.87 (1.82) |
| P-value | 0.378 | 0.527 | 0.601 | 0.527 | 0.547 | ||||||
| Blood Cd (µg/L) | GM (GSD) | 2.08 (1.35) | 2.98 (1.76) | 2.98 (1.76) | 3.19 (1.60) | 2.52 (1.55) | 2.79 (1.84) | 2.98 (1.76) | 2.54 (1.71) | 3.06 (1.64) | 2.49 (1.76) |
| P-value | 0.109 | 0.411 | 0.595 | 0.411 | 0.279 | ||||||
| Urinary Cd (µg/g cr) | GM (GSD) | 2.83 (1.88) | 5.32 (1.76) | 5.32 (1.76) | 4.91 (1.66) | 3.58 (2.00) | 3.84 (1.85) | 5.32 (1.76) | 3.13 (1.83) | 5.49 (1.58) | 3.01 (1.87) |
| P-value | 0.134 | 0.017 | 0.758 | 0.017 | 0.005 | ||||||
| Urinary Total As (µg/L) | GM(GSD) | 318.3 (2.43) | 150.7 (2.18) | 150.7 (2.18) | 135.9 (2.38) | 150.5 (3.92) | 175.7 (2.28) | 150.7 (2.18) | 174.5 (3.25) | 239.9 (2.19) | 135.6 (3.09) |
| P-value | 0.029 | 0.689 | 0.669 | 0.689 | 0.114 | ||||||
| iAs + MMA (µg/L) | GM (GSD) | 1.71 (6.15) | 1.88 (5.21) | 1.88 (5.21) | 1.04 (5.74) | 0.65 (6.70) | 1.31 (5.21) | 1.88 (5.21) | 0.72 (5.79) | 0.96 (6.69) | 1.03 (5.59) |
| P-value | 0.301 | 0.112 | 0.238 | 0.112 | 0.907 | ||||||
Mean arithmetic mean, SD standard deviation, GM geometric mean, GSD geometric standard deviation
Numbers in bold indicate significant differences (P < 0.05)
Table 4.
Geometric mean (GSD) concentrations of metals in urine and blood stratified by residential proximity and migration status (N = 28)
| Heavy metal | Year | Distance | Migration status | ||
|---|---|---|---|---|---|
| < 2 km | ≥ 2 km | Yes | No | ||
| Blood Pb (µg/dL) | 2008 | 4.93 (1.34) | 4.51 (1.43) | 4.45 (1.45) | 4.94 (1.34) |
| 2020 | 2.04 (1.50) | 1.88 (1.74) | 1.90 (1.72) | 2.00 (1.56) | |
| P-value | < 0.001 | < 0.001 | < 0.001 | < 0.001 | |
| Blood Cd (µg /dL) | 2008 | 3.93 (1.51) | 3.70 (1.73) | 3.53 (1.76) | 4.08 (1.49) |
| 2020 | 3.00 (1.67) | 2.70 (1.58) | 2.68 (1.63) | 2.97 (1.61) | |
| P-value | 0.129 | 0.009 | 0.028 | 0.044 | |
| Urine Cd (μg/g cr) | 2008 | 5.24 (1.30) | 4.55 (1.62) | 4.62 (1.67) | 5.05 (1.30) |
| 2020 | 5.32 (1.59) | 3.46 (1.87) | 3.24 (1.90) | 5.34 (1.53) | |
| P-value | 0.552 | 0.053 | 0.014 | 0.379 | |
GM geometric mean, GSD geometric standard deviation, cr creatinine
Numbers in bold indicate significant differences (P < 0.05)
Table 5.
Kidney function indices stratified by urinary cadmium levels
| Variable | < 5 μg/g cr (N = 26) | ≥ 5 μg/g cr (N = 11) | Total (N = 37) | Reference value | |
|---|---|---|---|---|---|
| NAG (U/g cr) | Mean ± SD | 9.20 ± 6.75 | 9.67 ± 3.70 | 9.34 ± 5.95 | < 11.5 |
| Αbnormal (%) | 4 (15.4%) | 2 (18.2%) | 6 (16.2%) | ||
| β2-MG (mg/g cr) | Mean ± SD | 0.43 ± 1.30 | 1.16 ± 3.18 | 0.79 ± 2.29 | < 0.3 |
| Αbnormal (%) | 5 (19.2%) | 4 (36.4%) | 11 (29.7%) | ||
| Egfr (mL/min) | Mean ± SD | 71.5 ± 22.7 | 70.5 ± 22.0 | 81.1 ± 21.2 | < 60 |
| Αbnormal (%) | 8 (30.7%) | 4 (36.4%) | 12 (32.3%) |
Mean arithmetic mean, SD standard deviation, NAG N-acetyl-β-D-glucosaminidase, β2-MG β2-microglobulin, eGFR estimated glomerular filtration rate, cr creatinine
Abnormal: ≥ Reference value
Table 6.
Bone mineral density stratified by urinary cadmium levels
| Variable | < 5 μg/g cr (N = 25) | ≥ 5 μg/g cr (N = 10) | Total (N = 35) | |
|---|---|---|---|---|
| Z-score (Spine) | Mean ± SD | 0.39 ± 1.76 | 0.70 ± 1.34 | 0.48 ± 1.64 |
| Z-score (Femur) | Mean ± SD | − 0.18 ± 0.40 | − 0.01 ± 0.63 | − 0.13 ± 0.47 |
| Osteoporosis | N (%) | 4 (16.0%) | 4 (40.0%) | 8 (22.9%) |
Mean arithmetic mean, SD standard deviation, cr creatinine
Osteoporosis: − 2.5 ≤ T-score
Discussion
The area surrounding the former Seo-Cheon Janghang Smelter and nearby abandoned metal mines is among the regions most vulnerable to environmental pollution in South Korea. [16, 21, 22]. Although the smelter ceased operations in 1989, controversy regarding its environmental effects has persisted. In 2008, a comprehensive environmental pollution survey was conducted, accompanied by a detailed health effect assessment of residents living near the smelter. The assessment revealed that residents were exposed to Pb, Cd, and As and were potentially at risk of adverse health effects such as kidney damage. Soil remediation and resident relocation projects were implemented following the studies mentioned above. However, ongoing health effects assessments reveal that residents remain exposed to high levels of environmental pollutants. The present study examined the exposure levels and health effects of residents who applied for environmental pollution damage relief in 2020. It also compared the 2020 data to those from 2008 and assessed heavy metal exposure levels in the general population. The average participant age was 79.6 years, with most having lived in the area while the smelter was in full operation.
To facilitate a clearer comparison of heavy metal exposure over time and across populations, Table 7 summarizes the average levels of blood Pb, blood Cd, and urinary Cd from the present study and previous national or regional surveys. The average blood Pb level in this study (1.95 µg/dL) was lower than that reported in the 2008 survey (4.14 µg/dL), with no participants exceeding the environmental exposure threshold of 5 µg/dL.
Table 7.
Comparison of blood and urinary heavy metal levels (Pb and Cd) between the present study and previous studies
| Study/Survey | Blood Pb (µg/dL) | Blood Cd (µg/L) | Urine Cd (µg/g cr) | Population | Year(s) |
|---|---|---|---|---|---|
| Present Study | 1.95 | 2.68 | 3.74 | Residents near smelter | 2020 |
| KoNEHS IV (Korea) | 1.51 | 0.71 | 0.39 | General Korean population | 2018–2020 |
| Abandoned Metal Mine Survey – Phase I | 2.84 | 1.59 | 2.23 | Residents near abandoned mine | 2008–2011 |
| Abandoned Metal Mine Survey – Phase II | 2.27 | 1.42 | 1.66 | Residents near abandoned mine | 2013–2017 |
| NHANES (U.S.) | 1.38 | 0.38 | 0.23 µg/L* | General population | 2017–2018 |
| JNHNS (Japan) | 1.77 | 0.58 | 0.58 µg/L* | General population | 2019 |
| CNHS (China) | 3.50 | 0.45 | 0.30 µg/L* | General population | 2018 |
KoNEHS IV Korea national environmental health survey, NHANES national health and nutrition examination survey, JNHNS Japan national health and nutrition survey, CNHS China national health survey
No participants in the present study had blood Pb concentrations exceeding the environmental exposure standard of 5 µg/dL. Blood Pb level did not differ significantly between participants employed as smelter workers and non-workers or between those who consumed locally grown rice and those who did not. Additionally, blood Pb levels did not significantly differ with lifestyle or residential area (Table 3). Analysis of participants measured in both 2008 and 2020 revealed a significant decline in blood Pb levels over time, regardless of residential area or migration status (Table 4). Comparing international populations, blood Pb levels in the present study were comparable to those in the US (1.38 µg/dL) and Japan (1.77 µg/dL) but lower than those in China (3.50 µg/dL) (Table 7) [23–25].
The mean blood Cd level was 2.68 µg/L, comparable to the 2008 level (2.64 µg/L) and consistently higher in females. This sex difference can be attributed to factors such as lifestyle differences, environmental exposure, and physiological characteristics [26]. No significant difference was observed in blood Cd level between smelter workers and non-workers or between participants who consumed locally grown rice and those who did not. Additionally, blood Cd levels did not significantly vary with lifestyle or residential area. Between 2008 and 2020, the mean blood Cd levels of residents within 2 km of the smelter remained significantly unchanged, while those of residents living > 2 km from the smelter decreased significantly. Levels in the study population exceeded those in the general populations of Korea, the US, Japan, and China (Table 7) [23–25, 27, 28]. Urinary Cd concentrations, adjusted for creatinine, were also elevated in this study (3.74 µg/g cr in 2020 vs. 2.72 µg/g cr in 2008), with 29.7% of participants exceeding the WHO reference value of 5 µg/g cr [29]. Creatinine adjustment of urinary Cd concentrations accounts for variations in urine dilution. Creatinine—a byproduct of muscle metabolism—is excreted in urine at a relatively constant rate. Normalizing urinary Cd concentrations to creatinine levels provides a more accurate assessment of cadmium exposure by minimizing the influence of variations in hydration status or urine volume [30]. This adjustment is crucial for standardizing measurements, thereby enhancing the reliability and comparability of Cd exposure assessments across individuals and populations [31]. In this survey, the urinary Cd concentrations in 32 participants (86.5%) exceeded the exposure threshold of 2.0 µg/g cr, a level recognized as indicative of cadmium-induced environmental pollution damage (Table 2) [32]. After adjusting for age and sex, no significant differences in urinary Cd concentrations were observed between participants who had worked at the smelter and those who had not, nor between those who consumed locally grown rice and those who did not. Moreover, urinary Cd concentration did not differ significantly by lifestyle factors or residential proximity. Analysis of multiple measurements revealed that urinary Cd concentrations significantly decreased in individuals who relocated, but no such change was observed in those who remained in that area (Table 3). These findings suggest that Cd exposure sources probably persisted within 2 km of the smelter and that relocating outside the affected area is associated with a significant reduction in exposure risk. Cd primarily accumulates in the liver and kidneys [33]. Blood and urinary Cd levels serve as indicators of current and cumulative exposures, respectively [6, 34, 35]. In this study, blood and urinary Cd levels remained high among residents living near the smelter. Multiple measurements revealed no significant change in blood Cd levels among those residing within 2 km of the smelter from 2008–2020. Hence, they were subjected to ongoing cadmium exposure. Urinary Cd concentrations did not significantly differ between 2008 and 2020 for residents living within 2 km of the smelter but were significantly lower in 2020 than in 2008 for those who relocated > 2 km away. In some residents, elevated urinary Cd concentrations probably indicate continued environmental Cd exposure rather than renal tubular damage and decreased Cd resorption. While the precise source of ongoing Cd exposure remains unclear, several potential environmental pathways warrant consideration. First, residual soil contamination near the smelter site represents a probable source, as Cd can persist in soil for decades and be absorbed by locally grown crops. Second, airborne dispersion of Cd-containing particulates from past smelter operations may have contributed to long-term environmental contamination, including household dust and surface water.
Environmental Cd exposure may cause renal tubular dysfunction [36]. Early signs of kidney damage include tubular dysfunction, characterized by the increased excretion of low-molecular-weight proteins such as β2-MG and NAG [37]. If left unchecked, early tubular damage can progress to more severe kidney damage. As early as 1950, decreased glomerular filtration rates were reported in cadmium-exposed workers [38]. eGFR—derived from blood cystatin C and creatinine levels—can be used to confirm the diagnosis of chronic kidney disease [20]. For both sexes, urinary Cd concentrations exhibited a positive correlation with NAG activity, β2-MG, and malondialdehyde levels, but these concentrations negatively correlated with eGFR and bone mineral density (BMD) values [37]. This present study demonstrated no significant correlation between urinary Cd exposure and the average values or proportions of individuals exceeding the threshold values for the kidney function indices mentioned (Table 5). No significant correlation was also observed between urinary Cd exposure and BMD or osteoporosis severity (Table 6).
In this study, total urinary As and hazardous As species—As3+ + As5+ + MMA—were separately quantified to assess As exposure. The total urinary and toxic As concentrations were 165.7 µg/L and 1.00 µg/L, respectively. A direct comparison between the 2008 and 2020 datasets was not feasible, as urinary arsenic concentrations in the earlier study (2008) were measured using AAS with the hydride generation technique.
The total As concentration measured in this study was higher than those reported in the recent Third Phase Health Effects Survey of Residents Around Abandoned Metal Mines (82.0–110.3 µg/L). Conversely, the concentration of toxic As levels reported in that survey (0.59–2.00 µg/L) is comparable to those observed in recent survey this present study. No significant differences in urinary As concentrations were observed between participants who had been employed at smelters and those who had not or between those who consumed locally grown rice and those who did not. Moreover, urinary As concentrations did not significantly vary according to lifestyle factors or residential area. Although the total arsenic concentrations observed in this study appeared somewhat elevated, comparable to those reported in other studies, the concentrations of hazardous arsenic species were not significantly different. These findings suggest that the elevated total arsenic levels are probably attributable to increased exposure to organic arsenic compounds, such as those derived from seafood consumption, rather than from environmental exposure to inorganic arsenic. Hence, dietary intake—especially of seafood—may have contributed significantly to the total urinary arsenic concentrations observed in this population [39, 40]. Supporting this interpretation, international comparisons reveal significant variability in urinary arsenic concentrations, probably reflecting differences in dietary patterns. For example, the average urinary arsenic concentration is 8.44 μg/L in the United States (NHANES 2017–2018) [23] and 10.5 μg/L in China (CNHS 2018) [25]. In Japan—where seafood consumption is relatively high—the average urinary arsenic concentration reaches 35.0 μg/L (JNHNS 2019) [24]. Arsenic—a metalloid or semimetal—is widely distributed throughout rocks, soil, water, and air. Inorganic As is commonly found in the groundwater sources consumed in countries such as Bangladesh, Chile, China, and other nations. Organic As compounds—such as arsenobetaine—are abundant in fish consumed by humans [40]. Arsenic is classified as a human carcinogen, with dietary intake recognized as the primary exposure route for the general population [41]. Mine tailings and other contaminated soils also represent potential sources of As exposure [42]. Soil measurement network data collected between 2014 and 2018 reported that the As levels do not exceed the established standards in any of the tested zones. Therefore, the soil remediation project implemented in the study area by the Ministry of the Environment was effective.
In this study, no significant differences in health outcomes, including renal impairment or osteoporosis, were observed based on cadmium exposure levels. This finding may be partially attributed to the relatively small sample size, which could have limited statistical power to detect meaningful associations. Furthermore, renal impairment may arise not only from heavy metal exposure, such as cadmium and arsenic, but also from underlying conditions, such as diabetes and hypertension. Given that most study participants were elderly and exhibited a high prevalence of these comorbidities, it became challenging to clearly distinguish renal effects specifically attributable to cadmium exposure. Regarding osteoporosis, the observed prevalence in this study was 22.9%, which is unexpectedly low considering the average participant age of 70 years. According to previous studies of the general Korean population, the prevalence of osteoporosis among individuals aged ≥ 50 years is approximately 22.4% [43]. The relatively low prevalence observed in this current study may be attributed to selection bias, as participation was voluntary and probably attracted individuals with relatively better overall health status.
This study has some limitations that should be considered. First, the relatively small sample size of 37 participants limited the generalizability of the findings. The absence of direct measurements of environmental factors, such as soil contamination or heavy metal concentrations in agricultural products, also limited our ability to ascertain specific exposure pathways. Variations in the analytical methodologies used to measure urinary cadmium concentrations may also affect the comparability of results. Nonetheless, a significant strength of this study is its longitudinal design, which was used to assess exposure levels in 28 participants at two-time points—2008 and 2020. This approach enabled the observation of temporal trends in cadmium exposure, offering valuable insights into the persistence of exposure despite remediation efforts.
The findings suggest that soil remediation efforts implemented since the closure of the Seo-Cheon Janghang Smelter in 1989 have significantly reduced overall heavy metal levels, particularly Pb and As exposure levels, in the vicinity of the facility. Conversely, the environmental Cd exposure risk remains relatively high within a 2-km radius of the smelter, raising concerns about declines in kidney function and BMD in the resident population. Therefore, continuous monitoring and appropriate compensation will be necessary for the affected individuals.
Acknowledgements
This work was supported by a Chung-Ang University Research Scholarship Grant in 2015.
Author contributions
All authors contributed to the study’s conception and design. Material preparation and data collection were performed by Da-Som Lee, Heon Kim, Yong-Dae Kim, Young-Seoub Hong, Jung-Duck Park, and Byung-Sun Choi. Data analysis was conducted by Jung-Eum Lee and Young-Hun Kim. The first draft of the manuscript was written by Young-Hun Kim and Da-Som Lee, with all authors providing comments on earlier versions of the manuscript. All authors read and approved the final manuscript.
Funding
This work was supported by a Chung-Ang University Research Scholarship Grant in 2015.
Data availability
The data supporting the findings of this study are available from the corresponding author upon reasonable request.
Declarations
Conflict of interest
The authors have no relevant financial or non-financial interests to disclose.
Ethical approval
Heavy metal exposure levels were evaluated in this study by collecting biological samples, such as blood and urine, with the consent of local residents. The study design received approval from the Chung-Ang University Institutional Review Board (CAUIRB) (Approval No. 1041078–202007-HRB-1731).
Consent to participate
Participants were informed of the purpose of this study. Those who wished to participate provided written consent.
Consent to publish
Participants were informed of the purpose of the present study. Those who wished to participate provided written consent.
Footnotes
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
References
- 1.Kříbek B, Majer V, Knesl I, Keder J, Mapani B, Kamona F et al (2016) Contamination of soil and grass in the Tsumeb smelter area, Namibia: Modeling of contaminants dispersion and ground geochemical verification. Appl Geochem 64:75–91. 10.1016/j.apgeochem.2015.07.006 [Google Scholar]
- 2.Adriano DC (2001) Trace elements in terrestrial environments: Biogeochemistry bioavailability, and risks of metals. Springer, New York [Google Scholar]
- 3.Jo H, Kim G, Chang J, Lee K, Lee C, Lee B (2021) Chronic exposure to lead and cadmium in residents living near a zinc smelter. Int J Environ Res Public Health 18:1731. 10.3390/ijerph18041731 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Du B, Zhou J, Lu B, Zhang C, Li D, Zhou J et al (2020) Environmental and human health risks from cadmium exposure near an active lead-zinc mine and a copper smelter. China Sci Total Environ 720:137585. 10.1016/j.scitotenv.2020.137585 [DOI] [PubMed] [Google Scholar]
- 5.Agency for Toxic Substances and Disease Registry (2022) Support document to the 2022 substance priority list. https://www.atsdr.cdc.gov/spl/resources/ATSDR-2022-SPL-Support-Document-508.pdf
- 6.Akter KF, Owens G, Davey DE, Naidu R (2005) Arsenic speciation and toxicity in biological systems. Rev Environ Contam Toxicol. 10.1007/0-387-27565-7_3 [DOI] [PubMed] [Google Scholar]
- 7.Bae H-S, Ryu D-Y, Choi B-S, Park J-D (2013) Urinary arsenic concentrations and their associated factors in Korean adults. Toxicol Res 29:137–142. 10.5487/TR.2013.29.2.137 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.International Agency for Research on Cancer (IARC) (2012) Arsenic and Arsenic Compounds. IARC Monogr Eval Carcinog Risks Hum 100C:41–93 [PMC free article] [PubMed] [Google Scholar]
- 9.Navas-Acien A et al (2005) Arsenic exposure and cardiovascular disease: a systematic review of the epidemiologic evidence. Am J Epidemiol 162:1037–1049 [DOI] [PubMed] [Google Scholar]
- 10.Agency for Toxic Substances and Disease Registry (ATSDR) (2020) Toxicological Profile for Lead. U.S. Department of Health and Human Services. https://stacks.cdc.gov/view/cdc/95222 [PubMed]
- 11.Health Canada. (2016) Third Report on Human Biomonitoring of Environmental Chemicals in Canada. https://www.canada.ca/en/health-canada/services/environmental-workplace-health/reports-publications/environmental-contaminants/third-report-human-biomonitoring-environmental-chemicals-canada.html
- 12.Health Canada. (2013) Second Report on Human Biomonitoring of Environmental Chemicals in Canada. https://www.canada.ca/en/health-canada/services/environmental-workplace-health/reports-publications/environmental-contaminants/second-report-human-biomonitoring-environmental-chemicals-canada-health-canada-2013.html
- 13.International Agency for Research on Cancer (IARC) (2006) Inorganic and Organic Lead Compounds. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans, Volume 87. Lyon, France: World Health Organization, International Agency for Research on Cancer. https://publications.iarc.fr/108
- 14.Agency for Toxic Substances and Disease Registry (2012) Toxicology profile for cadmium. https://www.atsdr.cdc.gov/toxprofiles/tp5.pdf [PubMed]
- 15.Jarup L, Akesson A (2009) Current status of cadmium as an environmental health problem. Toxicol Appl Pharmacol 238:201–208. 10.1016/j.taap.2009.04.020 [DOI] [PubMed] [Google Scholar]
- 16.Kim YD, Eom SY, Yim DH, Kim IS, Won HK, Park CH et al (2016) Environmental exposure to arsenic, lead, and cadmium in people living near Janghang copper smelter in Korea. J Korean Med Sci 31:489–496. 10.3346/jkms.2016.31.4.489 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.Jeong S, An JS, Kim YJ, Kim GH, Choi SI, Nam KP (2011) Study on heavy metal contamination characteristics and plant bioavailability for soils in the Janghang smelter area. J Soil Groundwater Environ 16:42–50 [Google Scholar]
- 18.Tchounwou PB, Yedjou CG, Patlolla AK, Sutton DJ (2012) Heavy metal toxicity and the environment. Exp Supp 101:133–164. 10.1007/978-3-7643-8340-4_6 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19.Bonsnes RW, Taussky HH (1945) On the colorimetric determination of creatinine by the jaffe reaction. J Biol Chem 158:581–591 [Google Scholar]
- 20.Inker LA, Schmid CH, Tighiouart H, Eckfeldt JH, Feldman HI, Greene T et al (2012) Estimating glomerular filtration rate from serum creatinine and cystatin. C N Engl J Med 367:20–29. 10.1056/NEJMoa1114248 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21.Park DU, Kim DS, Yu SD, Lee KM, Ryu SH, Kim SG et al (2014) Blood levels of cadmium and lead in residents near abandoned metal mine areas in Korea. Environ Monit Assess 186:5209–5220. 10.1007/s10661-014-3770-1 [DOI] [PubMed] [Google Scholar]
- 22.Moon JY, Eom SY, Seo JW, Lee JE, Choi BS, Kim H et al (2021) Effects of exposure to lead and cadmium on health of inhabitants of abandoned metal mine area in Korea. Arch Environ Contam Toxicol 80:490–498. 10.1007/s00244-021-00813-7 [DOI] [PubMed] [Google Scholar]
- 23.Centers for Disease Control and Prevention (2022) National Health and Nutrition Examination Survey 2017–2018. https://wwwn.cdc.gov/nchs/nhanes/continuousnhanes/default.aspx?BeginYear=2017
- 24.Ministry of Health, Labour, and Welfare (2020) The National Health and Nutrition Survey in Japan, 2019. https://www.mhlw.go.jp/stf/seisakunitsuite/bunya/kenkou_iryou/kenkou/eiyou/r1-houkoku_00002.html
- 25.He H, Pan L, Pa L, Cui Z, Ren X, Wang D et al (2018) Data resource profile: The China national health survey (CNHS). Int J Epidemiol 47:1734–1735. 10.1093/ije/dyy151 [DOI] [PubMed] [Google Scholar]
- 26.Vahter M, Akesson A, Lidén C, Ceccatelli S, Berglund M (2007) Gender differences in the disposition and toxicity of metals. Environ Res 104:85–95. 10.1016/j.envres.2006.08.003 [DOI] [PubMed] [Google Scholar]
- 27.KOSIS (Korean Statistical Information Service). Results of the Korean National Environmental Health Survey (KoNEHS) - Cadmium in Urine (Creatinine Adjusted) (2020) https://kosis.kr/statHtml/statHtml.do?orgId=106&tblId=DT_106N_99_1100058&vw_cd=MT_ZTITLE&list_id=106_002_002&scrId=&seqNo=&lang_mode=ko&obj_var_id=&itm_id=&conn_path=MT_ZTITLE&path=%252FstatisticsList%252FstatisticsListIndex.do. Accessed 23 Sept 2022
- 28.Korean Statistical Information Service. Blood lead levels. Updated 2022]. Accessed September 15, 2022]. https://kosis.kr/statHtml/statHtml.do?orgId=106&tblId=DT_106N_99_1100052&vw_cd=MT_OTITLE&list_id=106_002_002&scrId=&seqNo=&lang_mode=ko&obj_var_id=&itm_id=&conn_path=MT_OTITLE&path=%252FstatisticsList%252FstatisticsListIndex.do
- 29.WHO-IPCS, Cadmium. Environmental Health Criteria, vol. 134, World Health Organization, Geneva (1992) https://iris.who.int/bitstream/handle/10665/38998/9241571349-eng.pdf?sequence=1andisAllowed=y
- 30.Wang H, Dumont X, Haufroid V, Bernard A (2017) The physiological determinants of low-level urine cadmium: an assessment in a cross-sectional study among schoolchildren. Environ Health 16:99. 10.1186/s12940-017-0306-5 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 31.Ashizawa A, Faroon O, Ingerman L, Jenkins K, Tucker P, Wright S (2008) Draft toxicological profile for cadmium. https://stacks.cdc.gov/view/cdc/12391 [PubMed]
- 32.Lauwerys R, Bernard A, Buchet JP, Roels H, Bruaux P, Claeys F et al (1991) Does environmental exposure to cadmium represent a health risk? Conclusions from the Cadmibel study. Acta Clin Belg 46:219–225. 10.1080/17843286.1991.11718168 [DOI] [PubMed] [Google Scholar]
- 33.Thomas LD, Hodgson S, Nieuwenhuijsen M, Jarup L (2009) Early kidney damage in a population exposed to cadmium and other heavy metals. Environ Health Perspect 117:181–184. 10.1289/ehp.11641 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 34.Bernard A, Lauwerys R (1986) Effects of cadmium exposure in humans. In: Foulkes EC (ed) cadmium. Springer Nature, Berlin, pp 135–177 [Google Scholar]
- 35.Agency for Toxic Substances and Disease Registry (2007) Toxicology profile for cadmium. ATSDR Press. https://www.atsdr.cdc.gov/toxprofiles/tp2.pdf [PubMed]
- 36.Eom SY, Seo MN, Lee YS, Park KS et al (2017) Low-level environmental cadmium exposure induces kidney tubule damage in the general population of Korean adults. Arch Environ Contam Toxicol 73:401–439. 10.1007/s00244-017-0443-4 [DOI] [PubMed] [Google Scholar]
- 37.Li Y, Wang H, Yu J, Yan Q, Hu H, Zhang L et al (2020) An assessment of sensitivity biomarkers for urinary cadmium burden. BMC Nephrol 21:385. 10.1186/s12882-020-02036-9 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 38.Friberg L (1950) Health hazards in the manufacture of alkaline accumulators with special reference to chronic cadmium poisoning. A clinical and experimental study. Acta Med Scand Suppl 240:1–124 [PubMed] [Google Scholar]
- 39.Seo MN, Lee SG, Eom SY, Kim J, Oh SY, Kwon HJ et al (2016) Estimation of total and inorganic arsenic intake from the diet in Korean adults. Arch Environ Contam Toxicol 70:647–656. 10.1007/s00244-015-0257-1 [DOI] [PubMed] [Google Scholar]
- 40.Lee SG, Kang I, Seo MN, Lee JE, Eom SY, Hwang MS et al (2022) Exposure levels and contributing factors of various arsenic species and their health effects on Korean adults. Arch Environ Contam Toxicol 82:391–402. 10.1007/s00244-022-00913-y [DOI] [PubMed] [Google Scholar]
- 41.Akter KF, Owens G, Davey DE, Naidu R (2005) Arsenic speciation and toxicity in biological systems. Rev Environ Contam Toxicol 184:97–149. 10.1007/0-387-27565-7_3 [DOI] [PubMed] [Google Scholar]
- 42.Nikolaidis C, Orfanidis M, Hauri D, Mylonas S, Constantinidis T (2013) Public health risk assessment associated with heavy metal and arsenic exposure near an abandoned mine (Kirki, Greece). Int J Environ Health Res 23:507–519. 10.1080/09603123.2013.769202 [DOI] [PubMed] [Google Scholar]
- 43.Kim Y, Kim JH, Cho DS (2015) Gender difference in osteoporosis prevalence, awareness and treatment: based on the Korea national health and nutrition examination survey 2008–2011. J Korean Acad Nurs 45:293–305 [DOI] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
The data supporting the findings of this study are available from the corresponding author upon reasonable request.
