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Environmental exposures to lead, cadmium, and mercury and pterygium in Korean adults

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Abstract

Pterygium, one of the most common eye disorders, is an abnormal fibrovascular proliferation extending from the conjunctiva to the cornea. The mechanism of development in pterygium has not been fully elucidated; however, oxidative stress is suggested to be one of the major causes. Heavy metals such as lead (Pb), cadmium (Cd), and mercury (Hg) enter the human body and induce oxidative stress. However, no study has investigated the association of these heavy metals with pterygium. Therefore, this study aimed to evaluate the associations of environmental exposures to Pb, Cd, and Hg with pterygium in the Korean general adults. We analyzed data from 6,587 adults (≥ 20 years of age) who participated in the Korea National Health and Nutrition Examination Survey (KNHANES) 2008–2011. Pterygium was diagnosed as the presence of a wing-shaped fibrovascular growth. The exposures of Pb, Cd, and Hg were estimated by measuring blood concentrations. The prevalence of pterygium in this study population was 4.0% (348 subjects). After adjusting for potential confounders, the Pb level in blood was found to have a significant dose-dependent association with pterygium (p for trend = 0.001), and its highest quintile (vs. the lowest) had an odds ratio (OR) of 2.22 (95% CI: 1.30, 3.78) for pterygium. The Hg level in blood in the second quintile (vs. the lowest) had an OR of 1.64 (95% CI: 1.04, 2.59) for pterygium. In conclusion, this study suggests that environmental exposures to Pb and Hg in the Korean general adults may be related to the development of pterygium.

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Availability of data and materials

Both the data and analysis materials will be available online. Most of the data used in this study are freely available from the sources cited: https://knhanes.cdc.go.kr

References

  • ATSDR. 2015. Toxic substances portal-cadmium: public health statement for cadmium. Available: https://www.atsdr.cdc.gov/PHS/PHS.asp?id=46&tid=15

  • Balci M, Sahin S, Mutlu FM, Yagci R, Karanci P, Yildiz M (2011) Investigation of oxidative stress in pterygium tissue. Mol vis 17:443–447

    CAS  Google Scholar 

  • Barry V, Todd AC, Steenland K (2019) Bone lead associations with blood lead, kidney function and blood pressure among us, lead-exposed workers in a surveillance programme. Occup Environ Med 76:349–354

    Article  Google Scholar 

  • Bjorklund G, Crisponi G, Nurchi VM, Cappai R, Buha Djordjevic A, Aaseth J (2019) A review on coordination properties of thiol-containing chelating agents towards mercury, cadmium, and lead. Molecules 24

  • Bradley JC, Yang W, Bradley RH, Reid TW, Schwab IR (2010) The science of pterygia. Br J Ophthalmol 94:815–820

    Article  CAS  Google Scholar 

  • Branco V, Caito S, Farina M, Teixeira da Rocha J, Aschner M, Carvalho C (2017) Biomarkers of mercury toxicity: past, present, and future trends. J Toxicol Environ Health B Crit Rev 20:119–154

    Article  CAS  Google Scholar 

  • Choi YH, Park SK (2017) Environmental exposures to lead, mercury, and cadmium and hearing loss in adults and adolescents: KNHANES 2010–2012. Environ Health Perspect 125:067003

    Article  Google Scholar 

  • Coroneo MT, Di Girolamo N, Wakefield D (1999) The pathogenesis of pterygia. Curr Opin Ophthalmol 10:282–288

    Article  CAS  Google Scholar 

  • Di Girolamo N, Chui J, Coroneo MT, Wakefield D (2004) Pathogenesis of pterygia: role of cytokines, growth factors, and matrix metalloproteinases. Prog Retin Eye Res 23:195–228

    Article  CAS  Google Scholar 

  • Ekinci M, Ceylan E, Keles S, Cagatay HH, Apil A, Tanyildiz B et al (2014) Toxic effects of chronic mercury exposure on the retinal nerve fiber layer and macular and choroidal thickness in industrial mercury battery workers. Med Sci Monit 20:1284–1290

    Article  Google Scholar 

  • Elsir IT, Alrasheed SH (2018) Effect of prolonged and chronic occupational exposure to lead (pb) poison metal on anterior segments of the eye. Al-Basar International Journal of Ophthalmology 5:12

    Google Scholar 

  • EPA. 2019a. Lead: Learn about lead. Available: https://www.epa.gov/lead/protect-your-family-exposures-lead#sl-home [accessed 26 December 2019a]

  • EPA. 2019b. Mercury: How people are exposed to mercury. Available: https://www.epa.gov/mercury/how-people-are-exposed-mercury Accessed 26 Dec 2019b

  • Fadrowski JJ, Navas-Acien A, Tellez-Plaza M, Guallar E, Weaver VM, Furth SL (2010) Blood lead level and kidney function in us adolescents: the Third National Health and Nutrition Examination Survey. Arch Intern Med 170:75–82

    Article  CAS  Google Scholar 

  • Feng QY, Hu ZX, Song XL, Pan HW (2017) Aberrant expression of genes and proteins in pterygium and their implications in the pathogenesis. Int J Ophthalmol 10:973–981

    Google Scholar 

  • Flora G, Gupta D, Tiwari A (2012) Toxicity of lead: a review with recent updates. Interdiscip Toxicol 5:47–58

    Article  CAS  Google Scholar 

  • Gong Y, Fu Z, Liegl R, Chen J, Hellstrom A, Smith LE (2017) Omega-3 and omega-6 long-chain PUFAs and their enzymatic metabolites in neovascular eye diseases. Am J Clin Nutr 106:16–26

    Article  Google Scholar 

  • Hornung RW, Reed LD (1990) Estimation of average concentration in the presence of nondetectable values. Appl Occup Environ Hyg 5:46–51

    Article  CAS  Google Scholar 

  • Hu H, Shih R, Rothenberg S, Schwartz BS (2007) The epidemiology of lead toxicity in adults: measuring dose and consideration of other methodologic issues. Environ Health Perspect 115:455–462

    Article  CAS  Google Scholar 

  • Iraz M, Erdogan H, Ozyurt B, Ozugurlu F, Ozgocmen S, Fadillioglu E (2005) Omega-3 essential fatty acid supplementation and erythrocyte oxidant/antioxidant status in rats. Ann Clin Lab Sci 35:169–173

    CAS  Google Scholar 

  • Jarup L, Akesson A (2009) Current status of cadmium as an environmental health problem. Toxicol Appl Pharmacol 238:201–208

    Article  CAS  Google Scholar 

  • Jung SJ, Lee SH (2019) Association between three heavy metals and dry eye disease in Korean adults: results of the Korean National Health and Nutrition Examination Survey. Korean J Ophthalmol 33:26–35

    Article  Google Scholar 

  • Kasten-Jolly J, Pabello N, Bolivar VJ, Lawrence DA (2012) Developmental lead effects on behavior and brain gene expression in male and female BALB/cAnNTac mice. Neurotoxicology 33:1005–1020

    Article  CAS  Google Scholar 

  • Kasten-Jolly J, Lawrence DA (2017) Sex-specific effects of developmental lead exposure on the immune-neuroendocrine network. Toxicol Appl Pharmacol 334:142–157

    Article  CAS  Google Scholar 

  • KCDC (2009) Quality control and development of standardization manual for the medical laboratory tests in the national-wide health survey of 2008 year. Osong, Cheongju, Korea: Korea Center for Disease Control and Prevention

    Google Scholar 

  • KCDC (2010). Quality control and establishment of reference range for the clinical laboratory tests in the Fourth Korea National Health and Nutrition Examination Survey (KNHANES IV-3), 2009. Osong, Cheongju, Korea: Korea Center for Disease Control and Prevention

  • KCDC (2011) Quality control and examination of measurement traceability for the clinical laboratory tests in the national-wide health survey of the year of 2010. Osong, Cheongju, Korea: Korea Center for Disease Control and Prevention

  • KCDC (2012a) Korea health statistics 2011 : Korea National Health and Nutrition Examination Survey (KNHANES V-2). Osong, Cheongju, Korea: Korea Center for Disease Control and Prevention

  • KCDC (2012b) Korea health statistics 2008 : Korea National Health and Nutrition Examination Survey (KNHANES IV-2). Osong, Cheongju, Korea: Korea Center for Disease Control and Prevention

  • KCDC (2012c) KNHANES V (2010–2012c) Health examination guideline. Osong, Cheongju, Korea: Korea Center for Disease Control and Prevention

  • KCDC (2014a) KNHANES V (2010–2012) Analysis guideline. Osong, Cheongju, Korea: Korea Center for Disease Control and Prevention

  • KCDC (2014b) KNHANES IV (2007–2009) Analysis guideline. Osong, Cheongju, Korea: Korea Center for Disease Control and Prevention

  • Kilic-Toprak E, Toprak I, Caliskan S, Ozdemir Y, Demirtas O, Altintas F et al (2019) Oxidative stress and genotoxicity in pterygium: A systemic investigation. Eye Contact Lens 45:399–404

    Article  Google Scholar 

  • Lee KW, Choi Y-H, Hwang SH, Paik HJ, Kim MK, Wee WR et al (2017) Outdoor air pollution and pterygium in Korea. J Korean Med Sci 32:143

    Article  CAS  Google Scholar 

  • Lee SH, Kang EM, Kim GA, Kwak SW, Kim JM, Bae HW et al (2016a) Three toxic heavy metals in open-angle glaucoma with low-teen and high-teen intraocular pressure: a cross-sectional study from South Korea. PLoS One 11:e0164983

    Article  CAS  Google Scholar 

  • Lee W, Yoon JH, Roh J, Lee S, Seok H, Lee JH et al (2016b) The association between low blood lead levels and the prevalence of prehypertension among nonhypertensive adults in Korea. Am J Hum Biol 28:729–735

    Article  Google Scholar 

  • Lemire M, Fillion M, Frenette B, Mayer A, Philibert A, Passos CJ et al (2010) Selenium and mercury in the brazilian amazon: opposing influences on age-related cataracts. Environ Health Perspect 118:1584–1589

    Article  CAS  Google Scholar 

  • Lim CY, Kim SH, Chuck RS, Lee JK, Park CY (2015) Risk factors for pterygium in Korea: the Korean National Health and Nutrition Examination Survey V, 2010–2012. Medicine (Baltimore) 94:e1258

    Article  Google Scholar 

  • Lin W, Wang SL, Wu HJ, Chang KH, Yeh P, Chen CJ et al (2008) Associations between arsenic in drinking water and pterygium in southwestern Taiwan. Environ Health Perspect 116:952–955

    Article  CAS  Google Scholar 

  • Liu L, Wu J, Geng J, Yuan Z, Huang D (2013) Geographical prevalence and risk factors for pterygium: a systematic review and meta-analysis. BMJ Open 3:e003787

    Article  Google Scholar 

  • Lu P, Chen X, Kang Y, Ke L, Wei X, Zhang W (2007) Pterygium in Tibetans: a population-based study in China. Clin Exp Ophthalmol 35:828–833

    Article  Google Scholar 

  • Maxia C, Perra MT, Demurtas P, Minerba L, Murtas D, Piras F et al (2008) Expression of survivin protein in pterygium and relationship with oxidative DNA damage. J Cell Mol Med 12:2372–2380

    Article  CAS  Google Scholar 

  • Menke A, Muntner P, Batuman V, Silbergeld EK, Guallar E (2006) Blood lead below 0.48 micromol/L (10 μg/dL) and mortality among US adults. Circulation 114:1388–1394

  • Neal R, Cooper K, Gurer H, Ercal N (1998) Effects of N-acetylcysteine and 2,3-dimercaptosuccinic acid on lead induced oxidative stress in rat lenses. Toxicology 130:167–174

    Article  CAS  Google Scholar 

  • Oh SE, Kim GB, Hwang SH, Ha M, Lee KM (2017) Longitudinal trends of blood lead levels before and after leaded gasoline regulation in Korea. Environ Health Toxicol 32:e2017019

    Article  Google Scholar 

  • Oldenburg JB, Garbus J, McDonnell JM, McDonnell PJ (1990) Conjunctival pterygia. Mechanism of corneal topographic changes. Cornea 9:200–204

    Article  CAS  Google Scholar 

  • Ortak H, Demir HD, Mendil D, Sogut E, Ardagil A, Egri M (2012) Evaluation of iron, zinc, and copper levels in pterygium tissue. Jpn J Ophthalmol 56:219–223

    Article  CAS  Google Scholar 

  • Park SJ, Lee JH, Woo SJ, Kang SW, Park KH, Epidemiologic Survey Committee of Korean Ophthalmologic S (2015) Five heavy metallic elements and age-related macular degeneration: Korean National Health and Nutrition Examination Survey, 2008–2011. Ophthalmology 122:129–137

    Article  Google Scholar 

  • Passos CJ, Mergler D (2008) Human mercury exposure and adverse health effects in the Amazon: A review. Cad Saude Publica 24(Suppl 4):s503-520

    Article  Google Scholar 

  • Pereira P, Raimundo J, Barata M, Araujo O, Pousao-Ferreira P, Canario J et al (2015) A new page on the road book of inorganic mercury in fish body - tissue distribution and elimination following waterborne exposure and post-exposure periods. Metallomics 7:525–535

    Article  CAS  Google Scholar 

  • Pereira R, Guilherme S, Brandão F, Raimundo J, Santos MA, Pacheco M et al (2016) Insights into neurosensory toxicity of mercury in fish eyes stemming from tissue burdens, oxidative stress and synaptic transmission profiles. Mar Environ Res 113:70–79

    Article  CAS  Google Scholar 

  • Rhee SY, Hwang YC, Woo JT, Sinn DH, Chin SO, Chon S et al (2013) Blood lead is significantly associated with metabolic syndrome in Korean adults: an analysis based on the Korea National Health and Nutrition Examination Survey (KNHANES) 2008. Cardiovasc Diabetol 12:9

    Article  Google Scholar 

  • Rong SS, Peng Y, Liang YB, Cao D, Jhanji V (2014) Does cigarette smoking alter the risk of pterygium? A systematic review and meta-analysis. Invest Ophthalmol vis Sci 55:6235–6243

    Article  CAS  Google Scholar 

  • Schaumberg DA, Mendes F, Balaram M, Dana MR, Sparrow D, Hu H (2004) Accumulated lead exposure and risk of age-related cataract in men. JAMA 292:2750–2754

    Article  CAS  Google Scholar 

  • Sherwin JC, Hewitt AW, Kearns LS, Griffiths LR, Mackey DA, Coroneo MT (2013) The association between pterygium and conjunctival ultraviolet autofluorescence: the Norfolk Island eye study. Acta Ophthalmol 91:363–370

    Article  Google Scholar 

  • Somers EC, Ganser MA, Warren JS, Basu N, Wang L, Zick SM et al (2015) Mercury exposure and antinuclear antibodies among females of reproductive age in the United States: NHANES. Environ Health Perspect 123:792–798

    Article  CAS  Google Scholar 

  • Song P, Chang X, Wang M, An L (2017) Variations of pterygium prevalence by age, gender and geographic characteristics in China: A systematic review and meta-analysis. PLoS One 12:e0174587

    Article  CAS  Google Scholar 

  • Tan DTH, Chee S-P, Dear KBG, Lim ASM (1997) Effect of pterygium morphology on pterygium recurrence in a controlled trial comparing conjunctival autografting with bare sclera excision. JAMA Ophthalmology 115:1235–1240

    CAS  Google Scholar 

  • Threlfall TJ, English DR (1999) Sun exposure and pterygium of the eye: A dose-response curve. Am J Ophthalmol 128:280–287

    Article  CAS  Google Scholar 

  • Tsai YY, Cheng YW, Lee H, Tsai FJ, Tseng SH, Lin CL et al (2005) Oxidative DNA damage in pterygium. Mol vis 11:71–75

    CAS  Google Scholar 

  • Wang W, Schaumberg DA, Park SK (2016) Cadmium and lead exposure and risk of cataract surgery in U.S. Adults Int J Hyg Environ Health 219:850–856

    Article  CAS  Google Scholar 

  • Wang W, Moroi S, Bakulski K, Mukherjee B, Weisskopf MG, Schaumberg D et al (2018) Bone lead levels and risk of incident primary open-angle glaucoma: the VA Normative Aging Study. Environ Health Perspect 126:087002

    Article  Google Scholar 

  • WHO (2010) Ten chemicals of major public health concern. Available: https://www.who.int/ipcs/assessment/public_health/chemicals_phc/en/. Accessed 29 Dec 2019

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Funding

This study was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Korea Ministry of Science and Information and Communication Technology (ITC) (grant number 2020R1A2C110170311) and was additionally supported by the Gachon University Gil Medical Center (Grant number GCU-2016–5202) and the Korean Ministry of Environment under the “Environmental Health R&D Program” (Grant number 2021003310005). The funding sources played no role in the study design, data collection, data analysis, interpretation of results, or decisions made in the preparation and submission of the article.

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Author notes

  1. Dong Hyun Kim contributed equally to this study and should be considered as the co-corresponding author.

Authors and Affiliations

  1. Department of Preventive Medicine, Gachon University College of Medicine, Incheon, Korea

    Kyunghee Han, Min Jae Ju & Yoon-Hyeong Choi

  2. Department of Health Sciences and Technology, GAIHST, Gachon University, Incheon, Korea

    Min Jae Ju & Yoon-Hyeong Choi

  3. Department of Ophthalmology, Gil Medical Center, Gachon University College of Medicine, Incheon, Korea

    Dong Hyun Kim

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  1. Kyunghee Han
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Contributions

All authors participated in the literature search and interpretation of data. YC supervised the study. YC and DHK participated in designing the study. KH participated in making the figures, data collection, data analysis, and draft writing. KH, MJJ, and DHK participated in intellectual review.

Corresponding author

Correspondence to Yoon-Hyeong Choi.

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Ethics approval and consent to participate

This study was approved by the Institutional Review Board of the KCDC (IRB No. 2008-04EXP-01-C in 2008; 2009-01CON-03-2C in 2009; 2010-02CON-21-C in 2010; 2011-02CON-06-C in 2011). All participants provided written informed consent.

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All authors declare no competing interests.

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Responsible editor: Lotfi Aleya

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Han, K., Ju, M.J., Kim, D.H. et al. Environmental exposures to lead, cadmium, and mercury and pterygium in Korean adults. Environ Sci Pollut Res 29, 55058–55068 (2022). https://doi.org/10.1007/s11356-022-19250-7

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