Abstract
The purpose of this study was to evaluate lead exposure and its relationship with serum levels of predictive CVD biomarkers [asymmetric dimethylarginine (ADMA), adipocyte fatty acid-binding protein (FABP4), adiponectin, and chemerin] in women living in San Luis Potosi, Mexico. A mean blood lead level (BLL) of 11.5 ± 9.00 μg/dL (mean ± standard deviation) was found after all blood samples were analyzed. Regarding serum predictive CVD biomarkers, mean serum level of 0.68 ± 0.38 μmol/L, 20.5 ± 16.5 ng/mL, 12.5 ± 3.30 μg/mL, and 255 ± 130 ng/mL were found for ADMA, FABP4, adiponectin, and chemerin, respectively. Simple significant associations (Pearson´s correlations) between BLL and ADMA (r = 0.17; p = 0.04) and FABP4 (r = 0.23; p = 0.03) were found. Furthermore, a multivariate linear regression model showed that BLL was a significant predictor of serum ADMA (β = 0.06; p = 0.001) and FABP4 (β = 1.75; p = 0.0004) concentrations after adjusting by confounders. For serum chemerin and adiponectin levels, no associations were found with BLL. In conclusion, high serum ADMA and FABP4 (predictive CVD biomarkers) levels were found in women exposed to lead. Consequently, this research can be used as a point of departure for the prevention of CVD events in populations living in sites environmentally impacted with lead.
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References
Alissa EM, Ferns GA (2011) Heavy metal poisoning and cardiovascular disease. J Toxicol 2011:870125. https://doi.org/10.1155/2011/870125
Arbuckle TE, Liang CL, Morisset A-S et al (2016) Maternal and fetal exposure to cadmium, lead, manganese and mercury: the MIREC study. Chemosphere 163:270–282. https://doi.org/10.1016/j.chemosphere.2016.08.023
Bao Y, Lu Z, Zhou M et al (2011) Serum levels of adipocyte fatty acid-binding protein are associated with the severity of coronary artery disease in Chinese women. PLoS ONE 6:e19115. https://doi.org/10.1371/journal.pone.0019115
Barquera S, Campos-Nonato I, Hernández-Barrera L et al (2013) Prevalencia de obesidad en adultos mexicanos, ENSANUT 2012. Salud Publica Mex 55:151–160
Baum C, Johannsen SS, Zeller T et al (2016) ADMA and arginine derivatives in relation to non-invasive vascular function in the general population. Atherosclerosis 244:149–156. https://doi.org/10.1016/j.atherosclerosis.2015.10.101
Becker K, Schroeter-Kermani C, Seiwert M et al (2013) German health-related environmental monitoring: assessing time trends of the general population’s exposure to heavy metals. Int J Hyg Environ Health 216:250–254. https://doi.org/10.1016/j.ijheh.2013.01.002
Böger RH, Maas R, Schulze F, Schwedhelm E (2009a) Asymmetric dimethylarginine (ADMA) as a prospective marker of cardiovascular disease and mortality—an update on patient populations with a wide range of cardiovascular risk. Pharmacol Res 60:481–487. https://doi.org/10.1016/j.phrs.2009.07.001
Böger RH, Sullivan LM, Schwedhelm E et al (2009b) Plasma asymmetric dimethylarginine and incidence of cardiovascular disease and death in the community. Circulation 119:1592–1600
Borja-Aburto VH, Hertz-Picciotto I, Rojas Lopez M et al (1999) Blood lead levels measured prospectively and risk of spontaneous abortion. Am J Epidemiol 150:590–597
Bouras G, Deftereos S, Tousoulis D et al (2013) Asymmetric dimethylarginine (ADMA): a promising biomarker for cardiovascular disease? Curr Top Med Chem 13:180–200
Braun JM, Wright RJ, Just AC et al (2014) Relationships between lead biomarkers and diurnal salivary cortisol indices in pregnant women from Mexico City: a cross-sectional study. Environ Health 13:50. https://doi.org/10.1186/1476-069X-13-50
Burroughs Pena MS, Rollins A (2017) Environmental exposures and cardiovascular disease: a challenge for health and development in low- and middle-income countries. Cardiol Clin 35:71–86. https://doi.org/10.1016/j.ccl.2016.09.001
Černá M, Krsková A, Čejchanová M, Spěváčková V (2012) Human biomonitoring in the Czech Republic: an overview. Int J Hyg Environ Health 215:109–119. https://doi.org/10.1016/j.ijheh.2011.09.007
Choi W, Kim S, Baek Y-W et al (2016) Exposure to environmental chemicals among Korean adults-updates from the second Korean National Environmental Health Survey (2012–2014). Int J Hyg Environ Health. https://doi.org/10.1016/j.ijheh.2016.10.002
Chow WS, Tso AWK, Xu A et al (2013) Elevated circulating adipocyte-fatty acid binding protein levels predict incident cardiovascular events in a community-based cohort: a 12-year prospective study. J Am Heart Assoc 2:e004176. https://doi.org/10.1161/JAHA.112.004176
Diaz-Barriga F, Santos MA, Mejia JJ et al (1993) Arsenic and cadmium exposure in children living near a smelter complex in San Luis Potosi, Mexico. Environ Res 62:242–250
Estrada-Sanchez D, Ericson B, Juarez-Perez CA et al (2017) Intelligence quotient loss in Mexican pottery artisan’s children. Rev Med Inst Mex Seguro Soc 55:292–299
Furuhashi M, Ishimura S, Ota H et al (2011) Serum fatty acid-binding protein 4 is a predictor of cardiovascular events in end-stage renal disease. PLoS ONE 6:e27356. https://doi.org/10.1371/journal.pone.0027356
Furuhashi M, Saitoh S, Shimamoto K, Miura T (2014) Fatty acid-binding protein 4 (FABP4): pathophysiological Insights and potent clinical biomarker of metabolic and cardiovascular diseases. Clin Med Insights Cardiol 8:23–33. https://doi.org/10.4137/CMC.S17067
Gambelunghe A, Sallsten G, Borne Y et al (2016) Low-level exposure to lead, blood pressure, and hypertension in a population-based cohort. Environ Res 149:157–163. https://doi.org/10.1016/j.envres.2016.05.015
Garrido Latorre F, Hernandez-Avila M, Tamayo Orozco J et al (2003) Relationship of blood and bone lead to menopause and bone mineral density among middle-age women in Mexico City. Environ Health Perspect 111:631–636
Hao Y, Ma X, Luo Y et al (2014) Serum adipocyte fatty acid binding protein levels are positively associated with subclinical atherosclerosis in Chinese pre- and postmenopausal women with normal glucose tolerance. J Clin Endocrinol Metab 99:4321–4327. https://doi.org/10.1210/jc.2014-1832
Hsu C-P, Lin S-J, Chung M-Y, Lu T-M (2012) Asymmetric dimethylarginine predicts clinical outcomes in ischemic chronic heart failure. Atherosclerosis 225:504–510. https://doi.org/10.1016/j.atherosclerosis.2012.09.040
Hsu C-P, Hsu P-F, Chung M-Y et al (2014) Asymmetric dimethylarginine and long-term adverse cardiovascular events in patients with type 2 diabetes: relation with the glycemic control. Cardiovasc Diabetol 13:156. https://doi.org/10.1186/s12933-014-0156-1
Iii ATP, Quick GA, Reference D (2001) ATP III guidelines At-A-glance quick desk reference. Natl Inst Heal 329:211. https://doi.org/10.1016/j.bbrc.2005.02.046
Inan B, Ates I, Ozkayar N et al (2016) Are increased oxidative stress and asymmetric dimethylarginine levels associated with masked hypertension? Clin Exp Hypertens 38:294–298. https://doi.org/10.3109/10641963.2015.1089883
James Pa, Oparil S, Carter BL et al (2013) 2014 evidence-based guideline for the management of high blood pressure in adults. JAMA 1097:1–14. https://doi.org/10.1001/jama.2013.284427
Jasso-Pineda Y, Diaz-Barriga F, Yanez-Estrada L et al (2015) DNA damage in Mexican children living in high-risk contaminated scenarios. Sci Total Environ 518–519:38–48. https://doi.org/10.1016/j.scitotenv.2015.02.073
Kim S-A, Kim K-S, Lee Y-M et al (2015) Associations of organochlorine pesticides and polychlorinated biphenyls with total, cardiovascular, and cancer mortality in elders with differing fat mass. Environ Res 138:1–7. https://doi.org/10.1016/j.envres.2015.01.021
Krzyzanowska K, Mittermayer F, Wolzt M, Schernthaner G (2007) Asymmetric dimethylarginine predicts cardiovascular events in patients with type 2 diabetes. Diab Care 30:1834–1839. https://doi.org/10.2337/dc07-0019
La-Llave-Leon O, Lugo-Soto R, Aguilar-Duran M et al (2015) Relationship between blood lead levels and hematological indices in pregnant women. Women Health 55:90–102. https://doi.org/10.1080/03630242.2014.972019
La-Llave-León O, Estrada-Martínez S, Manuel Salas-Pacheco J et al (2011) Blood lead levels and risk factors in pregnant women from durango, Mexico. Arch Environ Occup Health 66:107–113. https://doi.org/10.1080/19338244.2010.511311
Leong T, Zylberstein D, Graham I et al (2008) Asymmetric dimethylarginine independently predicts fatal and nonfatal myocardial infarction and stroke in women: 24-Year follow-up of the population study of women in Gothenburg. Arterioscler Thromb Vasc Biol 28:961–967. https://doi.org/10.1161/ATVBAHA.107.156596
Ljunggren SA, Helmfrid I, Salihovic S et al (2014) Persistent organic pollutants distribution in lipoprotein fractions in relation to cardiovascular disease and cancer. Environ Int 65:93–99. https://doi.org/10.1016/j.envint.2013.12.017
Lluch P, Segarra G, Medina P (2015) Asymmetric dimethylarginine as a mediator of vascular dysfunction in cirrhosis. World J Gastroenterol 21:9466–9475. https://doi.org/10.3748/wjg.v21.i32.9466
Lu T-M, Chung M-Y, Lin M-W et al (2011) Plasma asymmetric dimethylarginine predicts death and major adverse cardiovascular events in individuals referred for coronary angiography. Int J Cardiol 153:135–140. https://doi.org/10.1016/j.ijcard.2011.06.120
Lukkhananan P, Thawonrachat N, Srihirun S et al (2015) Endothelial dysfunction in subjects with chronic cadmium exposure. J Toxicol Sci 40:605–613. https://doi.org/10.2131/jts.40.605
Maeda S, Miyaki A, Kumagai H et al (2013) Lifestyle modification decreases arterial stiffness and plasma asymmetric dimethylarginine level in overweight and obese men. Coron Artery Dis 24:583–588. https://doi.org/10.1097/MCA.0b013e3283647a99
Mastin JP (2005) Environmental cardiovascular disease. Cardiovasc Toxicol 5:91–94
McCarty MF (2016) Asymmetric dimethylarginine is a well established mediating risk factor for cardiovascular morbidity and mortality—should patients with elevated levels be supplemented with citrulline? Healthc (Basel, Switzerland) 4:1–12. https://doi.org/10.3390/healthcare4030040
NHANES IV (2009) Fourth national report on human exposure to environmental chemicals. Department of Health and Human Services Centers for Disease Control and Prevention, Atlanta
Nigra AE, Ruiz-Hernandez A, Redon J et al (2016) Environmental metals and cardiovascular disease in adults: a systematic review beyond lead and cadmium. Curr Environ Heal Rep 3:416–433. https://doi.org/10.1007/s40572-016-0117-9
Nisse C, Tagne-Fotso R, Howsam M et al (2017) Blood and urinary levels of metals and metalloids in the general adult population of Northern France: the IMEPOGE study, 2008–2010. Int J Hyg Environ Health 220:341–363. https://doi.org/10.1016/j.ijheh.2016.09.020
Ochoa-Martinez AC, Orta-Garcia ST, Rico-Escobar EM et al (2016) Exposure assessment to environmental chemicals in children from Ciudad Juarez, Chihuahua, Mexico. Arch Environ Contam Toxicol 70:657–670. https://doi.org/10.1007/s00244-016-0273-9
Ochoa-Martinez AC, Ruiz-Vera T, Almendarez-Reyna CI et al (2017a) Influence on serum asymmetric dimethylarginine (ADMA) concentrations of human paraoxonase 1 polymorphism (Q192R) and exposure to polycyclic aromatic hydrocarbons (PAHs) in Mexican women, a gene-environment interaction. Chemosphere 186:770–779. https://doi.org/10.1016/j.chemosphere.2017.08.055
Ochoa-Martinez AC, Ruiz-Vera T, Orta-Garcia ST et al (2017b) Association between Q192R paraoxonase 1 polymorphism and serumadipocyte-fatty acid binding protein (FABP4) levels in Mexican women. Ann Hum Biol 44:389–391. https://doi.org/10.1080/03014460.2016.1245785
Ochoa-Martinez AC, Ruiz-Vera T, Pruneda-Alvarez LG et al (2017c) Serum adipocyte-fatty acid binding protein (FABP4) levels in women from Mexico exposed to polycyclic aromatic hydrocarbons (PAHs). Environ Sci Pollut Res Int 24:1862–1870. https://doi.org/10.1007/s11356-016-7971-8
Osorio-Yanez C, Ayllon-Vergara JC, Aguilar-Madrid G et al (2013) Carotid intima-media thickness and plasma asymmetric dimethylarginine in Mexican children exposed to inorganic arsenic. Environ Health Perspect 121:1090–1096. https://doi.org/10.1289/ehp.1205994
Perez-Maldonado IN, Ochoa-Martinez AC, Orta-Garcia ST et al (2017) Concentrations of environmental chemicals in urine and blood samples of children from San Luis Potosi, Mexico. Bull Environ Contam Toxicol 99:258–263. https://doi.org/10.1007/s00128-017-2130-6
Perez-Vazquez MS, Ochoa-Martinez AC, RuIz-Vera T et al (2017) Evaluation of epigenetic alterations (mir-126 and mir-155 expression levels) in Mexican children exposed to inorganic arsenic via drinking water. Environ Sci Pollut Res Int. https://doi.org/10.1007/s11356-017-0367-6
Prokopowicz A, Sobczak A, Szula-Chraplewska M et al (2016) Effect of occupational exposure to lead on new risk factors for cardiovascular diseases. Occup Environ Med. https://doi.org/10.1136/oemed-2016-103996
Pruneda-Alvarez LG, Perez-Vazquez FJ, Ruiz-Vera T et al (2016a) Urinary 1-hydroxypyrene concentration as an exposure biomarker to polycyclic aromatic hydrocarbons (PAHs) in Mexican women from different hot spot scenarios and health risk assessment. Environ Sci Pollut Res Int 23:6816–6825. https://doi.org/10.1007/s11356-015-5918-0
Pruneda-Alvarez LG, Ruíz-Vera T, Ochoa-Martínez AC et al (2016b) Plasma asymmetric dimethylarginine (ADMA) levels in Mexican women exposed to polycyclic aromatic hydrocarbons (PAHs): a preliminary study. Sci Total Environ 572:1195–1202. https://doi.org/10.1016/j.scitotenv.2016.08.037
Pruneda-Álvarez LG, Pérez-Vázquez FJ, Salgado-Bustamante M et al (2012) Exposure to indoor air pollutants (polycyclic aromatic hydrocarbons, toluene, benzene) in Mexican indigenous women. Indoor Air 22:140–147. https://doi.org/10.1111/j.1600-0668.2011.00750.x
Reiser H, Klingenberg R, Hof D et al (2015) Circulating FABP4 is a prognostic biomarker in patients with acute coronary syndrome but not in asymptomatic individuals. Arterioscler Thromb Vasc Biol 35:1872–1879. https://doi.org/10.1161/ATVBAHA.115.305365
Rodriguez-Calvo R, Girona J, Alegret JM et al (2017) Role of the fatty acid binding protein 4 in heart failure and cardiovascular disease. J Endocrinol. https://doi.org/10.1530/JOE-17-0031
Ruiz-Vera T, Pruneda-Álvarez LG, Ochoa-Martínez ÁC et al (2015a) Assessment of vascular function in Mexican women exposed to polycyclic aromatic hydrocarbons from wood smoke. Environ Toxicol Pharmacol 40:423–429. https://doi.org/10.1016/j.etap.2015.07.014
Ruiz-Vera T, Pruneda-Alvarez LG, Perez-Vazquez FJ et al (2015b) Using urinary 1-hydroxypyrene concentrations to evaluate polycyclic aromatic hydrocarbon exposure in women using biomass combustion as main energy source. Drug Chem Toxicol 38:349–354. https://doi.org/10.3109/01480545.2014.968932
Schnabel R, Blankenberg S, Lubos E et al (2005) Asymmetric dimethylarginine and the risk of cardiovascular events and death in patients with coronary artery disease: results from the AtheroGene Study. Circ Res 97:e53–e59. https://doi.org/10.1161/01.RES.0000181286.44222.61
Schober SE, Mirel LB, Graubard BI et al (2006) Blood lead levels and death from all causes, cardiovascular disease, and cancer: results from the NHANES III mortality study. Environ Health Perspect 114:1538–1541. https://doi.org/10.1289/ehp.9123
Sciacqua A, Grillo N, Quero M et al (2012) Asymmetric dimethylarginine plasma levels and endothelial function in newly diagnosed type 2 diabetic patients. Int J Mol Sci 13:13804–13815. https://doi.org/10.3390/ijms131113804
Shibata R, Ouchi N, Ohashi K, Murohara T (2017) The role of adipokines in cardiovascular disease. J Cardiol. https://doi.org/10.1016/j.jjcc.2017.02.006
Trejo-Acevedo A, Diaz-Barriga F, Carrizales L et al (2009) Exposure assessment of persistent organic pollutants and metals in Mexican children. Chemosphere 74:974–980. https://doi.org/10.1016/j.chemosphere.2008.10.030
Tripepi G, Mattace Raso F, Sijbrands E et al (2011) Inflammation and asymmetric dimethylarginine for predicting death and cardiovascular events in ESRD patients. Clin J Am Soc Nephrol 6:1714–1721. https://doi.org/10.2215/CJN.11291210
Tuuri AL, Jauhiainen MS, Tikkanen MJ, Kaaja RJ (2017) Systolic blood pressure and fatty acid-binding protein 4 predict pregnancy-induced hypertension in overweight nulliparous women. Placenta 35:797–801. https://doi.org/10.1016/j.placenta.2014.07.016
von Eynatten M, Breitling LP, Roos M et al (2012) Circulating adipocyte fatty acid-binding protein levels and cardiovascular morbidity and mortality in patients with coronary heart disease: a 10-year prospective study. Arterioscler Thromb Vasc Biol 32:2327–2335. https://doi.org/10.1161/ATVBAHA.112.248609
Yan Q, Zhang Y, Hong J et al (2012) The association of serum chemerin level with risk of coronary artery disease in Chinese adults. Endocrine 41:281–288. https://doi.org/10.1007/s12020-011-9550-6
Yanez L, Garcia-Nieto E, Rojas E et al (2003) DNA damage in blood cells from children exposed to arsenic and lead in a mining area. Environ Res 93:231–240
Yu H-P, Jen H-L, Yin W-H, Wei J (2017) Circulating adiponectin levels following treatment can predict late clinical outcomes in chronic heart failure. Acta Cardiol Sin 33:139–149
Zaciragic A, Huskic J, Mulabegovic N et al (2014) An assessment of correlation between serum asymmetric dimethylarginine and glycated haemoglobin in patients with type 2 diabetes mellitus. Bosn J Basic Med Sci 14:21–24
Zeliger HI (2013) Lipophilic chemical exposure as a cause of cardiovascular disease. Interdiscip Toxicol 6:55–62. https://doi.org/10.2478/intox-2013-0010
Zhang Y, Zhang H, Lu J et al (2016) Changes in serum adipocyte fatty acid-binding protein in women with gestational diabetes mellitus and normal pregnant women during mid- and late pregnancy. J Diabetes Investig 7:797–804. https://doi.org/10.1111/jdi.12484
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This work was supported by CONACyT (Grant CONACyT- PDCPN2015-1558 and Fondo Sectorial SEMARNAT–CONACYT-249421). Special Thanks to Miss Laura Carmen Martinez for English language editing.
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Ochoa-Martínez, Á.C., Cardona-Lozano, E.D., Carrizales-Yáñez, L. et al. Serum Concentrations of New Predictive Cardiovascular Disease Biomarkers in Mexican Women Exposed to Lead. Arch Environ Contam Toxicol 74, 248–258 (2018). https://doi.org/10.1007/s00244-017-0491-9
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DOI: https://doi.org/10.1007/s00244-017-0491-9