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Exposure to polycyclic aromatic hydrocarbon mixtures and early kidney damage in Mexican indigenous population

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Abstract

The traditions and habits of indigenous communities in México include the use of wood and biomass burning to cook their food, which generates large amounts of smoke and therefore pollution inside the households. This smoke is composed of a complex mixture of polycyclic aromatic hydrocarbons (PAHs) which at high levels of exposure cause carcinogenic, genotoxic effects and some chronic pulmonary and cardiovascular diseases; however, few studies relate kidney health with exposure to PAHs. Thus, the aim of this study was the evaluation of 10 hydroxylated metabolites of PAHs (OH-PAHs), and their correlation with biomarkers of early kidney damage renal (cystatin-C (Cys-C)), osteopontin (OPN), retinol-binding protein-4 (RPB-4), and neutrophil gelatinase-associated lipocalin (NGAL) in the indigenous population of the Huasteca Potosina in Mexico. The results demonstrate the presence of the OH-PAHs and kidney damage biomarkers in 100% of the study population. The OH-PAHs were shown in the following order of frequency, 1-OH-PYR > 4-OH-PHE > 2-OH-NAP > 1-OH-NAP > 9-OH-FLU > 3-OH-FLU > 2-OH-FLU > 3-OH-PHE and with the following percentages of detection 97.6, 87.8, 78, 73.2, 68.3, 31.7, 14.6, and 12.2%, respectively. NGAL and RBP-4 were present in above 85% of the population, with mean concentrations of 78.5 ± 143.9 and 139.4 ± 131.7 ng/g creatinine, respectively, OPN (64%) with a mean concentration of 642.6 ± 723.3 ng/g g creatinine, and Cys-C with a mean concentration of 33.72 ± 44.96 ng/g creatinine. Correlations were found between 1-OH-NAP, 2-OH-NAP, 9-OH-FLU, and 4-OH-PHE and the four biomarkers of early kidney damage. 3-OH-FLU with OPN and 1-OH-PYR correlated significantly with NGAL, OPN, and RPB-4.

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References

  • Alomirah H, Al-Zenki S, Al-Hooti S, Zaghloul S, Sawaya W, Ahmed N, Kannan K (2011) Concentrations and dietary exposure to polycyclic aromatic hydrocarbons (PAHs) from grilled and smoked foods. Food Control 22:2028–2035

    Article  CAS  Google Scholar 

  • Arias AH, Villalón TR, Orazi M, Ronda AC, Marcovecchio J (2019) Hidrocarburos Aromáticos Policíclicos (HAPs) en ambientes marinos: Una revisión de América. JAINA, Costas y Mares ante el Cambio Climático 1:19–40

    Google Scholar 

  • Agency For Toxic Substances And Disease Registry (ATSDR) (1995) Toxicological profile for polycyclic aromatic hydrocarbons (PAHs). Atlanta, GA

    Google Scholar 

  • Avogbe PH, Ayi-Fanou L, Autrup H, Loft S, Fayomi B, Sanni A, Vinzents P, Møller P (2005) Ultrafine particulate matter and high-level benzene urban air pollution in relation to oxidative DNA damage. Carcinogenesis 26:613–620

    Article  CAS  Google Scholar 

  • Bagshaw SM, Bellomo R (2010) Cystatin C in acute kidney injury. Curr Opin Crit Care 16:533–539

    Article  Google Scholar 

  • Balmes JR, Eisen EA (2018) Household air pollution and chronic obstructive pulmonary disease. “A riddle, wrapped in a mystery, inside an enigma.” Am J Respir Crit Care Med 197:547–548

  • Bhargava A, Khanna R, Bhargava S, Kumar S (2004) Exposure risk to carcinogenic PAHs in indoor-air during biomass combustion whilst cooking in rural India. Atmos Environ 38:4761–4767

    Article  CAS  Google Scholar 

  • Blaszczyk E, Rogula-Kozlowska W, Klejnowski K, Fulara I, Mielzynska-Svach D (2017) Polycyclic aromatic hydrocarbons bound to outdoor and indoor airborne particles (PM2.5) and their mutagenicity and carcinogenicity in Silesian kindergartens, Poland. Air Qual Atmos Health 10:389–400

    Article  CAS  Google Scholar 

  • Cardenas-Gonzalez M, Osorio-Yanez C, Gaspar-Ramirez O, Pavkovic M, Ochoa-Martinez A, Lopez-Ventura D, Medeiros M, Barbier OC, Perez-Maldonado IN, Sabbisetti VS, Bonventre JV, Vaidya VS (2016) Environmental exposure to arsenic and chromium in children is associated with kidney injury molecule-1. Environ Res 150:653–662

    Article  CAS  Google Scholar 

  • Cárdenas JAG, Santiago OG, Soto MTM, Ocañas LG, Ulloa HG (2020): Capítulo 4. Hidrocarburos aromáticos policíclicos (HAPs) de impacto en salud presentes en el aire del área metropolitana de Monterrey, Bienestar y Salud Social. Tendencias, Nuevo León, México, pp 79

  • CDC (2013) Monohydroxy-Polycyclic Aromatic Hydrocarbons (OH-PAHs) in urine by Isotope Dilution Gas Chromatography/Tandem Mass Spectrometry (GC-MS/MS). Organic Analytical Toxicology Branch, Division of Laboratory Sciences, National Center for Environmental Health. In: Sciences DoL (Hrsg.), pp 1–38

  • Chevalier RL (2016) The proximal tubule is the primary target of injury and progression of kidney disease: role of the glomerulotubular junction. Am J Physiol Ren Physiol 311:F145–F161

    Article  CAS  Google Scholar 

  • Cui X, Cheng H, Liu X, Giubilato E, Critto A, Sun H, Zhang L (2018) Cadmium exposure and early renal effects in the children and adults living in a tungsten-molybdenum mining areas of South China. Environ Sci Pollut Res Int 25:15089–15101

    Article  CAS  Google Scholar 

  • de la Sota C, Lumbreras J, Pérez N, Ealo M, Kane M, Youm I, Viana M (2018) Indoor air pollution from biomass cookstoves in rural Senegal. Energy Sustain Dev 43:224–234

    Article  Google Scholar 

  • Díaz de León-Martínez L, Díaz-Barriga F, Barbier O, Ortíz DLG, Ortega-Romero M, Pérez-Vázquez F, Flores-Ramírez R (2019) Evaluation of emerging biomarkers of renal damage and exposure to aflatoxin-B1 in Mexican indigenous women: a pilot study. Environ Sci Pollut Res 26:12205–12216

    Article  CAS  Google Scholar 

  • Díaz de León-Martínez L, Ortega-Romero M, Grimaldo-Galeana JM, Barbier O, Vargas-Berrones K, García-Arreola ME, Rodriguez-Aguilar M, Flores-Ramírez R (2020) Assessment of kidney health and exposure to mixture pollutants in the Mexican indigenous population. Environ Sci Pollut Res 27:34557–34566

    Article  CAS  Google Scholar 

  • Domingos MA, Moreira SR, Gomez L, Goulart A, Lotufo PA, Bensenor I, Titan S (2016) Urinary retinol-binding protein: relationship to renal function and cardiovascular risk factors in chronic kidney disease. PLoS One 11:e0162782

    Article  CAS  Google Scholar 

  • Duan R-R, Hao K, Yang T (2020) Air pollution and chronic obstructive pulmonary disease. Chronic Diseases and Translational Medicine 6(4):260–269

    Article  Google Scholar 

  • Eickhoff C (2004). Ph D.Thesis: Studies of polycyclic aromatic hydrocarbons in Dungeness crabs: biomonitoring, physiologically based toxicokinetic model, and human health risk assessment. Biological Sciences Department-Simon Fraser University

  • Estévez-García JA, Schilmann A, Riojas-Rodríguez H, Berrueta V, Blanco S, Villaseñor-Lozano CG, Flores-Ramírez R, Cortez-Lugo M, Pérez-Padilla R (2020) Women exposure to household air pollution after an improved cookstove program in rural San Luis Potosi, Mexico. Sci Total Environ 702:134456

    Article  CAS  Google Scholar 

  • Fajgelj A, Ambrus Á (2000) Guidelines for single-laboratory validation of analytical methods for trace-level concentrations of organic chemicals. In: Fajgelj A, Ambrus Á (eds) Principles and Practices of Method Validation. The Royal Society of Chemistry, Cambridge, pp 179–252

    Google Scholar 

  • Farzan SF, Chen Y, Trachtman H, Trasande L (2016) Urinary polycyclic aromatic hydrocarbons and measures of oxidative stress, inflammation and renal function in adolescents: NHANES 2003-2008. Environ Res 144:149–157

    Article  CAS  Google Scholar 

  • Feldreich T, Carlsson AC, Helmersson-Karlqvist J, Riserus U, Larsson A, Lind L, Arnlov J (2017) Urinary osteopontin predicts incident chronic kidney disease, while plasma osteopontin predicts cardiovascular death in elderly men. Cardio Med 7:245–254

    Article  CAS  Google Scholar 

  • Fernando B, Alli-Shaik A, Hemage RKD, Badurdeen Z, Hettiarachchi TW, Abeysundara HTK, Abeysekara TDJ, Wazil A, Rathnayake S, Gunaratne J, Nanayakkara N (2019) Pilot study of renal urinary biomarkers for diagnosis of CKD of uncertain etiology. Kidney Int Rep 4:1401–1411

    Article  Google Scholar 

  • Flores-Ramírez R, Rico-Escobar E, Núñez-Monreal JE, García-Nieto E, Carrizales L, Ilizaliturri-Hernández C, Díaz-Barriga F (2012) Exposición infantil al plomo en sitios contaminados. Salud Publica Mex 54:383–392

    Article  Google Scholar 

  • Fuchs TC, Hewitt P (2011) Biomarkers for drug-induced renal damage and nephrotoxicity—an overview for applied toxicology. AAPS J 13:615–631

    Article  CAS  Google Scholar 

  • George B, Joy MS, Aleksunes LM (2018) Urinary protein biomarkers of kidney injury in patients receiving cisplatin chemotherapy. Exp Biol Med 243:272–282

    Article  CAS  Google Scholar 

  • Gilmour MI, Jaakkola MS, London SJ, Nel AE, Rogers CA (2006) How exposure to environmental tobacco smoke, outdoor air pollutants, and increased pollen burdens influences the incidence of asthma. Environ Health Perspect 114:627–633

    Article  CAS  Google Scholar 

  • Grova N, Faÿs F, Hardy E, Appenzeller B (2017) New insights into urine-based assessment of polycyclic aromatic hydrocarbon-exposure from a rat model: identification of relevant metabolites and influence of elimination kinetics. Environ Pollut 228:484–495

    Article  CAS  Google Scholar 

  • Guo Y, Senthilkumar K, Alomirah H, Moon H-B, Minh TB, Mohd MA, Nakata H, Kannan K (2013) Concentrations and profiles of urinary polycyclic aromatic hydrocarbon metabolites (OH-PAHs) in several Asian countries. Environ Sci Technol 47:2932–2938

    Article  CAS  Google Scholar 

  • Hao JN, Yan B (2017) Determination of urinary 1-hydroxypyrene for biomonitoring of human exposure to polycyclic aromatic hydrocarbons carcinogens by a lanthanide-functionalized metal-organic framework sensor. Adv Funct Mater 27:1603856

    Article  CAS  Google Scholar 

  • Ho CC, Wu WT, Chen YC, Liou SH, Yet SF, Lee CH, Tsai HT, Weng CY, Tsai MH, Lin P (2019) Identification of osteopontin as a biomarker of human exposure to fine particulate matter. Environ Pollut 245:975–985

    Article  CAS  Google Scholar 

  • Jacob J, Seidel A (2002) Biomonitoring of polycyclic aromatic hydrocarbons in human urine. J Chromatogr B 778:31–47

    Article  CAS  Google Scholar 

  • Jimenez-Cordova MI, Cardenas-Gonzalez M, Aguilar-Madrid G, Sanchez-Pena LC, Barrera-Hernandez A, Dominguez-Guerrero IA, Gonzalez-Horta C, Barbier OC, Del Razo LM (2018) Evaluation of kidney injury biomarkers in an adult Mexican population environmentally exposed to fluoride and low arsenic levels. Toxicol Appl Pharmacol 352:97–106

    Article  CAS  Google Scholar 

  • Jongeneelen F, Anzion R, Scheepers P, Bos R, Henderson PT, Nijenhuis E, Veenstra S, Brouns R, Winkes A (1988) 1-Hydroxypyrene in urine as a biological indicator of exposure to polycyclic aromatic hydrocarbons in several work environments. Ann Occupat Hyg 32:35–43

    CAS  Google Scholar 

  • Jongeneelen FJ (2001) Benchmark guideline for urinary 1-hydroxypyrene as biomarker of occupational exposure to polycyclic aromatic hydrocarbons. Ann Occup Hyg 45:3–13

    Article  CAS  Google Scholar 

  • Jongeneelen FJ (2014) A guidance value of 1-hydroxypyrene in urine in view of acceptable occupational exposure to polycyclic aromatic hydrocarbons. Toxicol Lett 231:239–248

    Article  CAS  Google Scholar 

  • Karami S, Boffetta P, Brennan P, Stewart PA, Zaridze D, Matveev V, Janout V, Kollarova H, Bencko V, Navratilova M, Szeszenia-Dabrowska N, Mates D, Gromiec JP, Sobotka R, Chow WH, Rothman N, Moore LE (2011) Renal cancer risk and occupational exposure to polycyclic aromatic hydrocarbons and plastics. J Occup Environ Med 53:218–223

    Article  CAS  Google Scholar 

  • Karimi SM, Maziyaki A, Ahmadian Moghadam S, Jafarkhani M, Zarei H, Moradi-Lakeh M, Pouran H (2020) Continuous exposure to ambient air pollution and chronic diseases: prevalence, burden, and economic costs. Rev Environ Health 35:379–399

    Article  CAS  Google Scholar 

  • Kim H-J, Min J-y, Seo Y-S, Min K-b (2018) Association between exposure to ambient air pollution and renal function in Korean adults. Ann Occupat Environ Med 30:14

    Article  Google Scholar 

  • Koroshi A (2007) Microalbuminuria, is it so important? Hippokratia 11:105–107

    CAS  Google Scholar 

  • Lacquaniti A, Fenga C, Venuti VA, Pernice L, Catanzariti S, Sirna G, Pernice F, Arena A, Lupica R, Abbate C, Buemi M (2012) Hydrocarbons and kidney damage: potential use of neutrophil gelatinase-associated lipocalin and sister chromatide exchange. Am J Nephrol 35:271–278

    Article  CAS  Google Scholar 

  • Leroyer A, Jeandel F, Maitre A, Howsam M, Deplanque D, Mazzuca M, Nisse C (2010) 1-Hydroxypyrene and 3-hydroxybenzo [a] pyrene as biomarkers of exposure to PAH in various environmental exposure situations. Sci Total Environ 408:1166–1173

    Article  CAS  Google Scholar 

  • Li J, Fan H, Liu K, Li X, Fan D, Lu X, Xia Y, Cao Y, Xiao C (2020) Associations of urinary polycyclic aromatic hydrocarbons with albuminuria in US adults, NHANES 2003–2014. Ecotoxicol Environ Saf 195:110445

    Article  CAS  Google Scholar 

  • Li Y, Rittenhouse-Olson K, Scheider WL, Mu L (2012) Effect of particulate matter air pollution on C-reactive protein: a review of epidemiologic studies. Rev Environ Health 27:133–149

    Article  CAS  Google Scholar 

  • Lin Y, Ramanathan G, Zhu Y, Yin F, Rea ND, Lu X, Tseng CH, Faull KF, Yoon AJ, Jerrett M, Zhu T, Qiu X, Araujo JA (2019) Pro-oxidative and proinflammatory effects after traveling from Los Angeles to Beijing: a biomarker-based natural experiment. Circulation 140:1995–2004

    Article  CAS  Google Scholar 

  • Liu Y, Tao S, Yang Y, Dou H, Yang Y, Coveney RM (2007) Inhalation exposure of traffic police officers to polycyclic aromatic hydrocarbons (PAHs) during the winter in Beijing, China. Sci Total Environ 383:98–105

    Article  CAS  Google Scholar 

  • Macıas-Zamora J, Mendoza-Vega E, Villaescusa-Celaya J (2002) PAHs composition of surface marine sediments: a comparison to potential local sources in Todos Santos Bay, BC, Mexico. Chemosphere 46:459–468

    Article  Google Scholar 

  • Marek-Bukowiec K, Konieczny A, Ratajczyk K, Macur K, Czaplewska P, Czyżewska-Buczyńska A, Kowal P, Witkiewicz W (2021) The Value of Urinary RBP4 in The Diagnosis of FSGS and other Renal Diseases. Research Square. https://doi.org/10.21203/rs.3.rs-35997/v2

  • Martinez-Salinas RI, Perez-Maldonado IN, Batres-Esquivel LE, Flores-Ramirez R, Diaz-Barriga F (2011) Assessment of DDT, DDE, and 1-hydroxypyrene levels in blood and urine samples in children from Chiapas Mexico. Environ Sci Pollut Res Int 19:2658–2666

    Article  CAS  Google Scholar 

  • Mendoza-Caamal EC, Barajas-Olmos F, García-Ortiz H, Cicerón-Arellano I, Martínez-Hernández A, Córdova EJ, Esparza-Aguilar M, Contreras-Cubas C, Centeno-Cruz F, Cid-Soto M, Morales-Marín ME, Reséndiz-Rodríguez A, Jiménez-Ruiz JL, Salas-Martínez MG, Saldaña-Alvarez Y, Mirzaeicheshmeh E, Rojas-Martínez MR, Orozco L (2020) Metabolic syndrome in indigenous communities in Mexico: a descriptive and cross-sectional study. BMC Public Health 20:339

    Article  Google Scholar 

  • Mihai S, Codrici E, Popescu ID, Enciu AM, Rusu E, Zilisteanu D, Necula LG, Anton G, Tanase C (2019) Inflammation-related patterns in the clinical staging and severity assessment of chronic kidney disease. Dis Markers 2019:1814304

    Article  CAS  Google Scholar 

  • Mirabelli MC, Boehmer TK, Damon SA, Sircar KD, Wall HK, Yip FY, Zahran HS, Garbe PL (2018) Air quality awareness among US adults with respiratory and heart disease. Am J Prev Med 54:679–687

    Article  Google Scholar 

  • O’Dell K, Hornbrook RS, Permar W, Levin EJ, Garofalo LA, Apel EC, Blake NJ, Jarnot A, Pothier MA, Farmer DK (2020) Hazardous air pollutants in fresh and aged Western US wildfire smoke and implications for long-term exposure. Environ Sci Technol 54:11838–11847

    Article  CAS  Google Scholar 

  • Ortega-Romero M, Méndez-Hernández P, Cruz-Angulo MC, Hernández-Sánchez AM, Álvarez-Elías AC, Muñoz-Arizpe R, Sales-Heredia F, Aguilar-Madrid G, Juárez-Perez CA, Soto V, Valadés T, Olvera-Rivas N, Obrador-Vera GT, Barbier OC, Medeiros M (2019) Chronic kidney disease in children aged 6–15 years and associated risk factors in Apizaco, Tlaxcala, Mexico, a pilot study. Nephron 143:264–273

    Article  Google Scholar 

  • PAHO (2018) Ambient and Household Air Pollution and Health: Frequently Asked Questions, Communicable Diseases and Environmental Determinants of Health. Obtained from: https://www.paho.org/es/temas/calidad-aire-salud/contaminacion-aire-ambiental-exterior-vivienda-preguntas-frecuentes

  • Palacios-Ramírez A, Ramírez RF, Pérez-Vázquez FJ, Rodríguez-Aguilar M, Schilmann A, Riojas-Rodríguez H, Van Brussel E, Díaz-Barriga F (2018) Evaluación de la exposición a hidrocarburos aromáticos policíclicos y partículas en suspensión (PM2, 5) por quema de biomasa en una zona indígena del Estado de San Luis Potosí, México. Rev Salud Ambien 18:29–36

    Google Scholar 

  • Perduca M, Nicolis S, Mannucci B, Galliano M, Monaco HL (2018) Human plasma retinol-binding protein (RBP4) is also a fatty acid-binding protein. Biochim Biophys Acta Mol Cell Biol Lipids 1863:458–466

    Article  CAS  Google Scholar 

  • Popp W, Vahrenholz C, Schell C, Grimmer G, Dettbarn G, Kraus R, Brauksiepe A, Schmeling B, Gutzeit T, von Bülow J (1997) DNA single strand breakage, DNA adducts, and sister chromatid exchange in lymphocytes and phenanthrene and pyrene metabolites in urine of coke oven workers. Occup Environ Med 54:176–183

    Article  CAS  Google Scholar 

  • Prozialeck WC, VanDreel A, Ackerman CD, Stock I, Papaeliou A, Yasmine C, Wilson K, Lamar PC, Sears VL, Gasiorowski JZ, DiNovo KM, Vaidya VS, Edwards JR (2016) Evaluation of cystatin C as an early biomarker of cadmium nephrotoxicity in the rat. Biometals 29:131–146

    Article  CAS  Google Scholar 

  • Rodriguez-Aguilar M, Diaz de Leon-Martinez L, Gorocica-Rosete P, Padilla RP, Thirion-Romero I, Ornelas-Rebolledo O, Flores-Ramirez R (2020) Identification of breath-prints for the COPD detection associated with smoking and household air pollution by electronic nose. Respir Med 163:105901

    Article  Google Scholar 

  • Rodríguez-Aguilar M, Díaz de León-Martínez L, García-Luna S, Gómez-Gómez A, González-Palomo AK, Pérez-Vázquez FJ, Díaz-Barriga F, Trujillo J, Flores-Ramírez R (2019) Respiratory health assessment and exposure to polycyclic aromatic hydrocarbons in Mexican indigenous population. Environ Sci Pollut Res 26:25825–25833

    Article  CAS  Google Scholar 

  • Sanchez-Guerra M, Pelallo-Martinez N, Diaz-Barriga F, Rothenberg SJ, Hernandez-Cadena L, Faugeron S, Oropeza-Hernandez LF, Guaderrama-Diaz M, Quintanilla-Vega B (2012) Environmental polycyclic aromatic hydrocarbon (PAH) exposure and DNA damage in Mexican children. Mutat Res 742:66–71

    Article  CAS  Google Scholar 

  • Schrezenmeier EV, Barasch J, Budde K, Westhoff T, Schmidt-Ott KM (2017) Biomarkers in acute kidney injury - pathophysiological basis and clinical performance. Acta Physiol 219:554–572

    Article  CAS  Google Scholar 

  • Singh A, Kamal R, Tiwari R, Gaur VK, Bihari V, Satyanarayana G, Patel DK, Azeez PA, Srivastava V, Ansari A (2018a) Association between PAHs biomarkers and kidney injury biomarkers among kitchen workers with microalbuminuria: a cross-sectional pilot study. Clin Chim Acta 487:349–356

    Article  CAS  Google Scholar 

  • Singh A, Kamal R, Tiwari R, Gaur VK, Bihari V, Satyanarayana GNV, Patel DK, Azeez PA, Srivastava V, Ansari A, Kesavachandran CN (2018b) Association between PAHs biomarkers and kidney injury biomarkers among kitchen workers with microalbuminuria: a cross-sectional pilot study. Clin Chim Acta; Int J Clin Chem 487:349–356

    Article  CAS  Google Scholar 

  • Trasande L, Urbina EM, Khoder M, Alghamdi M, Shabaj I, Alam MS, Harrison RM, Shamy M (2015) Polycyclic aromatic hydrocarbons, brachial artery distensibility and blood pressure among children residing near an oil refinery. Environ Res 136:133–140

    Article  CAS  Google Scholar 

  • Trasande L, Aldana SI, Trachtman H, Kannan K, Morrison D, Christakis DA, Whitlock K, Messito MJ, Gross RS, Karthikraj R, Sathyanarayana S (2020) Glyphosate exposures and kidney injury biomarkers in infants and young children. Environ Pollut 256:113334

    Article  CAS  Google Scholar 

  • Trejo-Acevedo A, Rivero-Pérez NE, Flores-Ramírez R, Orta-García ST, Varela-Silva JA, Pérez-Maldonado IN (2012) Assessment of the levels of persistent organic pollutants and 1-hydroxypyrene in blood and urine samples from Mexican children living in an endemic malaria area in Mexico. Bull Environ Contam Toxicol 88:828–832

    Article  CAS  Google Scholar 

  • Valcke M, Ouellet N, Dube M, Laouan Sidi EA, LeBlanc A, Normandin L, Balion C, Ayotte P (2019) Biomarkers of cadmium, lead and mercury exposure in relation with early biomarkers of renal dysfunction and diabetes: results from a pilot study among aging Canadians. Toxicol Lett 312:148–156

    Article  CAS  Google Scholar 

  • Vargas-Berrones K, Diaz de Leon-Martinez L, Bernal-Jacome L, Rodriguez-Aguilar M, Avila-Galarza A, Flores-Ramirez R (2020) Rapid analysis of 4-nonylphenol by solid phase microextraction in water samples. Talanta 209:120546

    Article  CAS  Google Scholar 

  • Vázquez Larios E, Ramirez Hernández B, Badillo Lagunes PI, Fregoso Aguilar TA, Hernández Rodríguez CH, Mendoza Pérez JA (2013) Caracterización de suelos contaminados con HAPs en el valle de Metztitlán, Hgo., y aplicación de un proceso de biorremediación con membranas limitantes de oxígeno. Química Hoy 3:18–25

    Google Scholar 

  • Verhulst A, Persy VP, Van Rompay AR, Verstrepen WA, Helbert MF, De Broe ME (2002) Osteopontin synthesis and localization along the human nephron. J Am Soc Nephrol 13:1210–1218

    Article  CAS  Google Scholar 

  • Wallin M, Sallsten G, Lundh T, Barregard L (2014) Low-level cadmium exposure and effects on kidney function. Occup Environ Med 71:848–854

    Article  Google Scholar 

  • Wang J, Cao H, Sun D, Qi Z, Guo C, Peng W, Sun Y, Xie Y, Liu X, Li B (2019) Associations between ambient air pollution and mortality from all causes, pneumonia, and congenital heart diseases among children aged under 5 years in Beijing, China: a population-based time series study. Environ Res 176:108531

    Article  CAS  Google Scholar 

  • Wang Y, Meng L, Pittman EN, Etheredge A, Hubbard K, Trinidad DA, Kato K, Ye X, Calafat AM (2017) Quantification of urinary mono-hydroxylated metabolites of polycyclic aromatic hydrocarbons by on-line solid phase extraction-high performance liquid chromatography-tandem mass spectrometry. Anal Bioanal Chem 409:931–937

    Article  CAS  Google Scholar 

  • Waring WS, Moonie A (2011) Earlier recognition of nephrotoxicity using novel biomarkers of acute kidney injury. Clin Toxicol 49:720–728

    Article  CAS  Google Scholar 

  • Webb J, Coomes OT, Mergler D, Ross NA (2018) Levels of 1-hydroxypyrene in urine of people living in an oil producing region of the Andean Amazon (Ecuador and Peru). Int Arch Occup Environ Health 91:105–115

    Article  CAS  Google Scholar 

  • Woudneh MB, Benskin JP, Grace R, Hamilton MC, Magee BH, Hoeger GC, Forsberg ND, Cosgrove JR (2016) Quantitative determination of hydroxy polycylic aromatic hydrocarbons as a biomarker of exposure to carcinogenic polycyclic aromatic hydrocarbons. J Chromatogr A 1454:93–100

    Article  CAS  Google Scholar 

  • Wunnapuk K, Liu X, Peake P, Gobe G, Endre Z, Grice JE, Roberts MS, Buckley NA (2013) Renal biomarkers predict nephrotoxicity after paraquat. Toxicol Lett 222:280–288

    Article  CAS  Google Scholar 

  • Yin W, Hou J, Xu T, Cheng J, Li P, Wang L, Zhang Y, Wang X, Hu C, Huang C, Yu Z, Yuan J (2018) Obesity mediated the association of exposure to polycyclic aromatic hydrocarbon with risk of cardiovascular events. Sci Total Environ 616-617:841–854

    Article  CAS  Google Scholar 

  • Zhou Y, Sun H, Xie J, Song Y, Liu Y, Huang X, Zhou T, Rong Y, Wu T, Yuan J, Chen W (2016) Urinary polycyclic aromatic hydrocarbon metabolites and altered lung function in Wuhan, China. Am J Respir Crit Care Med 193:835–846

    Article  CAS  Google Scholar 

  • Zillikens MC, Demissie S, Hsu YH, Yerges-Armstrong LM, Chou WC, Stolk L, Livshits G, Broer L, Johnson T, Koller DL, Kutalik Z, Luan J’, Malkin I, Ried JS, Smith AV, Thorleifsson G, Vandenput L, Hua Zhao J, Zhang W, Aghdassi A, Åkesson K, Amin N, Baier LJ, Barroso I, Bennett DA, Bertram L, Biffar R, Bochud M, Boehnke M, Borecki IB, Buchman AS, Byberg L, Campbell H, Campos Obanda N, Cauley JA, Cawthon PM, Cederberg H, Chen Z, Cho NH, Jin Choi H, Claussnitzer M, Collins F, Cummings SR, de Jager PL, Demuth I, Dhonukshe-Rutten RAM, Diatchenko L, Eiriksdottir G, Enneman AW, Erdos M, Eriksson JG, Eriksson J, Estrada K, Evans DS, Feitosa MF, Fu M, Garcia M, Gieger C, Girke T, Glazer NL, Grallert H, Grewal J, Han BG, Hanson RL, Hayward C, Hofman A, Hoffman EP, Homuth G, Hsueh WC, Hubal MJ, Hubbard A, Huffman KM, Husted LB, Illig T, Ingelsson E, Ittermann T, Jansson JO, Jordan JM, Jula A, Karlsson M, Khaw KT, Kilpeläinen TO, Klopp N, Kloth JSL, Koistinen HA, Kraus WE, Kritchevsky S, Kuulasmaa T, Kuusisto J, Laakso M, Lahti J, Lang T, Langdahl BL, Launer LJ, Lee JY, Lerch MM, Lewis JR, Lind L, Lindgren C, Liu Y, Liu T, Liu Y, Ljunggren Ö, Lorentzon M, Luben RN, Maixner W, McGuigan FE, Medina-Gomez C, Meitinger T, Melhus H, Mellström D, Melov S, Michaëlsson K, Mitchell BD, Morris AP, Mosekilde L, Newman A, Nielson CM, O’Connell JR, Oostra BA, Orwoll ES, Palotie A, Parker SCJ, Peacock M, Perola M, Peters A, Polasek O, Prince RL, Räikkönen K, Ralston SH, Ripatti S, Robbins JA, Rotter JI, Rudan I, Salomaa V, Satterfield S, Schadt EE, Schipf S, Scott L, Sehmi J, Shen J, Soo Shin C, Sigurdsson G, Smith S, Soranzo N, Stančáková A, Steinhagen-Thiessen E, Streeten EA, Styrkarsdottir U, Swart KMA, Tan ST, Tarnopolsky MA, Thompson P, Thomson CA, Thorsteinsdottir U, Tikkanen E, Tranah GJ, Tuomilehto J, van Schoor NM, Verma A, Vollenweider P, Völzke H, Wactawski-Wende J, Walker M, Weedon MN, Welch R, Wichmann HE, Widen E, Williams FMK, Wilson JF, Wright NC, Xie W, Yu L, Zhou Y, Chambers JC, Döring A, van Duijn CM, Econs MJ, Gudnason V, Kooner JS, Psaty BM, Spector TD, Stefansson K, Rivadeneira F, Uitterlinden AG, Wareham NJ, Ossowski V, Waterworth D, Loos RJF, Karasik D, Harris TB, Ohlsson C, Kiel DP (2017) Erratum: Large meta-analysis of genome-wide association studies identifies five loci for lean body mass. Nat Commun 8:1414

    Article  CAS  Google Scholar 

  • Zylka A, Dumnicka P, Kusnierz-Cabala B, Gala-Bladzinska A, Ceranowicz P, Kucharz J, Zabek-Adamska A, Maziarz B, Drozdz R, Kuzniewski M (2018) Markers of glomerular and tubular damage in the early stage of kidney disease in type 2 diabetic patients. Mediat Inflamm 2018:7659243

    Article  CAS  Google Scholar 

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Funding

The authors acknowledge grants and fellowships from National Council on Science and Technology- Sectoral Research FOSEC SS/IMSS/ISSSTE # A3-S-38681.

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RFR: Conceptualization, Sampling, Analytical methods and Funding; MOR: Conceptualization and Analytical methods, Writing and Editing; OCB: Conceptualization and Analytical methods, JGMM: Analytical methods; MRA: Analytical methods, HALR: Conceptualization and LDLM: Conceptualization, Sampling, Analytical methods Writing and Editing.

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Correspondence to Lorena Díaz de León-Martínez.

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The protocol was approved by the Research Ethics Committee of the Faculty of Medicine of the Autonomous University of San Luis Potosi and the Bioethics Commission of the State of San Luis Potosi (CEI-2018-002).

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Flores-Ramírez, R., Ortega-Romero, M., Christophe-Barbier, O. et al. Exposure to polycyclic aromatic hydrocarbon mixtures and early kidney damage in Mexican indigenous population. Environ Sci Pollut Res 28, 23060–23072 (2021). https://doi.org/10.1007/s11356-021-12388-w

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