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Assessment of kidney health and exposure to mixture pollutants in the Mexican indigenous population

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Abstract

The indigenous population is one of the most vulnerable to suffer from contaminated environments. One of the target organs to suffer early deterioration from exposure to toxins is the kidney. The objective of this article was to evaluate biomarkers of exposure to organic and inorganic toxins and biomarkers of early kidney damage in urine from an indigenous Tenek population in Mexico. The biomarkers of exposure were Li, Be, Al, V, Cr, Mn, Fe, Ni, Cu, Zn, As, Se, Mo, Sn, Ba, and Pb evaluated by ICP-MS and hippuric acid for toluene exposure evaluated by UV-coupled with liquid chromatography; the biomarkers of kidney damage were cystatin C (Cys-C), osteopontin (OPN), retinol-binding protein-4 (RPB-4), and neutrophil gelatinase-associated lipocalin (NGAL). Thirty-one urine samples were obtained from indigenous people; 16, 42, 45.1, and 45.2% of the population exceeded the reference values for Pb, Zn, As, and hippuric acid respectively. Our results demonstrate significant correlations between the metals tested and the proteins associated with renal damage; Cys-C, OPN, and RPB4 showed a significant correlation with Li, B, and Mo, as well as hippuric acid in the case of Cys-C and Zn in OPN and RPB-4; NGAL did not present significant correlations with any of the pollutants of the study. This pilot study contributes to the evidence of great inequity in health associated to environmental pollution matters faced by indigenous people and addresses the need of initiatives for mitigation under the perspective that health is a fundamental human right.

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References

  • ACGIH (2014)Threshold limit values and biological exposure indices for 2014. In: Hygienists ACoGI (Hrsg.), Cincinnati, Ohio, US

  • Ana-Lilia G-Y, Carlos K, Kazimierz W, Elva-Leticia P-L, Katarzina W, Gloria B (2006) Occupational exposure to toluene and its possible causative role in renal damage development in shoe workers. Int Arch Occup Environ Health 79:259–264

    CAS  Google Scholar 

  • Andrassy KM (2013) Comments on ‘KDIGO 2012 Clinical Practice Guideline for the Evaluation and Management of Chronic Kidney Disease’. Kidney Int 84:622–623

    CAS  Google Scholar 

  • Apel P, Angerer J, Wilhelm M, Kolossa-Gehring M (2017) New HBM values for emerging substances, inventory of reference and HBM values in force, and working principles of the German Human Biomonitoring Commission. Int J Hyg Environ Health 220:152–166

    Google Scholar 

  • Bompart G, Pécher C, Prévot D, Girolami J-P (1990) Mild renal failure induced by subchronic exposure to molybdenum: urinary kallikrein excretion as a marker of distal tubular effect. Toxicol Lett 52:293–300

    CAS  Google Scholar 

  • Burgaz S, Erdem O, Çakmak G, Erdem N, Karakaya A, Karakaya AE (2002) Cytogenetic analysis of buccal cells from shoeworkers and pathology and anatomy laboratory workers exposed to n-hexane, toluene, methyl ethyl ketone and formaldehyde. Biomarkers 7:151–161

    CAS  Google Scholar 

  • Camara-Lemarroy CR, Rodríguez-Gutiérrez R, Monreal-Robles R, González-González JG (2015) Acute toluene intoxication--clinical presentation, management and prognosis: a prospective observational study. BMC Emerg Med 15:19–19

    Google Scholar 

  • Cao L, Jiang H, Yang J, Fan L, Li F, Huang Q (2013) Simultaneous determination of benzene and toluene in pesticide emulsifiable concentrate by headspace GC-MS. J Anal Methods Chem 2013:121783

    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

    CAS  Google Scholar 

  • Castro VM, Roberson AM, McCoy TH, Wiste A, Cagan A, Smoller JW, Rosenbaum JF, Ostacher M, Perlis RH (2016) Stratifying risk for renal insufficiency among lithium-treated patients: an electronic health record study. Neuropsychopharmacology 41:1138–1143

    CAS  Google Scholar 

  • CDC (2019) Fourth national report on human exposure to environmental chemicals

  • Choi C-Y, Cho N, Park S-Y, Park S, Gil HW, Hong S-Y (2017) Urine methyl hippuric acid levels in acute pesticide poisoning: estimation of ingested xylene volume and association with clinical outcome parameters. J Korean Med Sci 32:2051–2057

    CAS  Google Scholar 

  • Çok I, Dagdelen A, Gökçe E (2003) Determination of urinary hippuric acid and o-cresol levels as biological indicators of toluene exposure in shoe-workers and glue sniffers. Biomarkers 8:119–127

    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 25:15089–15101

    CAS  Google Scholar 

  • Decharat S (2014) Hippuric Acid levels in paint workers at steel furniture manufacturers in Thailand. Saf Health Work 5:227–233

    Google Scholar 

  • Díaz de León-Martínez L, Díaz-Barriga F, Barbier O, Ortíz DLG, Ortega-Romero M, Pérez-Vázquez F, Flores-Ramírez R (2019a) 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

    Google Scholar 

  • Díaz de León-Martínez L, Solis-Mercado J, Rodríguez-Aguilar M, Díaz-Barriga F, Guzmán Ortíz D, Flores-Ramírez R (2019b) Assessment of aflatoxin B1-lysine adduct in serum of infant population of the Huasteca Potosina, México – a pilot study. World Mycotoxin J 12:421–429

    Google Scholar 

  • Domingos MAM, Moreira SR, Gomez L, Goulart A, Lotufo PA, Benseñor I, Titan S (2016) Urinary Retinol-Binding Protein: Relationship to renal function and cardiovascular risk factors in chronic kidney disease. PLoS One 11:e0162782–e0162782

    Google Scholar 

  • Dyck RF, Jiang Y, Osgood ND (2014) The long-term risks of end stage renal disease and mortality among First Nations and non-First Nations people with youth-onset diabetes. Can J Diabetes 38:237–243

    Google Scholar 

  • Estevez-Garcia JA, Schilmann A, Riojas-Rodriguez H, Berrueta V, Blanco S, Villasenor-Lozano CG, Flores-Ramirez R, Cortez-Lugo M, Perez-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

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Fernández-Llamazares Á, Garteizgogeascoa M, Basu N, Brondizio ES, Cabeza M, Martínez-Alier J, McElwee P, Reyes-García V (2019) A state-of-the-art review of Indigenous Peoples and environmental pollution. Integr Environ Assess Manag n/a

  • Filler G, Belostotsky V, Kobrzynski M, Huang SS, Yang L (2017) High prevalence of elevated molybdenum levels in pediatric CKD patients. A cross-sectional and longitudinal study. Clin Nephrol 88:79–85

    CAS  Google Scholar 

  • Flores-Ramirez R, Rico-Escobar E, Nunez-Monreal JE, Garcia-Nieto E, Carrizales L, Ilizaliturri-Hernandez C, Diaz-Barriga F (2012) Children exposure to lead in contaminated sites. Salud Publica Mex 54:383–392

    Google Scholar 

  • Flores-Ramirez R, Perez-Vazquez FJ, Cilia-Lopez VG, Zuki-Orozco BA, Carrizales L, Batres-Esquivel LE, Palacios-Ramirez A, Diaz-Barriga F (2016) Assessment of exposure to mixture pollutants in Mexican indigenous children. Environ Sci Pollut Res Int 23:8577–8588

    CAS  Google Scholar 

  • Flores-Ramirez R, Perez-Vazquez FJ, Rodriguez-Aguilar M, Medellin-Garibay SE, Van Brussel E, Cubillas-Tejeda AC, Carrizales-Yanez L, Diaz-Barriga F (2017) Biomonitoring of persistent organic pollutants (POPs) in child populations living near contaminated sites in Mexico. Sci Total Environ 579:1120–1126

    CAS  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

    CAS  Google Scholar 

  • Gonzalez-Calero L, Martin-Lorenzo M, Ramos-Barron A, Ruiz-Criado J, Maroto AS, Ortiz A, Gomez-Alamillo C, Arias M, Vivanco F, Alvarez-Llamas G (2016) Urinary kininogen-1 and retinol binding protein-4 respond to acute kidney injury: predictors of patient prognosis? Sci Rep 6:19667

    CAS  Google Scholar 

  • Grünfeld J-P, Rossier BC (2009) Lithium nephrotoxicity revisited. Nat Rev Nephrol 5:270–276

    Google Scholar 

  • Hays SM, Becker RA, Leung HW, Aylward LL, Pyatt DW (2007) Biomonitoring equivalents: a screening approach for interpreting biomonitoring results from a public health risk perspective. Regul Toxicol Pharmacol 47:96–109

    CAS  Google Scholar 

  • Hays SM, Aylward LL, Gagne M, Nong A, Krishnan K (2010) Biomonitoring equivalents for inorganic arsenic. Regul Toxicol Pharmacol 58:1–9

    CAS  Google Scholar 

  • Hays SM, Macey K, Nong A, Aylward LL (2014) Biomonitoring equivalents for selenium. Regul Toxicol Pharmacol 70:333–339

    CAS  Google Scholar 

  • Hays SM, Macey K, Poddalgoda D, Lu M, Nong A, Aylward LL (2016) Biomonitoring equivalents for molybdenum. Regul Toxicol Pharmacol 77:223–229

    CAS  Google Scholar 

  • HC (2019) Fifth Report on Human Biomonitoring of Environmental Chemicals in Canada. Minister of Health, Ottawa

    Google Scholar 

  • Hirano T, Murakami M, Fukada T, Nishida K, Yamasaki S, Suzuki T (2008) Roles of zinc and zinc signaling in immunity: zinc as an intracellular signaling molecule. Adv Immunol. Academic Press, pp 149–176

  • Hormozi M, Mirzaei R, Nakhaee A, Payandeh A, Izadi S, Dehghan Haghighi J, Rahimpoor R (2019) Quantification of urinary metabolites of toluene and xylene isomers as biological indices of occupational exposure in printing industry workers. Health Scope 8:e82962

    Google Scholar 

  • Hoyer JR, Asplin JR, Otvos L Jr (2001) Phosphorylated osteopontin peptides suppress crystallization by inhibiting the growth of calcium oxalate crystals. Kidney Int 60:77–82

    CAS  Google Scholar 

  • Igra AM, Harari F, Lu Y, Casimiro E, Vahter M (2016) Boron exposure through drinking water during pregnancy and birth size. Environ Int 95:54–60

    CAS  Google Scholar 

  • Jayasinghe S, Zhu Y-G (2020) Chronic kidney disease of unknown etiology (CKDu): using a system dynamics model to conceptualize the multiple environmental causative pathways of the epidemic. Sci Total Environ 705:135766

    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

    CAS  Google Scholar 

  • Kaleta B (2019) The role of osteopontin in kidney diseases. Inflamm Res 68:93–102

    CAS  Google Scholar 

  • Kao K-C, Tsai Y-H, Lin M-C, Huang C-C, Tsao TC-Y, Chen Y-C (2000) Hypokalemic muscular paralysis causing acute respiratory failure due to rhabdomyolysis with renal tubular acidosis in a chronic glue sniffer. J Toxicol Clin Toxicol 38:679–681

    CAS  Google Scholar 

  • Landrigan PJ, Fuller R, Acosta NJR, Adeyi O, Arnold R, Basu N(N), Baldé AB, Bertollini R, Bose-O'Reilly S, Boufford JI, Breysse PN, Chiles T, Mahidol C, Coll-Seck AM, Cropper ML, Fobil J, Fuster V, Greenstone M, Haines A, Hanrahan D, Hunter D, Khare M, Krupnick A, Lanphear B, Lohani B, Martin K, Mathiasen KV, McTeer MA, Murray CJL, Ndahimananjara JD, Perera F, Potočnik J, Preker AS, Ramesh J, Rockström J, Salinas C, Samson LD, Sandilya K, Sly PD, Smith KR, Steiner A, Stewart RB, Suk WA, van Schayck OCP, Yadama GN, Yumkella K, Zhong M (2018) The Lancet Commission on pollution and health. Lancet 391:462–512

    Google Scholar 

  • Liyanage T, Ninomiya T, Jha V, Neal B, Patrice HM, Okpechi I, Zhao MH, Lv J, Garg AX, Knight J, Rodgers A, Gallagher M, Kotwal S, Cass A, Perkovic V (2015) Worldwide access to treatment for end-stage kidney disease: a systematic review. Lancet 385:1975–1982

    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

    Google Scholar 

  • Mugica V, Ruiz ME, Watson J, Chow J (2003) Volatile aromatic compounds in Mexico City atmosphere: levels and source apportionment. Atmósfera 16:15–27

    Google Scholar 

  • Norden AGW, Lapsley M, Unwin RJ (2014) Chapter three - urine retinol-binding protein 4: a functional biomarker of the proximal renal tubule. In: Makowski GS (ed) Advances in Clinical Chemistry. Elsevier, pp 85–122

  • Oh HH, Park H, Kim DH, Son B-C, Lee C-K, Kim K, Ryu JY (2017) The relationship between urinary BTEX metabolites and residence setting among Korean homemakers: the first Korea National Environmental Health Survey (2009–2011). Ann Occup Environ Med 29:38

    Google Scholar 

  • OHCHR (2020): General call for contributions on the consequences of exposure of indigenous people to toxic and otherwise hazardous substances. In: toxics SRohra (Hrsg.), SR Hazardous Substances and Wastes. Office of the United Nations High Commissioner for Human Rights (OHCHR), Geneva

  • Orr SE, Bridges CC (2017) Chronic kidney disease and exposure to nephrotoxic metals. Int J Mol Sci 18:1039

    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

    Google Scholar 

  • Pérez-Herrera N, Díaz de León-Martínez L, Flores-Ramírez R, Barbier O, Ortega-Romero M, May-Euán F, Saldaña-Villanueva K, Perera-Rios J, Pérez-Vázquez FJ (2019) Evaluation of benzene exposure and early biomarkers of kidney damage in children exposed to solvents due to precarious work in Ticul, Yucatán, México. Ann Glob Health 85:94

    Google Scholar 

  • PNUD (2010) Informe sobre Desarrollo Humano 2010. La verdadera riqueza de las naciones: caminos al desarrollo humano

  • Poddalgoda D, Macey K, Jayawardene I, Krishnan K (2016) Derivation of biomonitoring equivalent for inorganic tin for interpreting population-level urinary biomonitoring data. Regul Toxicol Pharmacol 81:430–436

    CAS  Google Scholar 

  • Poddalgoda D, Macey K, Assad H, Krishnan K (2017) Development of biomonitoring equivalents for barium in urine and plasma for interpreting human biomonitoring data. Regul Toxicol Pharmacol 86:303–311

    CAS  Google Scholar 

  • Poddalgoda D, Macey K, Hancock S (2019) Derivation of biomonitoring equivalents (BE values) for zinc. Regul Toxicol Pharmacol 106:178–186

    CAS  Google Scholar 

  • Pruneda-Alvarez LG, Perez-Vazquez FJ, Salgado-Bustamante M, Martinez-Salinas RI, Pelallo-Martinez NA, Perez-Maldonado IN (2012) Exposure to indoor air pollutants (polycyclic aromatic hydrocarbons, toluene, benzene) in Mexican indigenous women. Indoor Air 22:140–147

    CAS  Google Scholar 

  • Prüss-Ustün AWJ, Corvalán C, Bos R, Neira M (2016) Preventing disease through healthy environments. A global assessment of the burden of disease from environmental risks. World Heatlh Organization, France

    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

    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

    Google Scholar 

  • Seo H-J, Cho Y-E, Kim T, Shin H-I, Kwun I-S (2010) Zinc may increase bone formation through stimulating cell proliferation, alkaline phosphatase activity and collagen synthesis in osteoblastic MC3T3-E1 cells. Nutr Res Pract 4:356–361

    CAS  Google Scholar 

  • UNDP (2014) Environmental justice comparative experiences in legal empowerment. United Nations Development Programme, New York

    Google Scholar 

  • UNDP (2019) Human Development Report 2019. Beyond income, beyond averages, beyond today: Inequalities in human development in the 21st century. United Nations Development Programme, New York

    Google Scholar 

  • Valcke M, Ouellet N, Dubé 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

    CAS  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

    CAS  Google Scholar 

  • Yeates K, Tonelli M (2006) Indigenous health: update on the impact of diabetes and chronic kidney disease. Curr Opin Nephrol Hypertens 15:588–592

    Google Scholar 

  • Yoshida M, Fukumoto M, Kishimoto T, Yamamura Y, Shimizu H, Sakai O (1993) Effects of zinc, selenium, and calcium on the nephrotoxicity of cadmium in primary cultures of rat renal proximal epithelial cells. Biol Trace Elem Res 36:219–227

    CAS  Google Scholar 

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Funding

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

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Authors and Affiliations

  1. Centro de Investigación Aplicada en Ambiente y Salud (CIAAS), Avenida Sierra Leona No. 550, Colonia Lomas Segunda Sección, 78210, San Luis Potosí, SLP, México

    Lorena Díaz de León-Martínez, José Moisés Grimaldo-Galeana, Karla Vargas-Berrones, María Elena García-Arreola & Maribel Rodriguez-Aguilar

  2. Departamento de Toxicología, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional (CINVESTAV-IPN), México, Ciudad de México, México

    Manolo Ortega-Romero & Olivier Barbier

  3. CONACYT Research Fellow, Coordinación para la Innovación y Aplicación de la Ciencia y la Tecnología (CIACYT), Avenida Sierra Leona No. 550, Colonia Lomas Segunda Sección, 78210, San Luis Potosí, SLP, México

    Rogelio Flores-Ramírez

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  1. Lorena Díaz de León-Martínez
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  2. Manolo Ortega-Romero
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Díaz de León-Martínez, L., Ortega-Romero, M., Grimaldo-Galeana, J.M. et al. Assessment of kidney health and exposure to mixture pollutants in the Mexican indigenous population. Environ Sci Pollut Res 27, 34557–34566 (2020). https://doi.org/10.1007/s11356-020-09619-x

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