Skip to main content

Advertisement

SpringerLink
Log in

Evaluation of emerging biomarkers of renal damage and exposure to aflatoxin-B1 in Mexican indigenous women: a pilot study

Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Aflatoxins (AFs) are mycotoxins produced by Aspergillus parasiticus and Aspergillus flavus which frequently contaminate maize. These compounds are considered toxic, especially AFB1 which has been classified as a human carcinogen, due to its relationship with the generation of hepatocellular carcinoma. Studies in vivo, in animal models, prove that chronic consumption of AFB1 has an association with renal adverse effects, but evidence in humans is scarce. Therefore, the main objective of this research was to conduct a pilot study to evaluate the correlation between exposure to AFB1 and early-stage renal damage in indigenous women of San Luis Potosí, Mexico. Exposure to AFB1 was measured through the biomarker AFB1-lysine and renal damage through kidney injury molecule-1 (KIM-1), neutrophil gelatinase-associated lipocalin (NGAL), and cystatin-C (Cys-C). AFB1-Lys was measured by HPLC-FLD. The method was validated with a correlation coefficient of 0.99 and limit of detection and quantification of 3.5 and 4.7 pg mL−1, respectively. Levels of NGAL, KIM-1, and Cys-C were determined (median (P25–P75), 5.96 (3.16–15.91), 0.137 (0.137–0.281), and 18.49 (5.76–29.57) ng mL−1, respectively). Additionally, glomerular filtration rate (GFR) (83.3 (59.8–107.4) mL/min/1.73 m2) and serum creatinine (SCr) (0.88 (0.72–1.22) mg dL−1) were obtained. The median concentrations for AFB1-Lys were 2.08 (1.89–5.8) pg mg−1 of albumin. Statistically significant correlations between AFB1-Lys/KIM-1 (Rho = 0.498, p = 0.007) and AFB1/Cys-C (Rho = 0.431, p = 0.014) were found. Our results indicate that women are exposed to AFB1, due to the fact that the AFB1-Lys biomarker was found in a high percentage of the study population (83%). In addition, the results of exposure to AFB1 show a strong significant correlation between KIM-1 and Cys-C that may indicate the toxic renal effect. These results are alarming because of the high toxicity of this compound and require adequate intervention to reduce AFB1 exposure in these populations.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price includes VAT (France)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

References

  • Aelion CM, Davis HT, Lawson AB, Cai B, McDermott S (2013) Associations between soil lead concentrations and populations by race/ethnicity and income-to-poverty ratio in urban and rural areas. Environ Geochem Hlth 35:1–12

    Article  CAS  Google Scholar 

  • Amato DK, Alvarez-Aguilar C, Castaneda-Limones R, Rodriguez E, Avila-Diaz M, Arreola F, Gomez A, Ballesteros H, Becerril K, Paniagua R (2005) Prevalence of chronic kidney disease in an urban Mexican population. Kidney Int 68:S11–S17

    Article  Google Scholar 

  • AOAC/FAO/IAEA/IUPAC (2000) Guidelines for single-laboratory validation of analytical methods for trace-level concentrations of organic chemicals. In: Fajgelj A, Ambrus A (eds) Principles and practices of method validation. Royal Society of Chemistry, Cambridge

    Google Scholar 

  • Asghar MA, Iqbal J, Ahmed A, Khan MA, Shamsuddin ZA (2014) Aflatoxin B1 in betel nuts (Areca catechu L.) imported to Pakistan from different regions of South Asia. Food Addit Contam Part B Surveill 7:176–181

    Article  CAS  Google Scholar 

  • Beardall J, Miller JD (1994) Natural occurrence of mycotoxins other than aflatoxin in Africa, Asia and South America. Mycotoxin Res 10:21–40

    Article  CAS  Google Scholar 

  • Bedard LL, Massey TE (2006) Aflatoxin B-1-induced DNA damage and its repair. Cancer Lett 241:174–183

    Article  CAS  Google Scholar 

  • Benli E, Ayyildiz SN, Cirrik S, Noyan T, Ayyildiz A, Cirakoglu A (2017) Early term effect of ureterorenoscopy (URS) on the kidney: research measuring NGAL, KIM-1, FABP and CYS C levels in urine. Int Braz J Urol 43:887–895

    Article  Google Scholar 

  • Bennett JW, Klich M (2003) Mycotoxins. Clin Microbiol Rev 16:497–516

    Article  CAS  Google Scholar 

  • Bosch JP (1995) Renal reserve: a functional view of glomerular filtration rate. Semin Nephrol 15:381–385

    CAS  Google Scholar 

  • Camarillo EH, Ramirez-Martinez A, Carvajal-Moreno M, Vargas-Ortiz M, Wesolek N, Rodriguez Jimenes GDC, Garcia Alvarado MA, Roudot AC, Salgado Cervantes MA, Robles-Olvera VJ (2018) Assessment of aflatoxin M1 and M2 exposure risk through Oaxaca cheese consumption in southeastern Mexico. Int J Environ Health Res:1–12

  • 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 

  • Carvajal M, Rojo F, Mendez I, Bolanos A (2003) Aflatoxin B-1 and its interconverting metabolite aflatoxicol in milk: the situation in Mexico. Food Addit Contam 20:1077–1086

    Article  CAS  Google Scholar 

  • Castillo-Urueta P, Carvajal M, Mendez I, Meza F, Galvez A (2011) Survey of aflatoxins in maize tortillas from Mexico City. Food Addit Contam Part B Surveill 4:42–51

    Article  CAS  Google Scholar 

  • Chin CK, Abdullah A, Sugita-Konishi Y (2012) Dietary intake of aflatoxins in the adult Malaysian population - an assessment of risk. Food Addit Contam B 5:286–294

    Article  CAS  Google Scholar 

  • Chu YJ, Yang HI, Wu HC, Lee MH, Liu J, Wang LY, Lu SN, Jen CL, You SL, Santella RM, Chen CJ (2018) Aflatoxin B1 exposure increases the risk of hepatocellular carcinoma associated with hepatitis C virus infection or alcohol consumption. Eur J Cancer 94:37–46

    Article  CAS  Google Scholar 

  • Correa-Rotter R, Wesseling C, Johnson RJ (2014) CKD of unknown origin in Central America: the case for a Mesoamerican nephropathy. Am J Kidney Dis 63:506–520

    Article  Google Scholar 

  • de Rijk TC, van Egmond HP, van der Fels-Klerx HJ, Herbes R, de Nijs M, Samson RA, Slate AB, van der Spiegel M (2015) A study of the 2013 Western European issue of aflatoxin contamination of maize from the Balkan area. World Mycotoxin J 8:641–651

    Article  CAS  Google Scholar 

  • Delanaye P, Schaeffner E, Ebert N, Cavalier E, Mariat C, Krzesinski JM, Moranne O (2012) Normal reference values for glomerular filtration rate: what do we really know? Nephrol Dial Transpl 27:2664–2672

    Article  Google Scholar 

  • Desalegn B, Nanayakkara S, Harada KH, Hitomi T, Chandrajith R, Karunaratne U, Abeysekera T, Koizumi A (2011) Mycotoxin detection in urine samples from patients with chronic kidney disease of uncertain etiology in Sri Lanka. Bull Environ Contam Toxicol 87:6–10

    Article  CAS  Google Scholar 

  • Diaz GJ, Sanchez MP (2015) Determination of aflatoxin M1 in breast milk as a biomarker of maternal and infant exposure in Colombia. Food Addit Contam Part A Chem Anal Control Expo Risk Assess 32:1192–1198

    Article  CAS  Google Scholar 

  • Dvorackova I, Kusak V, Vesely D, Vesela J, Nesnidal P (1977) Aflatoxin and encephalopathy with fatty degeneration of viscera (Reye). Ann Nutr Aliment 31:977–989

    CAS  Google Scholar 

  • El-Mahalaway AM (2015) Protective effect of curcumin against experimentally induced aflatoxicosis on the renal cortex of adult male albino rats: a histological and immunohistochemical study. Int J Clin Exp Pathol 8:6019–6030

    CAS  Google Scholar 

  • Essigmann JM, Croy RG, Nadzan AM, Busby WF Jr, Reinhold VN, Buchi G, Wogan GN (1977) Structural identification of the major DNA adduct formed by aflatoxin B1 in vitro. Proc Natl Acad Sci U S A 74:1870–1874

    Article  CAS  Google Scholar 

  • EU (2015) Commission Regulation (EC) No 1881/2006 of 19 December 2006 setting maximum levels for certain contaminants in foodstuffs. In: Union OJotE (Hrsg.), European Union

  • Flores-Ramirez R, Medellin-Garibay SE, Castillo CG, Ilizaliturri-Hernandez CA, Zuki-Orozco BA, Batres-Esquivel L, Diaz-Barriga F (2015) Application of focused ultrasound-assisted extraction to the determination of persistent organic pollutants (POPs) in soil samples. Bull Environ Contam Toxicol 95:207–214

    Article  CAS  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

    Article  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

    Article  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

    Article  CAS  Google Scholar 

  • Glahn RP, Beers KW, Bottje WG, Wideman RF Jr, Huff WE (1990) Altered renal function in broilers during aflatoxicosis. Poult Sci 69:1796–1799

    Article  CAS  Google Scholar 

  • Groopman JD, Egner PA, Schulze KJ, Wu LS, Merrill R, Mehra S, Shamim AA, Ali H, Shaikh S, Gernand A, Khatry SK, LeClerq SC, West KP Jr, Christian P (2014) Aflatoxin exposure during the first 1000 days of life in rural South Asia assessed by aflatoxin B(1)-lysine albumin biomarkers. Food Chem Toxicol 74:184–189

    Article  CAS  Google Scholar 

  • Grubb A (2017) Cystatin C is indispensable for evaluation of kidney disease. EJIFCC 28:268–276

    CAS  Google Scholar 

  • Gutierrez-Padilla JA, Mendoza-Garcia M, Plascencia-Perez S, Renoirte-Lopez K, Garcia-Garcia G, Lloyd A, Tonelli M (2010) Screening for CKD and cardiovascular disease risk factors using mobile clinics in Jalisco, Mexico. Am J Kidney Dis 55:474–484

    Article  CAS  Google Scholar 

  • Han WK, Bailly V, Abichandani R, Thadhani R, Bonventre JV (2002) Kidney injury molecule-1 (KIM-1): a novel biomarker for human renal proximal tubule injury. Kidney Int 62:237–244

    Article  CAS  Google Scholar 

  • Hoffmann D, Fuchs TC, Henzler T, Matheis KA, Herget T, Dekant W, Hewitt P, Mally A (2010) Evaluation of a urinary kidney biomarker panel in rat models of acute and subchronic nephrotoxicity. Toxicology 277:49–58

    Article  CAS  Google Scholar 

  • Horwitz W (1982) Evaluation of analytical methods used for regulation of foods and drugs. Anal Chem 54:67A–76A

    Article  CAS  Google Scholar 

  • IARC (2002) Aflatoxin. In: IARC monograph on the evaluation of carcinogenic risk to humans. Some traditional herbal medicines, some mycotoxins, naphthalene, styrene. In: Cancer IAfRo (Hrsg.), Lyon, France

  • Iqbal SZ, Paterson RR, Bhatti IA, Asi MR (2010) Survey of aflatoxins in chillies from Pakistan produced in rural, semi-rural and urban environments. Food Addit Contam Part B Surveill 3:268–274

    Article  CAS  Google Scholar 

  • Iqbal SZ, Asi MR, Hanif U, Zuber M, Jinap S (2016) The presence of aflatoxins and ochratoxin A in rice and rice products; and evaluation of dietary intake. Food Chem 210:135–140

    Article  CAS  Google Scholar 

  • Jager AV, Tonin FG, Baptista GZ, Souto PCMC, Oliveira CAF (2016) Assessment of aflatoxin exposure using serum and urinary biomarkers in Sao Paulo, Brazil: a pilot study. Int J Hyg Envir Heal 219:294–300

    Article  CAS  Google Scholar 

  • Jain RB (2017) Trends in the levels of urine and serum creatinine: data from NHANES 2001-2014. Environ Sci Pollut Res Int 24:10197–10204

    Article  Google Scholar 

  • JECFA (2017) Evaluation of certain contaminants in food: eighty-third report of the Joint FA, WHO

  • Jeon YK, Kim MR, Huh JE, Mok JY, Song SH, Kim SS, Kim BH, Lee SH, Kim YK, Kim IJ (2011) Cystatin C as an early biomarker of nephropathy in patients with type 2 diabetes. J Korean Med Sci 26:258–263

    Article  CAS  Google Scholar 

  • Jiang Y, Jolly PE, Preko P, Wang JS, Ellis WO, Phillips TD, Williams JH (2008) Aflatoxin-related immune dysfunction in health and in human immunodeficiency virus disease. Clin Dev Immunol 2008:790309

    Article  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 

  • Johnson NM, Qian G, Xu L, Tietze D, Marroquin-Cardona A, Robinson A, Rodriguez M, Kaufman L, Cunningham K, Wittmer J, Guerra F, Donnelly KC, Williams JH, Wang JS, Phillips TD (2010) Aflatoxin and PAH exposure biomarkers in a U.S. population with a high incidence of hepatocellular carcinoma. Sci Total Environ 408:6027–6031

    Article  CAS  Google Scholar 

  • Kang MS, Nkurunziza P, Muwanika R, Qian G, Tang L, Song X, Xue K, Nkwata A, Ssempebwa J, Lutalo T, Asiki G, Serwadda D, Seeley J, Kaleebu P, Nalugoda F, Newton R, William JH, Wang JS (2015) Longitudinal evaluation of aflatoxin exposure in two cohorts in south-western Uganda. Food Addit Contam Part A Chem Anal Control Expo Risk Assess 32:1322–1330

    Article  CAS  Google Scholar 

  • Kataria A, Trasande L, Trachtman H (2015) The effects of environmental chemicals on renal function. Nat Rev Nephrol 11:610–625

    Article  CAS  Google Scholar 

  • KDIGO (2013) Kidney Disease: Improving Global Outcomes (KDIGO). Official Journal of the International Society of Nephrology 3(1):1–150

    Google Scholar 

  • Kensler TW, Roebuck BD, Wogan GN, Groopman JD (2011) Aflatoxin: a 50-year odyssey of mechanistic and translational toxicology. Toxicol Sci 120(Suppl 1):S28–S48

    Article  CAS  Google Scholar 

  • Kim SS, Song SH, Kim IJ, Yang JY, Lee JG, Kwak IS, Kim YK (2012) Clinical implication of urinary tubular markers in the early stage of nephropathy with type 2 diabetic patients. Diabetes Res Clin Pract 97:251–257

    Article  CAS  Google Scholar 

  • Kumar P, Mahato DK, Kamle M, Mohanta TK, Kang SG (2017) Aflatoxins: a global concern for food safety, human health and their management. Front Microbiol 7

  • Leem AY, Park MS, Park BH, Jung WJ, Chung KS, Kim SY, Kim EY, Jung JY, Kang YA, Kim YS, Kim SK, Chang J, Song JH (2017) Value of serum cystatin C measurement in the diagnosis of sepsis-induced kidney injury and prediction of renal function recovery. Yonsei Med J 58:604–612

    Article  CAS  Google Scholar 

  • Leroy JL, Wang JS, Jones K (2015) Serum aflatoxin B-1-lysine adduct level in adult women from Eastern Province in Kenya depends on household socio-economic status: a cross sectional study. Soc Sci Med 146:104–110

    Article  Google Scholar 

  • Liao CM, Chen SC (2005) A probabilistic modeling approach to assess human inhalation exposure risks to airborne aflatoxin B-1 (AFB(1)). Atmos Environ 39:6481–6490

    Article  CAS  Google Scholar 

  • Malik A, Ali S, Shahid M, Bhargava R (2014) Occupational exposure to Aspergillus and aflatoxins among food-grain workers in India. Int J Occup Env Health 20:189–193

    Article  CAS  Google Scholar 

  • McCoy LF, Scholl PF, Schleicher RL, Groopman JD, Powers CD, Pfeiffer CM (2005) Analysis of aflatoxin B1-lysine adduct in serum using isotope-dilution liquid chromatography/tandem mass spectrometry. Rapid Commun Mass Spectrom 19:2203–2210

    Article  CAS  Google Scholar 

  • McMillan A, Renaud JB, Burgess KMN, Orimadegun AE, Akinyinka OO, Allen SJ, Miller JD, Reid G, Sumarah MW (2018) Aflatoxin exposure in Nigerian children with severe acute malnutrition. Food Chem Toxicol 111:356–362

    Article  CAS  Google Scholar 

  • Mendoza JR, Rodas A, Oliva A, Sabillon L, Colmenares A, Clarke J, Hallen-Adams HE, Campabadal C, Bianchini A (2018) Safety and quality assessment of smallholder farmers’ maize in the Western Highlands of Guatemala. J Food Prot 81:776–784

    Article  CAS  Google Scholar 

  • Mitchell NJ, Bowers E, Hurburgh C, Wu F (2016) Potential economic losses to the US corn industry from aflatoxin contamination. Food Addit Contam A 33:540–550

    Article  CAS  Google Scholar 

  • Mohamed F, Endre Z, Jayamanne S, Pianta T, Peake P, Palangasinghe C, Chathuranga U, Jayasekera K, Wunnapuk K, Shihana F, Shahmy S, Buckley N (2015) Mechanisms underlying early rapid increases in creatinine in paraquat poisoning. PLoS One 10:e0122357

    Article  CAS  Google Scholar 

  • Mohd Redzwan S, Rosita J, Mohd Sokhini AM, Nurul ‘Aqilah AR, Wang JS, Kang MS, Zuraini A (2014) Detection of serum AFB1-lysine adduct in Malaysia and its association with liver and kidney functions. Int J Hyg Environ Health 217:443–451

    Article  CAS  Google Scholar 

  • Ordunez P, Silva LC (2014) Pesticides and the epidemic of CKD in Central America. Am J Kidney Dis 64:477

    Article  Google Scholar 

  • Ortega-Beltran A, Guerrero-Herrera MD, Ortega-Corona A, Vidal-Martinez VA, Cotty PJ (2014) Susceptibility to aflatoxin contamination among maize landraces from Mexico. J Food Prot 77:1554–1562

    Article  CAS  Google Scholar 

  • Ortega-Beltran A, Jaime R, Cotty PJ (2015) Aflatoxin-producing fungi in maize field soils from sea level to over 2000 masl: a three year study in Sonora, Mexico. Fungal Biol 119:191–200

    Article  Google Scholar 

  • Oyelami OA, Maxwell SM, Adelusola KA, Aladekoma TA, Oyelese AO (1998) Aflatoxins in autopsy kidney specimens from children in Nigeria. J Toxicol Environ Health A 55:317–323

    Article  CAS  Google Scholar 

  • Park JW, Kim EK, Shon DH, Kim YB (2002) Natural co-occurrence of aflatoxin B1, fumonisin B1 and ochratoxin A in barley and corn foods from Korea. Food Addit Contam 19:1073–1080

    Article  CAS  Google Scholar 

  • Plasencia J (2004) Aflatoxins in maize: a Mexican perspective. J Toxicol-Toxin Rev 23:155–177

    Article  CAS  Google Scholar 

  • Poreba R, Gac P, Poreba M, Antonowicz-Juchniewicz J, Andrzejak R (2011) Relation between occupational exposure to lead, cadmium, arsenic and concentration of cystatin C. Toxicology 283:88–95

    Article  CAS  Google Scholar 

  • Rached E, Hoffmann D, Blumbach K, Weber K, Dekant W, Mally A (2008) Evaluation of putative biomarkers of nephrotoxicity after exposure to ochratoxin a in vivo and in vitro. Toxicol Sci 103:371–381

    Article  CAS  Google Scholar 

  • Rastogi R, Srivastava AK, Rastogi AK (2001) Long term effect of aflatoxin B(1) on lipid peroxidation in rat liver and kidney: effect of picroliv and silymarin. Phytother Res 15:307–310

    Article  CAS  Google Scholar 

  • Rati ER, Shantha T, Ramesh HP (1991) Effect of long term feeding and withdrawal of aflatoxin B1 and ochratoxin A on kidney cell transformation in albino rats. Indian J Exp Biol 29:813–817

    CAS  Google Scholar 

  • Redzwan SM, Abd Mutalib MS, Wang JS, Ahmad Z, Kang MS, Rahman NAA, Nasrabadi EN, Jamaluddin R (2016) Effect of supplementation of fermented milk drink containing probiotic Lactobacillus casei Shirota on the concentrations of aflatoxin biomarkers among employees of Universiti Putra Malaysia: a randomised, double-blind, cross-over, placebo-controlled study. Brit J Nutr 115:39–54

    Article  CAS  Google Scholar 

  • Sass DC, Jager AV, Tonin FG, Rosim RE, Constantino MG, Oliveira CAF (2015) Synthesis and purification of the aflatoxin B-1-lysine adduct. Toxin Rev 34:53–59

    Article  CAS  Google Scholar 

  • Scholl PF (2004) Development of a quantitative LC-MS method for the analysis of aflatoxin B1 serum albumin adducts. Chem Res Toxicol 17:1764–1764

    Google Scholar 

  • Scholl PF, Groopman JD (2008) Long-term stability of human aflatoxin B1 albumin adducts assessed by isotope dilution mass spectrometry and high-performance liquid chromatography-fluorescence. Cancer Epidemiol Biomark Prev 17:1436–1439

    Article  CAS  Google Scholar 

  • Seetha A, Monyo ES, Tsusaka TW, Msere HW, Madinda F, Chilunjika T, Sichone E, Mbughi D, Chilima B, Matumba L (2018) Aflatoxin-lysine adducts in blood serum of the Malawian rural population and aflatoxin contamination in foods (groundnuts, maize) in the corresponding areas. Mycotoxin Res 34:195–204

    Article  CAS  Google Scholar 

  • Shuaib FMB et al (2010) Association between anemia and aflatoxin B-1 biomarker levels among pregnant women in Kumasi, Ghana. Am J Trop Med Hyg 83:1077–1083. https://doi.org/10.4269/ajtmh.2010.09.0772

  • Smith JW, Kroker-Lobos MF, Lazo M, Rivera-Andrade A, Egner PA, Wedemeyer H, Torres O, Freedman ND, McGlynn KA, Guallar E, Groopman JD, Ramirez-Zea M (2017) Aflatoxin and viral hepatitis exposures in Guatemala: molecular biomarkers reveal a unique profile of risk factors in a region of high liver cancer incidence. PLoS One 12:e0189255

    Article  CAS  Google Scholar 

  • SSA (2003) NORMA Oficial Mexicana NOM-187-SSA1/SCFI-2002, Productos y servicios. Masa, tortillas, tostadas y harinas preparadas para su elaboración y establecimientos donde se procesan. Especificaciones sanitarias. Información comercial. Métodos de prueba. In: Salud Sd (Hrsg.), Mexico

  • Suarez-Bonnet E, Carvajal M, Mendez-Ramirez I, Castillo-Urueta P, Cortes-Eslava J, Gomez-Arroyo S, Melero-Vara JM (2013) Aflatoxin (B1, B2, G1, and G2 ) contamination in rice of Mexico and Spain, from local sources or imported. J Food Sci 78:T1822–T1829

    Article  CAS  Google Scholar 

  • Torres C, Aragon A, Gonzalez M, Lopez I, Jakobsson K, Elinder CG, Lundberg I, Wesseling C (2010) Decreased kidney function of unknown cause in Nicaragua: a community-based survey. Am J Kidney Dis 55:485–496

    Article  Google Scholar 

  • Vaidya VS, Waikar SS, Ferguson MA, Collings FB, Sunderland K, Gioules C, Bradwin G, Matsouaka R, Betensky RA, Curhan GC, Bonventre JV (2008) Urinary biomarkers for sensitive and specific detection of acute kidney injury in humans. Clin Transl Sci 1:200–208

    Article  CAS  Google Scholar 

  • van Timmeren MM, van den Heuvel MC, Bailly V, Bakker SJ, van Goor H, Stegeman CA (2007) Tubular kidney injury molecule-1 (KIM-1) in human renal disease. J Pathol 212:209–217

    Article  CAS  Google Scholar 

  • Velazquez WR, Martinez SP, Espinosa VHI, Vera MAN, Palacios ED, Rojo F (2009) Total aflatoxins in cows feed and AFM(1) in milk in dairy herds from Jalisco State, Mexico. Tec Pecu Mex 47:223–230

    Google Scholar 

  • Voth-Gaeddert LE, Stoker M, Cornell D, Oerther DB (2018a) What causes childhood stunting among children of San Vicente, Guatemala: employing complimentary, system-analysis approaches. Int J Hyg Environ Health 221:391–399

    Article  Google Scholar 

  • Voth-Gaeddert LE, Stoker M, Torres O, Oerther DB (2018b) Association of aflatoxin exposure and height-for-age among young children in Guatemala. Int J Environ Health Res:1–13

  • Wild CP, Garner RC, Montesano R, Tursi F (1986) Aflatoxin-B1 binding to plasma-albumin and liver DNA upon chronic administration to rats. Carcinogenesis 7:853–858

    Article  CAS  Google Scholar 

  • Wild CP, Hudson GJ, Sabbioni G, Chapot B, Hall AJ, Wogan GN, Whittle H, Montesano R, Groopman JD (1992) Dietary-intake of aflatoxins and the level of albumin-bound aflatoxin in peripheral-blood in the Gambia, West Africa. Cancer Epidem Biomar 1:229–234

    CAS  Google Scholar 

  • Xu L, Qian G, Tang L, Su J, Wang JS (2010) Genetic variations of hepatitis B virus and serum aflatoxin-lysine adduct on high risk of hepatocellular carcinoma in Southern Guangxi, China. J Hepatol 53:671–676

    Article  CAS  Google Scholar 

  • Yard EE, Daniel JH, Lewis LS, Rybak ME, Paliakov EM, Kim AA, Montgomery JM, Bunnell R, Abudo MU, Akhwale W, Breiman RF, Sharif SK (2013) Human aflatoxin exposure in Kenya, 2007: a cross-sectional study. Food Addit Contam Part A Chem Anal Control Expo Risk Assess 30:1322–1331

    Article  CAS  Google Scholar 

  • Yashiro M, Kamata T, Segawa H, Kadoya Y, Murakami T, Muso E (2009) Comparisons of cystatin C with creatinine for evaluation of renal function in chronic kidney disease. Clin Exp Nephrol 13:598–604

    Article  CAS  Google Scholar 

  • Zuki-Orozco BA, Batres-Esquivel LE, Ortiz-Perez MD, Juarez-Flores BI, Martinez FDB (2016) Determination of aflatoxins B1, B2, G1 and G2 in tortillas from a rural community in San Luis Potosi, Mexico. Toxicol Lett 259:S135–S135

    Article  Google Scholar 

Download references

Funding

This research received grants and fellowships from the National Council for Science and Technology National Problems (# 2015-1340).

Author information

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, Mexico

    Lorena Díaz de León-Martínez, Fernando Díaz-Barriga & Francisco Pérez-Vázquez

  2. Departamento de Toxicología, Centro de Investigación y de Estudios Avanzados-Instituto Politécnico Nacional (CINVESTAV-IPN), Mexico City, Mexico

    Olivier Barbier & Manolo Ortega-Romero

  3. Departamento de Biotecnología y Bioquímica Centro de Investigación de Estudios Avanzados del -Instituto Politécnico Nacional (CINVESTAV-IPN), Campus Guanajuato, Irapuato, Mexico

    Dora Linda Guzmán Ortíz

  4. 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, Mexico

    Rogelio Flores-Ramírez

Authors
  1. Lorena Díaz de León-Martínez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fernando Díaz-Barriga
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Olivier Barbier
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dora Linda Guzmán Ortíz
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Manolo Ortega-Romero
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Francisco Pérez-Vázquez
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Rogelio Flores-Ramírez
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rogelio Flores-Ramírez.

Ethics declarations

The study was approved by the bioethics committee of the Faculty of Medicine of the Autonomous University of San Luis Potosí.

Additional information

Responsible editor: Philippe Garrigues

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Díaz de León-Martínez, L., Díaz-Barriga, F., Barbier, O. et al. 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 (2019). https://doi.org/10.1007/s11356-019-04634-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-019-04634-z

Keywords

Search

Navigation