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Enzymatic Activity of Glutathione S-Transferase and Dental Fluorosis Among Children Receiving Two Different Levels of Naturally Fluoridated Water

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Abstract

This study was conducted to measure the activity of the enzyme glutathione S-transferase (GST) in saliva and to compare the activity of this enzyme in children with and without dental fluorosis in communities with different concentrations of naturally fluoridated water. A total of 141 schoolchildren participated in this cross-sectional study. Children were selected from two communities: one with a low (0.4 ppm) and the other with a high (1.8 ppm) water fluoride concentration. Dental fluorosis was evaluated by applying the Thylstrup and Fejerskov Index (TFI) criteria. Stimulated saliva was obtained, and fluoride concentration and GST activity were measured. The GST activity was compared among children with different levels of dental fluorosis using multinomial logistic regression models and odds ratios (OR). The mean age of the children was 10.6 (±1.03) years. Approximately half of the children showed dental fluorosis (52.5 %). The average GST activity was 0.5678 (±0.1959) nmol/min/μg. A higher concentration of fluoride in the saliva was detected in children with a higher GST activity (p = 0.039). A multinomial logistic regression model used to evaluate the GST activity and the dental fluorosis score identified a strong association between TFI = 2–3 (OR = 15.44, p = 0.007) and TFI ≥ 4 (OR = 55.40, p = 0.026) and the GST activity level, compared with children showing TFI = 0–1, adjusted for age and sex. Schoolchildren with higher levels of dental fluorosis and a higher fluoride concentration in the saliva showed greater GST activity. The increased GST activity most likely was the result of the body’s need to inactivate free radicals produced by exposure to fluoride.

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Abbreviations

CAT:

Catalase

DM:

Diabetes mellitus

GPx:

Glutathione peroxidase

GSH:

Glutathione

GST:

Glutathione S-transferase

ROS:

Reactive oxygen species

SOD:

Superoxide dismutase

TFI:

Thylstrup and Fejerskov Index

WHO:

World Health Organization

References

  1. Verkerk RH (2010) The paradox of overlapping micronutrient risk and benefits obligates risk/benefit analysis. Toxicology 278:27–38

    Article  CAS  PubMed  Google Scholar 

  2. Abanto Alvarez AJ, Rezende KM, Marocho SM, Alves FB, Celiberti P, Ciamponi AL (2009) Dental fluorosis: exposure, prevention and management. Med Oral Patol Oral Cir Bucal 14(2):E103–E107

    PubMed  Google Scholar 

  3. Chouhan S, Flora SJ (2008) Effects of fluoride on the tissue oxidative stress and apoptosis in rats: biochemical assay supported by IR spectroscopy data. Toxicology 254:61–67

    Article  CAS  PubMed  Google Scholar 

  4. Denbesten P, Li W (2011) Chronic fluoride toxicity: dental fluorosis. Monogr Oral Sci 22:81–96

    Article  PubMed  PubMed Central  Google Scholar 

  5. Hartl G (2004) World Health Organization. WHO issues revised drinking water guidelines to help prevent water-related outbreaks and disease. Available from: http://www.who.int/mediacentre/news/releases/2004/pr67/en/. Accessed 10 Mar 2016

  6. Beltrán-Valladares PR, Cocom-Tun H, Casanova-Rosado JF, Vallejos-Sánchez AA, Medina-Solís CE, Maupomé G (2005) Prevalence of dental fluorosis and additional sources of exposure to fluoride as risk factors to dental fluorosis in schoolchildren of Campeche, México. Rev Investig Clin 57(4):532–539

    Google Scholar 

  7. Huizar-Álvarez R, Varela-González G, Espinoza M (2014) Groundwater flow systems and fluoride content in the water of Tenextepango, Morelos, Mexico. Rev Mex Cienc Geol 31:238–247

    Google Scholar 

  8. Barbier O, Arreola-Mendoza L, Del Razo LM (2010) Molecular mechanisms of fluoride toxicity. Chem Biol Interact 188(2):319–313

    Article  CAS  PubMed  Google Scholar 

  9. Rashid K, Sinha K, Sil PC (2013) An update on oxidative stress-mediated organ pathophysiology. Food Chem Toxicol 62:584–600

    Article  CAS  PubMed  Google Scholar 

  10. Battino M, Ferreiro MS, Gallardo I, Newman HN, Bullon P (2002) The antioxidant capacity of saliva. J Clin Periodontol 29(3):189–194

    Article  CAS  PubMed  Google Scholar 

  11. Niki E (2010) Assessment of antioxidant capacity in vitro and in vivo. Free Radic Biol Med 49(4):503–515

    Article  CAS  PubMed  Google Scholar 

  12. Yuan L, Zhang L, Ma W, Zhou X, Ji J, Li N, et al. (2013) Glutathione S-transferase M1 and T1 gene polymosphisms with consumption of high fruit-juice and vegetable diet affect antioxidant capacity in healthy adults. Nutrition 29(7–8):965–971

    Article  CAS  PubMed  Google Scholar 

  13. Wei D, Zhang XL, Wang YZ, Yang CX, Chen G (2010) Lipid peroxidation levels, total oxidant status and superoxide dismutase in serum, saliva and gingival crevicular fluid in chronic periodontitis patients before and afther periodontal therapy. Aust Dent J 55(1):70–78

    Article  CAS  PubMed  Google Scholar 

  14. Livnat G, Bentur L, Kuzmisnsky E, Nagler RM (2010) Salivary profile and oxidative stress in children and adolescents with cystic fibrosis. J Oral Pathol Med 39(1):16–21

    Article  CAS  PubMed  Google Scholar 

  15. Reznick AZ, Shehadeh N, Shafir Y, Nagler RM (2006) Free radicals related effects and antioxidants in saliva and serum of adolescents with type 1 diabetes mellitus. Arch Oral Biol 51(8):640–648

    Article  CAS  PubMed  Google Scholar 

  16. Mahdy K, Abd-El-Shaheed A, Khadr ME, El-Shamy KA (2009) Antioxidant status and lipid peroxidation activity in evaluating hepatocellular damage in children. East Mediterr Health J 15(4):842–852

    CAS  PubMed  Google Scholar 

  17. Mexican Official Standard NOM-012-SSA3–2012 (2013) Establishing the criteria for the implementation of health research projects in humans. Secretary of Health, México

  18. Juárez-López M, Huizar-Álvarez R, Molina-Frechero N, Murrieta-Pruneda F, Cortés-Aguilera T (2011) Fluoride in water and dental fluorosis in a community of Queretaro state Mexico. J Environ Prot 2:744–749

    Article  Google Scholar 

  19. Mexican Official Standard NOM-127-SSA1-1994 (1995) Environmental health, water for human consumption, water quality and permissible limits and drinking water treatment. Ministry of Health, Mexico

  20. Kumar D, Pandey RK, Agrawal D, Agrawal D (2011) An estimation and evaluation of total antioxidant capacity of saliva in children with severe early childhood caries. Int J Paediatr Dent 21(6):459–464

    Article  PubMed  Google Scholar 

  21. Mandinic Z, Curcic M, Antonijevic B, Carevic M, Mandic J, Djukic-Cosic D, et al. (2010) Fluoride in drinking water and dental fluorosis. Sci Total Environ 408:3507–3512

    Article  CAS  PubMed  Google Scholar 

  22. Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139

    CAS  PubMed  Google Scholar 

  23. Gómez-Quiroz LE, Factor VM, Kaposi-Novak P, Coulouarn C, Conner EA, Thorgeirsson SS (2008) Hepatocyte-specific c-Met deletion disrupts redox homeostasis and sensitizes to Fas-mediated apoptosis. J Biol Chem 283(21):14581–14589

    Article  PubMed  PubMed Central  Google Scholar 

  24. Aoba T, Fejerskov O (2002) Dental fluorosis: chemistry and biology. Crit Rev Oral Biol Med 13(2):155–170

    Article  CAS  PubMed  Google Scholar 

  25. Avezov K, Reznick AZ, Aizenbud D (2015) Oxidative stress in the oral cavity: sources and pathological outcomes. Respir Physiol Neurobiol 209:91–94

    Article  CAS  PubMed  Google Scholar 

  26. Deponte M (2013) Glutathione catalysis and the reaction mechanisms of glutathione-dependent enzymes. Biochim Biophys Acta 1830(5):3217–3266

    Article  CAS  PubMed  Google Scholar 

  27. Flora SJ, Mittal M, Mishra D (2009) Co-exposure to arsenic and fluoride on oxidative stress, glutathione linked enzymes, biogenic amines and DNA damage in mouse brain. J Neurol Sci 285(1–2):198–205

    Article  CAS  PubMed  Google Scholar 

  28. Muchandi S, Walimbe H, Bijle MN, Nankar M, Chaturvedi S, Karekar P (2015) Comparative evaluation and correlation of salivary total antioxidant capacity and salivary pH in caries-free and severe early childhood caries children. J Contemp Dent Pract 16(3):234–237

    Article  PubMed  Google Scholar 

  29. Tulunoglu O, Demirtas S, Tulunoglu I (2006) Total antioxidant levels of saliva in children related to caries, age and gender. Int J Paediatr Dent 16(3):186–191

    Article  CAS  PubMed  Google Scholar 

  30. Da Costa LA, García-Bailo B, Badawi A, El-Sohemy A (2012) Genetic determinats of dietary antioxidant status. Prog Mol Biol Transl Sci 108:179–200

    Article  CAS  PubMed  Google Scholar 

  31. Mousny M, Omelon S, Wise L, Everett ET, Dumitriu M, Holmyard DP, et al. (2008) Fluoride effects on bone formation and mineralization are influenced by genetics. Bone 43(6):1067–1074

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Fukushima R, Pessan J, Sampaio F, Buzalaf M (2011) Factors associated with fluoride concentrations in whole and parotid ductal saliva. Caries Res 45:568–573

    Article  CAS  PubMed  Google Scholar 

  33. Varela-González G, García-Pérez A, Huizar-Álvarez R, Irigoyen-Camacho M, Espinoza-Jaramillo M (2013) Fluorosis and dental caries in the hydrogeological environments of southeastern communities in the state of Morelos, Mexico. J Environ Prot 4:994–1001

    Article  Google Scholar 

  34. Wen D, Zhang F, Zhang E, Wang C, Han S, Zheng Y (2013) Arsenic, fluoride and iodine in groundwater of China. J Geochem Explor 135:1–21

    Article  CAS  Google Scholar 

  35. Saldaña A (2013) Labor brokers in Morelos: supply of farm laborers in central and northwestern of Mexico. Estud Soc 22(43):138–158

    Google Scholar 

  36. National Institute of Statistics and Geography (INEGI) (2007) Agricultural landscape in Morelos. Agricultural census. Available from: http://internet.contenidos.inegi.org.mx/contenidos/productos//prod_serv/contenidos/espanol/bvinegi/productos/censos/agropecuario/2007/panora_agrop/mor/PanagroMor1.pdf. Accessed 07 Jun 2016

  37. Federal Commission for the Protection against Sanitary Risk, Mexico (COFEPRIS) (2015) Fertilizers and pesticides. Available from: http://www.cofepris.gob.mx/AZ/Paginas/Plaguicidas%20y%20Fertilizantes/PlaguicidasYFertilizantes.aspx. Accessed 06 Jun 2016

  38. Irigoyen-Camacho ME, García A, Mejía A, Huizar R (2016) Nutritional status and dental fluorosis among schoolchildren in communities with different drinking water fluoride concentrations in a central region in Mexico. Sci Total Environ 541:512–519

    Article  CAS  PubMed  Google Scholar 

  39. Boischio A (2013) World Health Organization. Fluoride in drinking water. Available from: http://www.paho.org/hq/index.php?option=com_content&view=article&id=8193%3A2013-fluor-agua-consumo&catid=4716%3Acontent&Itemid=39798&lang=es. Accessed 06 Jun 2016

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Acknowledgments

This research is the result of a project by Irvin Fabian Bonola Gallardo to obtain the Ph.D. degree in the Doctorado en Ciencias Biológicas y de la Salud of Universidad Autónoma Metropolitana. Irvin Fabian Bonola Gallardo was supported by grant 216553 agreement: PFP-20-93 of CONACYT-México.

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Authors and Affiliations

  1. Division of Biological Sciences and Health, Metropolitan Autonomous University, Mexico City, Mexico

    Irvin Bonola-Gallardo

  2. Department of Health Care, Metropolitan Autonomous University Xochimilco, Mexico City, Mexico

    María Esther Irigoyen-Camacho

  3. Department of Chemistry, Metropolitan Autonomous University Iztapalapa, Mexico City, Mexico

    Liliana Vera-Robles & Antonio Campero

  4. Department of Health Sciences, Metropolitan Autonomous University Iztapalapa, Mexico City, Mexico

    Luis Gómez-Quiroz

Authors
  1. Irvin Bonola-Gallardo
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  2. María Esther Irigoyen-Camacho
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  3. Liliana Vera-Robles
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  4. Antonio Campero
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  5. Luis Gómez-Quiroz
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Corresponding author

Correspondence to María Esther Irigoyen-Camacho.

Ethics declarations

The study fulfilled ethical codes (the Declaration of Helsinki and the official Mexican standard on health research [17]) and was conducted in accordance with good clinical practice standards. The study was approved by the scientific committee of the PhD Program in Biological and Health Sciences at the Autonomous Metropolitan University, Mexico. The ethical aspects of the protocol were reviewed and approved by this board (DCB.093.12).

Conflict of Interest

The authors declare that they have no competing interests.

Informed Consent

Informed consent was obtained from all individual participants included in the study.

Ethical Approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

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Bonola-Gallardo, I., Irigoyen-Camacho, M.E., Vera-Robles, L. et al. Enzymatic Activity of Glutathione S-Transferase and Dental Fluorosis Among Children Receiving Two Different Levels of Naturally Fluoridated Water. Biol Trace Elem Res 176, 40–47 (2017). https://doi.org/10.1007/s12011-016-0806-0

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  • DOI: https://doi.org/10.1007/s12011-016-0806-0

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