Advertisement

Biological Trace Element Research

, Volume 153, Issue 1–3, pp 145–154 | Cite as

Mercury (Hg) Exposure in Breast-Fed Infants and Their Mothers and the Evidence of Oxidative Stress

  • Iman Al-Saleh
  • Mai Abduljabbar
  • Reem Al-Rouqi
  • Rola Elkhatib
  • Ammar Alshabbaheen
  • Neptune Shinwari
Article

Abstract

The objective of this work was to assess exposure to mercury (Hg) and its induction of oxidative stress in 155 healthy lactating Saudi mothers and their infants. Samples of breast milk and blood were collected from the mothers, while urine was taken from both infants and mothers. Both urinary 8-hydroxy-2′-deoxyguanosine (8-OHdG) and malondialdehyde (MDA) were measured in mothers and infants as biomarkers of oxidative stress. The mean concentration of Hg in breast milk was 1.19 μg/L (range 0.012–6.44 μg/L) with only one mother having Hg >4 μg/L, the upper limit established by the US Agency for Toxic Substance and Disease Registry. However, 57.4 % had Hg ≥1 μg/L, the background level for Hg in human milk. The mean urinary Hg corrected for creatinine (Hg-C) in mothers and infants was 1.47 and 7.90 μg/g creatinine, respectively, with a significant correlation between the two (p < 0.001). Urinary Hg levels over 5 μg/g creatinine (the background level in an unexposed population) were found in 3.3 % of mothers and 50.1 % of infants. None of the mothers had total blood Hg above the US Environmental Protection Agency’s maximum reference dose of 5.8 μg/L. No correlation was noted between urinary Hg in infants and Hg in breast milk (p > 0.05). Hg in breast milk, though, was associated with Hg in blood (p < 0.001), suggesting the efficient transfer of Hg from blood to milk. Hg in the breast milk of mothers and in the urine of infants affected the excretion of urinary MDA and 8-OHdG, respectively, in a dose-related manner. These findings reveal for the first time lactational exposure to Hg-induced oxidative stress in breast-fed infants, which may play a role in pathogenesis, particularly during neurodevelopment. This will also contribute to the debate over the benefits of breast milk versus the adverse effects of exposure to pollutants. Nevertheless, breastfeeding should not be discouraged, but efforts should be made to identify and eliminate the source of Hg exposure in the population.

Keywords

Mercury (Hg) Lactating women Oxidative stress Breast milk Urine Blood 

Notes

Acknowledgments

The investigators thank King Abdulaziz City for Science and Technology (ARP-29-23) for funding this study. We would like to thank all the women who participated in this study and the staff of primary health-care units in Riyadh.

References

  1. 1.
    World Health Organization, WHO (1990) Methylmercury. In: Environmental health criteria 101. WHO, GenevaGoogle Scholar
  2. 2.
    World Health Organization, WHO (2003) CICAD 50. Elemental mercury and inorganic mercury compounds: human health aspects. IPCS, World Health Organization, Geneva, SwitzerlandGoogle Scholar
  3. 3.
    Chan TY (2011) Inorganic mercury poisoning associated with skin-lightening cosmetic products. Clin Toxicol (Phila) 49:886–891CrossRefGoogle Scholar
  4. 4.
    Clarkson TW, Magos L (2006) The toxicology of mercury and its chemical compounds. Crit Rev Toxicol 36:609–662PubMedCrossRefGoogle Scholar
  5. 5.
    Dorea JG (2004) Mercury and lead during breast-feeding. Br J Nutr 92:21–40PubMedCrossRefGoogle Scholar
  6. 6.
    Stein J, Schettler T, Wallinga D, Valenti M (2002) In harm’s way: toxic threats to child development. J Dev Behav Pediatr 23(1 Suppl):S13–S22PubMedCrossRefGoogle Scholar
  7. 7.
    Daston G, Faustman E, Ginsberg G, Fenner-Crisp P, Olin S, Sonawane B, Bruckner J, Breslin W, McLaughlin TJ (2004) A framework for assessing risks to children from exposure to environmental agents. Environ Health Perspect 112:238–256PubMedCrossRefGoogle Scholar
  8. 8.
    Valko M, Morris H, Cronin MT (2005) Metals, toxicity and oxidative stress. Curr Med Chem 12:1161–1208PubMedCrossRefGoogle Scholar
  9. 9.
    Ercal N, Gurer-Orhan H, Aykin-Burns N (2001) Toxic metals and oxidative stress part I: mechanisms involved in metal-induced oxidative damage. Curr Top Med Chem 1:529–539PubMedCrossRefGoogle Scholar
  10. 10.
    Gobe G, Crane D (2010) Mitochondria, reactive oxygen species and cadmium toxicity in the kidney. Toxicol Lett 198:49–55PubMedCrossRefGoogle Scholar
  11. 11.
    Roberts RA, Smith RA, Safe S, Szabo C, Tjalkens RB, Robertson FM (2010) Toxicological and pathophysiological roles of reactive oxygen and nitrogen species. Toxicology 276:85–94PubMedCrossRefGoogle Scholar
  12. 12.
    Hwang ES, Kim GH (2007) Biomarkers for oxidative stress status of DNA, lipids, and proteins in vitro and in vivo cancer research. Toxicology 229:1–10PubMedCrossRefGoogle Scholar
  13. 13.
    Valavanidis A, Vlachogianni T, Fiotakis C (2009) 8-hydroxy-2′-deoxyguanosine (8-OHdG): a critical biomarker of oxidative stress and carcinogenesis. J Environ Sci Health C Environ Carcinog Ecotoxicol Rev 27:120–139PubMedCrossRefGoogle Scholar
  14. 14.
    Del Rio D, Stewart AJ, Pellegrini N (2005) A review of recent studies on malondialdehyde as toxic molecule and biological marker of oxidative stress. Nutr Metab Cardiovasc Dis 15:316–228PubMedCrossRefGoogle Scholar
  15. 15.
    Crespo-López ME, Macêdo GL, Pereira SI, Arrifano GP, Picanço-Diniz DL, do Nascimento JL, Herculano AM (2009) Mercury and human genotoxicity: critical considerations and possible molecular mechanisms. Pharmacol Res 60:212–220PubMedCrossRefGoogle Scholar
  16. 16.
    Ceccatelli S, Daré E, Moors M (2010) Methylmercury-induced neurotoxicity and apoptosis. Chem Biol Interact 188:301–308PubMedCrossRefGoogle Scholar
  17. 17.
    Houston MC (2011) Role of mercury toxicity in hypertension, cardiovascular disease, and stroke. J Clin Hypertens (Greenwich) 13:621–627CrossRefGoogle Scholar
  18. 18.
    Al-Saleh I, Al anoud Al-Sedairi A, Elkhatib R (2012) Effect of mercury (Hg) dental amalgam fillings on renal and oxidative stress biomarkers in children. Sci Total Environ 431:188–196PubMedCrossRefGoogle Scholar
  19. 19.
    Asikainen TM, Raivio KO, Saksela M, Kinnula VL (1998) Expression and developmental profile of antioxidant enzymes in human lung and liver. Am J Respir Cell Mol Biol 19:942–949PubMedCrossRefGoogle Scholar
  20. 20.
    Auten RL, Davis JM (2009) Oxygen toxicity and reactive oxygen species: the devil is in the details. Pediatr Res 66:121–127PubMedCrossRefGoogle Scholar
  21. 21.
    Jensen AA (1991) Levels and trends of environmental chemicals in human milk. In: Jensen AA, Slorach SA (eds) Chemical contaminants in human milk. CRC, Boca Raton, pp 45–198Google Scholar
  22. 22.
    Al-Saleh I, Al-Doush I (1997) Mercury content in skin-lightening creams and potential hazards to the health of Saudi Women. J Toxicol Environ Health 51:123–130PubMedGoogle Scholar
  23. 23.
    Food and Drug Administration, FDA (1992) FDA’s cosmetics handbook. U.S. Department of Health and Human Services, Public Health Service, Food and Drug AdministrationGoogle Scholar
  24. 24.
    Al-Saleh I, Shinwari N, Mashhour A, Mohamed G, Rabah A (2011) Heavy metals (lead, cadmium and mercury) in maternal, cord blood and placenta of healthy women. Int J Hyg Environ Health 214:79–101PubMedCrossRefGoogle Scholar
  25. 25.
    Wilhelm M, Ewers U, Schulz C (2004) Revised and new reference values for some trace elements in blood and urine for human biomonitoring in environmental medicine. Int J Hyg Environ Health 207:69–73PubMedCrossRefGoogle Scholar
  26. 26.
    Sly PD, Flack F (2008) Susceptibility of children to environmental pollutants. Ann NY Acad Sci 1140:163–183PubMedCrossRefGoogle Scholar
  27. 27.
    Castoldi AF, Johansson C, Onishchenko N, Coccini T, Roda E, Vahter M, Ceccatelli S, Manzo L (2008) Human developmental neurotoxicity of methylmercury: Impact of variables and risk modifiers. Reg Toxicol Pharmacol 51:201–214CrossRefGoogle Scholar
  28. 28.
    Karagas MR, Choi AL, Oken E, Horvat M, Schoeny R, Kamai E, Cowell W, Grandjean P, Korrick S (2012) Evidence on the human health effects of low-level methylmercury exposure. Environ Health Perspect 120:799–806PubMedCrossRefGoogle Scholar
  29. 29.
    Myers GJ, Thurston SW, Pearson AT, Davidson PW, Cox C, Shamlaye CF, Cernichiari E, Clarkson TW (2009) Postnatal exposure to methyl mercury from fish consumption: a review and new data from the Seychelles Child Development Study. Neurotoxicology 30:338–349PubMedCrossRefGoogle Scholar
  30. 30.
    Al-Saleh I, Al-Sedairi A (2011) Mercury (Hg) burden in children: the impact of dental amalgam. Sci Total Environ 409:3003–3015PubMedCrossRefGoogle Scholar
  31. 31.
    Fukunaga K, Yoshida M, Nakazona N (1998) A simple, rapid, highly sensitive and reproducible quantitation method for plasma malonialdehyde by high-performance liquid chromatography. Biomed Chromatogr 12:300–303PubMedCrossRefGoogle Scholar
  32. 32.
    Agency for Toxic Substances and Disease Registry, ATSDR (1999) Report no.: CAS# 7439-97-6. http://www.atsdr.cdc.gov/toxprofiles/tp.asp?id=115&tid=24. Accessed 20 Jan 2013
  33. 33.
    Al-Saleh I, Shinwari N, Mashhour A (2003) Heavy metals concentrations in the breast milk of Saudi women. Biol Trace Elem Res 96:21–38PubMedCrossRefGoogle Scholar
  34. 34.
    da Cunha LR, da Costa TH, Caldas ED (2013) Mercury concentration in breast milk and infant exposure assessment during the first 90 days of lactation in a midwestern region of Brazil. Biol Trace Elem Res 151:30–37PubMedCrossRefGoogle Scholar
  35. 35.
    Orün E, Yalçin SS, Aykut O, Orhan G, Koç-Morgil G, Yurdakök K, Uzun R (2012) Mercury exposure via breast-milk in infants from a suburban area of Ankara, Turkey. Turk J Pediatr 54:136–143PubMedGoogle Scholar
  36. 36.
    Goudarzi MA, Parsaei P, Nayebpour F, Rahimi E (2012) Determination of mercury, cadmium and lead in human milk in Iran. Toxicol Ind Health. doi: 10.1177/0748233712445047. PubMed PMID: 22534496
  37. 37.
    García-Esquinas E, Pérez-Gómez B, Fernández MA, Pérez-Meixeira AM, Gil E, de Paz C, Iriso A, Sanz JC, Astray J, Cisneros M, de Santos A, Asensio A, García-Sagredo JM, García JF, Vioque J, Pollán M, López-Abente G, González MJ, Martínez M, Bohigas PA, Pastor R, Aragonés N (2011) Mercury, lead and cadmium in human milk in relation to diet, lifestyle habits and sociodemographic variables in Madrid (Spain). Chemosphere 85:268–276PubMedCrossRefGoogle Scholar
  38. 38.
    Jensen AA (1983) Chemical contaminants in human milk. Residue Rev 89:1–127PubMedCrossRefGoogle Scholar
  39. 39.
    Whitehead RG, Paul AA (2000) Long-term adequacy of exclusive breast-feeding: how scientific research has led to revised opinions. Proc Nutr Soc 59:17–23PubMedCrossRefGoogle Scholar
  40. 40.
    United States Environmental Protection Agency, US EPA (1997) Mercury study report to congress. Volume v: health effects of mercury and mercury compounds. Office of Air Quality Planning and Standards and Office of Research and Development, Washington, DC. http://www.epa.gov/ttn/atw/112nmerc/volume5.pdf. Accessed 20 Jan 2013
  41. 41.
    Boischio AA, Henshel D (2000) Fish consumption, fish lore, and mercury pollution-risk communication for the Madeira River people. Environ Res 84:108–126PubMedCrossRefGoogle Scholar
  42. 42.
    United States Environmental Protection Agency, US EPA (2007) Mercury. Human exposure. http://www.epa.gov/mercury/exposure.htm. Accessed 20 Jan 2013
  43. 43.
    McKelvey W, Jeffery N, Clark N, Kass D, Parsons PJ (2011) Population-based inorganic mercury biomonitoring and the identification of skin care products as a source of exposure in New York City. Environ Health Perspect 119:203–209PubMedCrossRefGoogle Scholar
  44. 44.
    Watson GE, Evans K, Thurston SW, van Wijngaarden E, Wallace JM, McSorley EM, Bonham MP, Mulhern MS, McAfee AJ, Davidson PW, Shamlaye CF, Strain JJ, Love T, Zareba G, Myers GJ (2012) Prenatal exposure to dental amalgam in the Seychelles Child Development Nutrition Study: associations with neurodevelopmental outcomes at 9 and 30 months. Neurotoxicology 33:1511–1517PubMedCrossRefGoogle Scholar
  45. 45.
    Valent F, Horvat M, Sofianou-Katsoulis A, Spiric Z, Mazej D, Little D, Prasouli A, Mariuz M, Tamburlini G, Nakou S, Barbone F (2013) Neurodevelopmental effects of low-level prenatal mercury exposure from maternal fish consumption in a Mediterranean cohort: study rationale and design. J Epidemiol 23:146–152PubMedCrossRefGoogle Scholar
  46. 46.
    Sundberg J, Jönsson S, Karlsson MO, Hallén IP, Oskarsson A (1998) Kinetics of methylmercury and inorganic mercury in lactating and nonlactating mice. Toxicol Appl Pharmacol 151:319–329PubMedCrossRefGoogle Scholar
  47. 47.
    Björnberg KA, Vahter M, Berglund B, Niklasson B, Blennow M, Sandborgh-Englund G (2005) Transport of methylmercury and inorganic mercury to the fetus and breast-fed infant. Environ Health Perspect 113:1381–1385PubMedCrossRefGoogle Scholar
  48. 48.
    Vahter M, Akesson A, Lind B, Björs U, Schütz A, Berglund M (2000) Longitudinal study of methylmercury and inorganic mercury in blood and urine of pregnant and lactating women, as well as in umbilical cord blood. Environ Res 84:186–194PubMedCrossRefGoogle Scholar
  49. 49.
    Wong YT, Ruan R, Tay FE (2006) Relationship between levels of oxidative DNA damage, lipid peroxidation and mitochondrial membrane potential in young and old F344 rats. Free Radic Res 40:393–402PubMedCrossRefGoogle Scholar
  50. 50.
    Canakci CF, Cicek Y, Yildirim A, Sezer U, Canakci V (2009) Increased levels of 8-hydroxydeoxyguanosine and malondialdehyde and its relationship with antioxidant enzymes in saliva of periodontitis patients. Eur J Dent 3:100–106PubMedGoogle Scholar
  51. 51.
    Marnett LJ (1999) Lipid peroxidation—DNA damage by malondialdehyde. Mutat Res 424:83–95PubMedCrossRefGoogle Scholar
  52. 52.
    Park JW, Floyd RA (1992) Lipid peroxidation products mediate the formation of 8-hydroxydeoxyguanosine in DNA. Free Radic Biol Med 12:245–250PubMedCrossRefGoogle Scholar
  53. 53.
    Mead MN (2008) Contaminants in human milk: weighing the risks against the benefits of breastfeeding. Environ Health Perspect 116:A427–A434PubMedGoogle Scholar
  54. 54.
    Section on Breastfeeding (2012) Breastfeeding and the use of human milk. Pediatrics 129:29(3):e827–841Google Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Iman Al-Saleh
    • 1
  • Mai Abduljabbar
    • 1
  • Reem Al-Rouqi
    • 1
  • Rola Elkhatib
    • 1
  • Ammar Alshabbaheen
    • 1
  • Neptune Shinwari
    • 1
  1. 1.Environmental Health Section, Biological and Medical Research DepartmentKing Faisal Specialist Hospital and Research CentreRiyadhSaudi Arabia

Personalised recommendations