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Contribution of breast milk and formula to arsenic exposure during the first year of life in a US prospective cohort

Abstract

Arsenic is a carcinogen that can also affect the cardiac, respiratory, neurological and immune systems. Children have higher dietary arsenic exposure than adults owing to their more restricted diets and greater intake per unit body mass. We evaluated the potential contributions of breast milk and formula to arsenic exposure throughout the first year of life for 356 infants in the prospective New Hampshire Birth Cohort Study (NHBCS) using infant diets reported by telephone at 4, 8 and 12 months of age; measured household water arsenic concentrations; and literature data. Based on our central-tendency models, population-wide geometric mean (GM) estimated arsenic exposures in the NHBCS were relatively low, decreasing from 0.1 μg/kg/day at 4 months of age to 0.07 μg/kg/day at 12 months of age. At all three time points, exclusively formula-fed infants had GM arsenic exposures ~8 times higher than exclusively breastfed infants owing to arsenic in both tap water and formula powder. Estimated maximum exposures reached 9 μg/kg/day among exclusively formula-fed infants in households with high tap water arsenic (80 μg/l). Overall, modeled arsenic exposures via breast milk and formula were low throughout the first year of life, unless formula was prepared with arsenic-contaminated tap water.

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References

  1. Farzan SF, Karagas MR, Chen Y . In utero and early life arsenic exposure in relation to long-term health and disease. Toxicol Appl Pharmacol 2013; 272: 384–390.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Naujokas MF, Anderson B, Ahsan H, Vasken Aposhian H, Graziano JH, Thompson C et al. The broad scope of health effects from chronic arsenic exposure: update on a worldwide public health problem. Environ Health Perspect 2013; 121: 8.

    Article  Google Scholar 

  3. Rahman A, Persson LA, Nermell B, El Arifeen S, Ekstrom EC, Smith AH et al. Arsenic exposure and risk of spontaneous abortion, stillbirth, and infant mortality. Epidemiology 2010; 21: 797–804.

    Article  PubMed  Google Scholar 

  4. Vahter M . Health effects of early life exposure to arsenic. Basic Clin Pharmacol Toxicol 2008; 102: 204–211.

    Article  CAS  PubMed  Google Scholar 

  5. Roy A, Kordas K, Lopez P, Rosado JL, Cebrian ME, Vargas GG et al. Association between arsenic exposure and behavior among first-graders from Torreon, Mexico. Environ Res 2011; 111: 670–676.

    Article  CAS  PubMed  Google Scholar 

  6. Hamadani JD, Tofail F, Nermell B, Gardner R, Shiraji S, Bottai M et al. Critical windows of exposure for arsenic-associated impairment of cognitive function in pre-school girls and boys: a population-based cohort study. Int J Epidemiol 2011; 40: 1593–1604.

    Article  CAS  PubMed  Google Scholar 

  7. Kwok RK, Kaufmann RB, Jakariya M . Arsenic in drinking-water and reproductive health outcomes: a study of participants in the Bangladesh integrated nutrition programme. J Health Popul Nutr 2006; 24: 190–205.

    PubMed  Google Scholar 

  8. Steinmaus C, Ferreccio C, Acevedo J, Yuan Y, Liaw J, Duran V et al. Increased lung and bladder cancer incidence in adults after in utero and early-life arsenic exposure. Cancer Epidemiol Biomarkers Prev 2014; 23: 1529–1538.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Bodwell JE, Kingsley LA, Hamilton JW . Arsenic at very low concentrations alters glucocorticoid receptor (GR)-mediated gene activation but not GR mediated gene repression; complex dose response effects are closely correlated with levels of activated GR and require a functional GR DNA binding domain. Chem Res Toxicol 2004; 17: 1064–1076.

    Article  CAS  PubMed  Google Scholar 

  10. Farzan SF, Korrick S, Li Z, Enelow R, Gandolfi AJ, Madan J et al. In utero arsenic exposure and infant infection in a United States cohort: a prospective study. Environ Res 2013; 126: 24–30.

    Article  CAS  PubMed  Google Scholar 

  11. Argos M, Kalra T, Rathouz PJ, Chen Y, Pierce B, Parvez F et al. Arsenic exposure from drinking water, and all-cause and chronic-disease mortalities in Bangladesh (HEALS): a prospective cohort study. Lancet 2010; 376: 252–258.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Chen CJ, Wang CJ . Ecological correlation between arsenic level in well water and age-adjusted mortality from malignant neoplasms. Cancer Res 1990; 50: 5470–5474.

    CAS  PubMed  Google Scholar 

  13. Samanta G, Sharma R, Roychowdhury T, Chakraborti D . Arsenic and other elements in hair, nails, and skin-scales of arsenic victims in West Bengal, India. Sci Total Environ 2004; 326: 33–47.

    Article  CAS  PubMed  Google Scholar 

  14. Cubadda F, Aureli F, D'Amato M, Raggi A, Turco AC, Mantovani A . Speciated urinary arsenic as a biomarker of dietary exposure to inorganic arsenic in residents living in high-arsenic areas in Latium, Italy. Pure Appl Chem 2012; 84: 203–214.

    Article  CAS  Google Scholar 

  15. Karagas MR, Stukel TA, Tosteson TD . Assessment of cancer risk and environmental levels of arsenic in New Hampshire. Int J Hyg Environ Health 2002; 205: 85–94.

    Article  CAS  PubMed  Google Scholar 

  16. International Agency for Research on Cancer (IARC) Some Drinking-Water Disinfectants and Contaminants, Including Arsenic. World Health Organization: Lyon, France. 2004.

  17. Edmonds JS, Francesconi KA . Arsenic in seafoods - human health-aspects and regulations. Mar Pollut Bull 1993; 26: 665–674.

    Article  CAS  Google Scholar 

  18. Meharg A, Sun G, Williams PN, Adomako EE, Deacon C, Zhu Y-G et al. Inorganic arsenic levels in baby rice are of concern. Environ Pollut 2008; 152: 746–749.

    Article  CAS  PubMed  Google Scholar 

  19. Tseng CH . A review on environmental factors regulating arsenic methylation in humans. Toxicol Appl Pharmacol 2009; 235: 338–350.

    Article  CAS  PubMed  Google Scholar 

  20. Gosse JA, Taylor VF, Jackson BP, Hamilton JW, Bodwell JE . Monomethylated trivalent arsenic species disrupt steroid receptor interactions with their DNA response elements at non-cytotoxic cellular concentrations. J Applied Toxicol 2014; 34: 498–505.

    Article  CAS  Google Scholar 

  21. Medeiros M, Zheng X, Novak P, Wnek SM, Chyan V, Escudero-Lourdes C et al. Global gene expression changes in human urothelial cells exposed to low-level monomethylarsonous acid. Toxicology 2012; 291: 102–112.

    Article  CAS  PubMed  Google Scholar 

  22. Styblo M, Del Razo LM, Vega L, Germolec DR, LeCluyse EL, Hamilton GA et al. Comparative toxicity of trivalent and pentavalent inorganic and methylated arsenicals in rat and human cells. Arch Toxicol 2000; 74: 289–299.

    Article  CAS  PubMed  Google Scholar 

  23. Petrick JS, Ayala-Fierro F, Cullen WR, Carter DE, Vasken Aposhian H . Monomethylarsonous acid (MMA(III)) is more toxic than arsenite in Chang human hepatocytes. Toxicol Appl Pharmacol 2000; 163: 203–207.

    Article  CAS  PubMed  Google Scholar 

  24. Cohen SM, Arnold LL, Eldan M, Lewis AS, Beck BD . Methylated arsenicals: the implications of metabolism and carcinogenicity studies in rodents to human risk assessment. Crit Rev Toxicol 2006; 36: 99–133.

    Article  CAS  PubMed  Google Scholar 

  25. Cohen SM, Arnold LL, Beck BD, Lewis AS, Eldan M . Evaluation of the carcinogenicity of inorganic arsenic. Crit Rev Toxicol 2013; 43: 711–752.

    Article  CAS  PubMed  Google Scholar 

  26. European Food Safety Authority (EFSA). EFSA Panel on Contaminants in the Food Chain (CONTAM): Scientific Opinion on Arsenic in Food. EFSA J 2009; 7: 1351.

    Article  Google Scholar 

  27. Tsuji JS, Yost LJ, Barraj LM, Scrafford CG, Mink PJ . Use of background inorganic arsenic exposures to provide perspective on risk assessment results. Regul Toxicol Pharmacol 2007; 48: 59–68.

    Article  CAS  PubMed  Google Scholar 

  28. Hernandez-Martinez R, Navarro-Blasco I . Survey of total mercury and arsenic content in infant cereals marketed in Spain and estimated dietary intake. Food Control 2013; 30: 423–432.

    Article  CAS  Google Scholar 

  29. Ljung K, Palm B, Grander M, Vahter M . High concentrations of essential and toxic elements in infant formula and infant foods - a matter of concern. Food Chem 2011; 127: 943–951.

    Article  CAS  PubMed  Google Scholar 

  30. Sorbo A, Turco AC, Di Gregorio M, Ciaralli L . Development and validation of an analytical method for the determination of arsenic, cadmium and lead content in powdered infant formula by means of quadrupole inductively coupled plasma mass spectrometry. Food Control 2014; 44: 159–165.

    Article  CAS  Google Scholar 

  31. Jackson BP, Taylor VF, Punshon T, Cottingham KL . Arsenic concentration and speciation in infant formulas and first foods. Pure Appl Chem 2012; 84: 215–223.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. U.S. Food and Drug Administration. Analytical Results from Inorganic Arsenic in Rice and Rice Products Sampling. Arsenic in Rice and Rice Products. 2013; http://www.fda.gov/downloads/Food/FoodborneIllnessContaminants/Metals/UCM352467.pdf. (accessed 4 September 2015).

  33. Carignan CC, Cottingham KL, Jackson BP, Farzan SF, Gandolfi AJ, Punshon T et al. Estimated exposure to arsenic in breastfed and formula-fed infants in a United States Cohort. Environ Health Perspect 2015; 123: 500–506.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Björklund KL, Vahter M, Palm B, Grandér M, Lignell S, Berglund M . Metals and trace element concentrations in breast milk of first time healthy mothers: a biological monitoring study. Environ Health 2012; 11: 92.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Samanta G, Das D, Mandal BK, Chowdhury TR, Chakraborti D, Pal A et al. Arsenic in the breast milk of lactating women in arsenic-affected areas of West Bengal, India and its effect on infants. J Environ Sci Health A Tox Hazard Subst Environ Eng 2007; 42: 1815–1825.

    Article  CAS  PubMed  Google Scholar 

  36. Concha G, Vogler G, Nermell B, Vahter M . Low-level arsenic excretion in breast milk of native Andean women exposed to high levels of arsenic in the drinking water. Int Archiv Occup Environ Health 1998; 71: 42–46.

    Article  CAS  Google Scholar 

  37. Fängström B, Moore S, Nermell B, Kuenstl L, Goessler W, Grandér M et al. Breast-feeding protects against arsenic exposure in Bangladeshi infants. Environ Health Perspect 2008; 116: 963–969.

    Article  PubMed  PubMed Central  Google Scholar 

  38. Sternowsky HJ, Moser B, Szadkowsky D . Arsenic in breast milk during the first 3 months of lactation. Int J Hyg Environ Health 2002; 205: 405–409.

    Article  CAS  PubMed  Google Scholar 

  39. Islam MR, Attia J, Alauddin M, McEvoy M, McElduff P, Slater C et al. Availability of arsenic in human milk in women and its correlation with arsenic in urine of breastfed children living in arsenic contaminated areas in Bangladesh. Environ Health 2014; 13: 101.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Vahter ME, Li L, Nermell B, Rahman A, El Arifeen S, Rahman M et al. Arsenic exposure in pregnancy: a population-based study in Matlab, Bangladesh. J Health Popul Nutr 2006; 24: 236–245.

    PubMed  Google Scholar 

  41. Centers for Disease Control and Prevention (CDC). Breastfeeding Report Card, United States, 2013. Centers for Disease Control and Prevention, National Center for Chronic Disease Prevention and Health Promotion, Division of Nutrition, Physical Activity and Obesity. http://www.cdc.gov/breastfeeding/pdf/2013breastfeedingreportcard.pdf.

  42. Gilbert-Diamond D, Cottingham KL, Gruber JF, Punshon T, Sayarath V, Gandolfi AJ et al. Rice consumption contributes to arsenic exposure in US women. Proc Natl Acad Sci USA 2011; 108: 20656–20660.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. U.S. Environmental Protection Agency (US EPA) Child-Specific Exposure Factors Handbook (Final Report). U.S. Environmental Protection Agency: Washington, DC, USA. 2008. http://cfpub.epa.gov/ncea/cfm/recordisplay.cfm?deid=1992432008.

  44. U.S. Environmental Protection Agency. Chronic Health Hazard Assessments for Noncarcinogenic Effects, Reference Dose for Chronic Oral Exposure (RfD). Integrated Risk Information System (IRIS) on inorganic arsenic. Verification date February 3, 1994. http://www.epa.gov/iris/subst/0278.htm.

  45. National Research Council Critical Aspects of EPA's IRIS Assessment of Inorganic Arsenic: Interim Report. National Academies Press: Washington, DC, USA. 2013. http://www.nap.edu/catalog.php?record_id=18594.

  46. Josyula AB, McClellen H, Hysong TA, Kurzius-Spencer M, Poplin GS, Sturup S et al. Reduction in urinary arsenic with bottled-water intervention. J Health Popul Nutr 2006; 24: 298–304.

    PubMed  PubMed Central  Google Scholar 

  47. Meharg AA, Sun GX, Williams PN, Adomako E, Deacon C, Zhu YG et al. Inorganic arsenic levels in baby rice are of concern. Environ Pollut 2008; 152: 746–749.

    Article  CAS  PubMed  Google Scholar 

  48. Lai PY, Cottingham KL, Steinmaus C, Karagas MR, Miller MD . Arsenic and rice: translating research to address health care providers' needs. J Ped 2015; 167: 797–803.

    Article  Google Scholar 

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Acknowledgements

We thank the participants and staff members of the New Hampshire Birth Cohort Study and members of the Cottingham Laboratory for their assistance. Archana Ramanujan and David Fried conducted the medical record reviews for infant body weights. Patricia Fabian and three anonymous reviewers provided helpful comments on a draft manuscript. This publication was supported in part by grants P01 ES022832 and P20 ES018175 from the National Institute of Environmental Health Sciences (NIEHS) and RD83459901 and RD83544201 from the Environmental Protection Agency (EPA). Contents are solely the responsibility of the grantee and do not necessarily represent the official views of the US EPA. Further, the US EPA does not endorse the purchase of any commercial products or services mentioned in the publication.

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Correspondence to Kathryn L Cottingham.

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Carignan, C., Karagas, M., Punshon, T. et al. Contribution of breast milk and formula to arsenic exposure during the first year of life in a US prospective cohort. J Expo Sci Environ Epidemiol 26, 452–457 (2016). https://doi.org/10.1038/jes.2015.69

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