Current Diabetes Reports

, 19:147 | Cite as

Early-Life Arsenic Exposure, Nutritional Status, and Adult Diabetes Risk

  • Ana Navas-AcienEmail author
  • Miranda J. Spratlen
  • Ahlam Abuawad
  • Nancy J. LoIacono
  • Anne K. Bozack
  • Mary V. Gamble
Diabetes Epidemiology (E Selvin and K Foti, Section Editors)
Part of the following topical collections:
  1. Topical Collection on Diabetes Epidemiology


Purpose of Review

In utero influences, including nutrition and environmental chemicals, may induce long-term metabolic changes and increase diabetes risk in adulthood. This review evaluates the experimental and epidemiological evidence on the association of early-life arsenic exposure on diabetes and diabetes-related outcomes, as well as the influence of maternal nutritional status on arsenic-related metabolic effects.

Recent Findings

Five studies in rodents have evaluated the role of in utero arsenic exposure with diabetes in the offspring. In four of the studies, elevated post-natal fasting glucose was observed when comparing in utero arsenic exposure with no exposure. Rodent offspring exposed to arsenic in utero also showed elevated insulin resistance in the 4 studies evaluating it as well as microRNA changes related to glycemic control in 2 studies. Birth cohorts of arsenic-exposed pregnant mothers in New Hampshire, Mexico, and Taiwan have shown that increased prenatal arsenic exposure is related to altered cord blood gene expression, microRNA, and DNA methylation profiles in diabetes-related pathways. Thus far, no epidemiologic studies have evaluated early-life arsenic exposure with diabetes risk. Supplementation trials have shown B vitamins can reduce blood arsenic levels in highly exposed, undernourished populations. Animal evidence supports that adequate B vitamin status can rescue early-life arsenic-induced diabetes risk, although human data is lacking.


Experimental animal studies and human evidence on the association of in utero arsenic exposure with alterations in gene expression pathways related to diabetes in newborns, support the potential role of early-life arsenic exposure in diabetes development, possibly through increased insulin resistance. Given pervasive arsenic exposure and the challenges to eliminate arsenic from the environment, research is needed to evaluate prevention interventions, including the possibility of low-cost, low-risk nutritional interventions that can modify arsenic-related disease risk.


Arsenic Diabetes Early-life exposures Nutrition One-carbon metabolism 


Funding information

Ana Navas-Acien reports support from the National Institute of Environmental Health Sciences (P42ES010349, P30ES009089, R01ES028758, R01ES025216).

Miranda J. Spratlen reports support from the National Institutes of Health (F31ES027796).

Ahlam Abuawad reports support from the National Institute of General Medical Sciences (GM062454).

Nancy J. LoIacono reports support from the National Institutes of Health (P42ES010349, P30ES009089, R01ES028758).

Anne K. Bozack reports support from the National Institutes of Health (T32ES007322, F31ES029019).

Mary V. Gamble reports support from the National Institutes of Health (P42ES010349).

Compliance with Ethical Standards

Conflict of Interest

Ana Navas-Acien, Miranda J. Spratlen, Ahlam Abuawad, Nancy J. LoIacono, Anne K. Bozack, and Mary V. Gamble declare that they have no conflict of interest.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.


Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. 1.
    Gillman MW, Barker D, Bier D, et al. Meeting report on the 3rd International Congress on Developmental Origins of Health and Disease (DOHaD). Pediatr Res. 2007;61:625–9.PubMedCrossRefPubMedCentralGoogle Scholar
  2. 2.
    Aerts L, Van Assche FA. Animal evidence for the transgenerational development of diabetes mellitus. Int J Biochem Cell Biol. 2006;38:894–903.PubMedCrossRefPubMedCentralGoogle Scholar
  3. 3.
    Yajnik CS. Transmission of obesity-adiposity and related disorders from the mother to the baby. Ann Nutr Metab. 2014;64(Suppl 1):8–17.PubMedCrossRefPubMedCentralGoogle Scholar
  4. 4.
    Council USNR. Critical aspects of the EPA’s IRIS assessment of inorganic arsenic: Interim Report. In: Medicine TNAoSE, ed.: The National Acadamies Press; 2013.Google Scholar
  5. 5.
    Chen Y, Graziano JH, Parvez F, et al. Arsenic exposure from drinking water and mortality from cardiovascular disease in Bangladesh: prospective cohort study. BMJ. 2011;342:d2431.PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Jiang JY, Liu ML, Parvez F, et al. Association between arsenic exposure from drinking water and longitudinal change in blood pressure among HEALS cohort participants. Environ Health Perspect. 2015;123:806–12.PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    Karagas MR, Gossai A, Pierce B, Ahsan H. Drinking water arsenic contamination, skin lesions, and malignancies: a systematic review of the global evidence. Curr Environ Health Rep. 2015;2:52–68.PubMedPubMedCentralCrossRefGoogle Scholar
  8. 8.
    Kibriya MG, Jasmine F, Parvez F, et al. Association between genome-wide copy number variation and arsenic-induced skin lesions: a prospective study. Environ Health. 2017;16:75.PubMedPubMedCentralCrossRefGoogle Scholar
  9. 9.
    Spratlen MJ, Grau-Perez M, Umans JG, et al. Arsenic, one carbon metabolism and diabetes-related outcomes in the strong heart family study. Environ Int. 2018;121:728–40.PubMedCrossRefPubMedCentralGoogle Scholar
  10. 10.
    • Grau-Perez M, Kuo CC, Gribble MO, et al. Association of low-moderate arsenic exposure and arsenic metabolism with incident diabetes and insulin resistance in the Strong Heart Family Study. Environ Health Perspect. 2017;125:127004 This epidemiologic study in children and adolescents in the USA found a possible interaction between folate and vitamin B12 and arsenic metabolism biomarkers on diabetes risk.PubMedPubMedCentralCrossRefGoogle Scholar
  11. 11.
    Wasserman GA, Liu X, Loiacono NJ, et al. A cross-sectional study of well water arsenic and child IQ in Maine schoolchildren. Environ Health. 2014;13:23.PubMedPubMedCentralCrossRefGoogle Scholar
  12. 12.
    Martin EM, Styblo M, Fry RC. Genetic and epigenetic mechanisms underlying arsenic-associated diabetes mellitus: a perspective of the current evidence. Epigenomics. 2017;9:701–10.PubMedPubMedCentralCrossRefGoogle Scholar
  13. 13.
    Andrew AS, Jewell DA, Mason RA, Whitfield ML, Moore JH, Karagas MR. Drinking-water arsenic exposure modulates gene expression in human lymphocytes from a U.S. population. EnvironHealth Perspect. 2008;116:524–31.PubMedPubMedCentralCrossRefGoogle Scholar
  14. 14.
    Rojas D, Rager JE, Smeester L, et al. Prenatal arsenic exposure and the epigenome: identifying sites of 5-methylcytosine alterations that predict functional changes in gene expression in newborn cord blood and subsequent birth outcomes. Toxicol Sci. 2015;143:97–106.PubMedCrossRefPubMedCentralGoogle Scholar
  15. 15.
    Rager JE, Bailey KA, Smeester L, et al. Prenatal arsenic exposure and the epigenome: altered microRNAs associated with innate and adaptive immune signaling in newborn cord blood. Environ Mol Mutagen. 2014;55:196–208.PubMedCrossRefPubMedCentralGoogle Scholar
  16. 16.
    Kaushal A, Zhang H, Karmaus WJJ, et al. Genome-wide DNA methylation at birth in relation to in utero arsenic exposure and the associated health in later life. Environ Health. 2017;16:50.PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Davila-Esqueda ME, Morales JM, Jimenez-Capdeville ME, et al. Low-level subchronic arsenic exposure from prenatal developmental stages to adult life results in an impaired glucose homeostasis. Experimental and clinical endocrinology & diabetes. official journal, German Society of Endocrinology [and] German Diabetes Association. 2011;119:613–7.CrossRefGoogle Scholar
  18. 18.
    Ditzel EJ, Nguyen T, Parker P, Camenisch TD. Effects of arsenite exposure during fetal development on energy metabolism and susceptibility to diet-induced fatty liver disease in male mice. Environ Health Perspect. 2016;124:201–9.PubMedCrossRefPubMedCentralGoogle Scholar
  19. 19.
    Bonaventura MM, Bourguignon NS, Bizzozzero M, et al. Arsenite in drinking water produces glucose intolerance in pregnant rats and their female offspring. Food Chem Toxicol. 2017;100:207–16.PubMedCrossRefPubMedCentralGoogle Scholar
  20. 20.
    Huang MC, Douillet C, Dover EN, Styblo M. Prenatal arsenic exposure and dietary folate and methylcobalamin supplementation alter the metabolic phenotype of C57BL/6J mice in a sex-specific manner. Arch Toxicol. 2018;92:1925–37.PubMedPubMedCentralCrossRefGoogle Scholar
  21. 21.
    Sanchez-Soria P, Broka D, Quach S, Hardwick RN, Cherrington NJ, Camenisch TD. Fetal exposure to arsenic results in hyperglycemia, hypercholesterolemia, and nonalcoholic fatty liver disease in adult mice. J Toxicol Health. 2014;1.CrossRefGoogle Scholar
  22. 22.
    Yajnik CS. Obesity epidemic in India: intrauterine origins? Proc Nutr Soc. 2004;63:387–96.PubMedCrossRefPubMedCentralGoogle Scholar
  23. 23.
    Yajnik CS. Early life origins of insulin resistance and type 2 diabetes in India and other Asian countries. J Nutr. 2004;134:205–10.PubMedCrossRefPubMedCentralGoogle Scholar
  24. 24.
    Stewart CP, Christian P, Schulze KJ, et al. Low maternal vitamin B-12 status is associated with offspring insulin resistance regardless of antenatal micronutrient supplementation in rural Nepal. J Nutr. 2011;141:1912–7.PubMedCrossRefPubMedCentralGoogle Scholar
  25. 25.
    Rush EC, Katre P, Yajnik CS. Vitamin B12: one carbon metabolism, fetal growth and programming for chronic disease. Eur J Clin Nutr. 2014;68:2–7.PubMedCrossRefPubMedCentralGoogle Scholar
  26. 26.
    Bozack AK, Saxena R, Gamble MV. Nutritional influences on one-carbon metabolism: effects on arsenic methylation and toxicity. Annu Rev Nutr. 2018;38:401–29.PubMedPubMedCentralCrossRefGoogle Scholar
  27. 27.
    Gamble MV, Liu X, Ahsan H, et al. Folate and arsenic metabolism: a double-blind, placebo-controlled folic acid-supplementation trial in Bangladesh. Am J Clin Nutr. 2006;84:1093–101.PubMedPubMedCentralCrossRefGoogle Scholar
  28. 28.
    Gamble MV, Liu X, Slavkovich V, et al. Folic acid supplementation lowers blood arsenic. Am J ClinNutr. 2007;86:1202–9.Google Scholar
  29. 29.
    Bailey KA, Smith AH, Tokar EJ, et al. Mechanisms underlying latent disease risk associated with early-life arsenic exposure: current research trends and scientific gaps. Environ Health Perspect. 2016;124:170–5.PubMedCrossRefPubMedCentralGoogle Scholar
  30. 30.
    Fowler PA, Drake AJ, O’Shaughnessy PJ, et al. Comment on “effects of arsenite during fetal development on energy metabolism and susceptibility to diet-induced fatty liver diseases in male mice” and “mechanisms underlying latent disease risk associated with early-life arsenic exposure: current trends and scientific gaps”. Environ Health Perspect. 2016;124:A99.PubMedPubMedCentralCrossRefGoogle Scholar
  31. 31.
    Li Y, He Y, Qi L, et al. Exposure to the Chinese famine in early life and the risk of hyperglycemia and type 2 diabetes in adulthood. Diabetes. 2010;59:2400–6.PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Vaiserman AM. Early-life nutritional programming of type 2 diabetes: experimental and quasi-experimental evidence. Nutrients. 2017;9.PubMedCentralCrossRefGoogle Scholar
  33. 33.
    Reusens B, Theys N, Dumortier O, Goosse K, Remacle C. Maternal malnutrition programs the endocrine pancreas in progeny. Am J Clin Nutr. 2011;94:1824S–9S.PubMedCrossRefPubMedCentralGoogle Scholar
  34. 34.
    Martinez JA, Cordero P, Campion J, Milagro FI. Interplay of early-life nutritional programming on obesity, inflammation and epigenetic outcomes. Proc Nutr Soc. 2012;71:276–83.PubMedCrossRefPubMedCentralGoogle Scholar
  35. 35.
    Desai M, Jellyman JK, Ross MG. Epigenomics, gestational programming and risk of metabolic syndrome. Int J Obes. 2015;39:633–41.CrossRefGoogle Scholar
  36. 36.
    Young JL, Cai L, States JC. Impact of prenatal arsenic exposure on chronic adult diseases. Syst Biol Reprod Med. 2018:1–15.Google Scholar
  37. 37.
    Fry RC, Navasumrit P, Valiathan C, et al. Activation of inflammation/NF-kappaB signaling in infants born to arsenic-exposed mothers. PLoS Genet. 2007;3:e207.PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    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;272:384–90.PubMedPubMedCentralCrossRefGoogle Scholar
  39. 39.
    States JC, Singh AV, Knudsen TB, et al. Prenatal arsenic exposure alters gene expression in the adult liver to a proinflammatory state contributing to accelerated atherosclerosis. PLoS One. 2012;7:e38713.PubMedPubMedCentralCrossRefGoogle Scholar
  40. 40.
    Ren X, Gaile DP, Gong Z, et al. Arsenic responsive microRNAs in vivo and their potential involvement in arsenic-induced oxidative stress. Toxicol Appl Pharmacol. 2015;283:198–209.PubMedPubMedCentralCrossRefGoogle Scholar
  41. 41.
    Tsang V, Fry RC, Niculescu MD, et al. The epigenetic effects of a high prenatal folate intake in male mouse fetuses exposed in utero to arsenic. Toxicol Appl Pharmacol. 2012;264:439–50.PubMedPubMedCentralCrossRefGoogle Scholar
  42. 42.
    Rahman M, Sohel N, Yunus M, et al. Increased childhood mortality and arsenic in drinking water in Matlab. Bangladesh: a population-based cohort study. PLoS One. 2013;8:e55014.PubMedPubMedCentralCrossRefGoogle Scholar
  43. 43.
    Hawkesworth S, Wagatsuma Y, Kippler M, et al. Early exposure to toxic metals has a limited effect on blood pressure or kidney function in later childhood, rural Bangladesh. Int J Epidemiol. 2013;42:176–85.PubMedCrossRefPubMedCentralGoogle Scholar
  44. 44.
    Yorifuji T, Tsuda T, Grandjean P. Unusual cancer excess after neonatal arsenic exposure from contaminated milk powder. J Natl Cancer Inst. 2010;102:360–1.PubMedPubMedCentralCrossRefGoogle Scholar
  45. 45.
    Yorifuji T, Tsuda T, Doi H, Grandjean P. Cancer excess after arsenic exposure from contaminated milk powder. Environ Health Prev Med. 2011;16:164–70.PubMedCrossRefPubMedCentralGoogle Scholar
  46. 46.
    Kuo CC, Su PH, Sun CW, Liu HJ, Chang CL, Wang SL. Early-life arsenic exposure promotes atherogenic lipid metabolism in adolescence: a 15-year birth cohort follow-up study in Central Taiwan. Environ Int. 2018;118:97–105.PubMedCrossRefPubMedCentralGoogle Scholar
  47. 47.
    Grau-Perez M, Kuo CC, Spratlen M, et al. The association of arsenic exposure and metabolism with type 1 and type 2 diabetes in youth: the SEARCH case-control study. Diabetes Care. 2017;40:46–53.PubMedCrossRefPubMedCentralGoogle Scholar
  48. 48.
    Hall MN, Gamble MV. Nutritional manipulation of one-carbon metabolism: effects on arsenic methylation and toxicity. J Toxicol. 2012;2012:595307.PubMedPubMedCentralCrossRefGoogle Scholar
  49. 49.
    Ducker GS, Rabinowitz JD. One-carbon metabolism in health and disease. Cell Metab. 2017;25:27–42.PubMedCrossRefPubMedCentralGoogle Scholar
  50. 50.
    Finer S, Saravanan P, Hitman G, Yajnik C. The role of the one-carbon cycle in the developmental origins of type 2 diabetes and obesity. Diabet Med. 2014;31:263–72.PubMedCrossRefPubMedCentralGoogle Scholar
  51. 51.
    Lopez-Carrillo L, Gamboa-Loira B, Becerra W, et al. Dietary micronutrient intake and its relationship with arsenic metabolism in Mexican women. Environ Res. 2016;151:445–50.PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    Gruber JF, Karagas MR, Gilbert-Diamond D, et al. Associations between toenail arsenic concentration and dietary factors in a New Hampshire population. Nutr J. 2012;11:45.PubMedPubMedCentralCrossRefGoogle Scholar
  53. 53.
    • Spratlen MJ, Gamble MV, Grau-Perez M, et al. Arsenic metabolism and one-carbon metabolism at low-moderate arsenic exposure: evidence from the Strong Heart Study. Food Chem Toxicol. 2017;105:387–97 This epidemiologic study in a population exposed to low moderate arsenic levels support that one-carbon metabolism nutrients are related to arsenic metabolism, consistent with clinical trials of folate and B vitamin supplementation conducted in Bangladesh.PubMedPubMedCentralCrossRefGoogle Scholar
  54. 54.
    Kurzius-Spencer M, da Silva V, Thomson CA, et al. Nutrients in one-carbon metabolism and urinary arsenic methylation in the National Health and Nutrition Examination Survey (NHANES) 2003–2004. Sci Total Environ. 2017;607–608:381–90.PubMedCrossRefPubMedCentralGoogle Scholar
  55. 55.
    Heck JE, Gamble MV, Chen Y, et al. Consumption of folate-related nutrients and metabolism of arsenic in Bangladesh. Am J Clin Nutr. 2007;85:1367–74.PubMedCrossRefPubMedCentralGoogle Scholar
  56. 56.
    Aposhian HV, Aposhian MM. Arsenic toxicology: five questions. Chem Res Toxicol. 2006;19:1–15.PubMedCrossRefPubMedCentralGoogle Scholar
  57. 57.
    Niedzwiecki MM, Hall MN, Liu X, et al. Interaction of plasma glutathione redox and folate deficiency on arsenic methylation capacity in Bangladeshi adults. Free Radic Biol Med. 2014;73:67–74.PubMedCrossRefPubMedCentralGoogle Scholar
  58. 58.
    Vahter ME. Interactions between arsenic-induced toxicity and nutrition in early life. J Nutr. 2007;137:2798–804.PubMedCrossRefPubMedCentralGoogle Scholar
  59. 59.
    •• Huang MC, Douillet C, Dover EN, et al. Metabolic phenotype of wild-type and As3mt-knockout C57BL/6J mice exposed to inorganic arsenic: the role of dietary fat and Folate intake. Environ Health Perspect. 2018;126:127003 This experimental study in mice showed that joint exposure to arsenite and folate could rescue the metabolic effects induced by arsenite in male mice but not in female.PubMedPubMedCentralCrossRefGoogle Scholar
  60. 60.
    Fretts AM, Howard BV, McKnight B, et al. Associations of processed meat and unprocessed red meat intake with incident diabetes: the Strong Heart Family Study. Am J Clin Nutr. 2012;95:752–8.PubMedPubMedCentralCrossRefGoogle Scholar
  61. 61.
    Eilat-Adar S, Mete M, Fretts A, et al. Dietary patterns and their association with cardiovascular risk factors in a population undergoing lifestyle changes: the Strong Heart Study. Nutr Metab Cardiovasc Dis. 2013;23:528–35.PubMedCrossRefPubMedCentralGoogle Scholar
  62. 62.
    Navas-Acien A, Umans JG, Howard BV, et al. Urine arsenic concentrations and species excretion patterns in American Indian communities over a 10-year period: the Strong Heart Study. Environ Health Perspect. 2009;117:1428–33.PubMedPubMedCentralCrossRefGoogle Scholar
  63. 63.
    Vahter M. Mechanisms of arsenic biotransformation. Toxicology. 2002;181–182:211–7.PubMedCrossRefPubMedCentralGoogle Scholar
  64. 64.
    Challenger F. Biological Methylation. Chemical Reviews. 1945;36:315–61.CrossRefGoogle Scholar
  65. 65.
    Cullen WR, Reimer KJ. Arsenic speciation in the environment. Chem Rev. 1989;89:713–64.CrossRefGoogle Scholar
  66. 66.
    Naranmandura H, Suzuki N, Suzuki KT. Trivalent arsenicals are bound to proteins during reductive methylation. Chem Res Toxicol. 2006;19:1010–8.PubMedCrossRefPubMedCentralGoogle Scholar
  67. 67.
    Vahter M. Genetic polymorphism in the biotransformation of inorganic arsenic and its role in toxicity. Toxicol Lett. 2000;112–113:209–17.PubMedCrossRefPubMedCentralGoogle Scholar
  68. 68.
    Hernandez A, Marcos R. Genetic variations associated with interindividual sensitivity in the response to arsenic exposure. Pharmacogenomics. 2008;9:1113–32.PubMedCrossRefPubMedCentralGoogle Scholar
  69. 69.
    Loffredo CA, Aposhian HV, Cebrian ME, Yamauchi H, Silbergeld EK. Variability in human metabolism of arsenic. Environ Res. 2003;92:85–91.PubMedCrossRefPubMedCentralGoogle Scholar
  70. 70.
    Tellez-Plaza M, Gribble MO, Voruganti VS, et al. Heritability and preliminary genome-wide linkage analysis of arsenic metabolites in urine. Environ Health Perspect. 2013;121:345–51.PubMedPubMedCentralCrossRefGoogle Scholar
  71. 71.
    Melak D, Ferreccio C, Kalman D, et al. Arsenic methylation and lung and bladder cancer in a case-control study in northern Chile. Toxicol Appl Pharmacol. 2014;274:225–31.PubMedCrossRefPubMedCentralGoogle Scholar
  72. 72.
    Chen Y, Wu F, Liu M, et al. A prospective study of arsenic exposure, arsenic methylation capacity, and risk of cardiovascular disease in Bangladesh. Environ Health Perspect. 2013;121:832–8.PubMedPubMedCentralCrossRefGoogle Scholar
  73. 73.
    Chen YC, Guo YL, Su HJ, et al. Arsenic methylation and skin cancer risk in southwestern Taiwan. J Occup Environ Med. 2003;45:241–8.PubMedCrossRefPubMedCentralGoogle Scholar
  74. 74.
    Chen YC, Su HJ, Guo YL, Houseman EA, Christiani DC. Interaction between environmental tobacco smoke and arsenic methylation ability on the risk of bladder cancer. Cancer Causes Control. 2005;16:75–81.PubMedCrossRefPubMedCentralGoogle Scholar
  75. 75.
    Chen YC, Su HJ, Guo YL, et al. Arsenic methylation and bladder cancer risk in Taiwan. Cancer Causes Control. 2003;14:303–10.PubMedCrossRefPubMedCentralGoogle Scholar
  76. 76.
    Hsueh YM, Chiou HY, Huang YL, et al. Serum beta-carotene level, arsenic methylation capability, and incidence of skin cancer. Cancer Epidemiol Biomark Prev. 1997;6:589–96.Google Scholar
  77. 77.
    Wu MM, Chiou HY, Hsueh YM, et al. Effect of plasma homocysteine level and urinary monomethylarsonic acid on the risk of arsenic-associated carotid atherosclerosis. Toxicol Appl Pharmacol. 2006;216:168–75.PubMedCrossRefPubMedCentralGoogle Scholar
  78. 78.
    Chen Y, Wu F, Graziano JH, et al. Arsenic exposure from drinking water, arsenic methylation capacity, and carotid intima-media thickness in Bangladesh. Am J Epidemiol. 2013;178:372–81.PubMedPubMedCentralCrossRefGoogle Scholar
  79. 79.
    Kuo CC, Moon KA, Wang SL, Silbergeld EK, Navas-Acien A. The association of arsenic metabolism with cancer, cardiovascular disease and diabetes: a systematic review of the epidemiological evidence. Environ Health Perspect 2017;125:087001.PubMedPubMedCentralCrossRefGoogle Scholar
  80. 80.
    Kuo CC, Howard BV, Umans JG, et al. Arsenic exposure, arsenic metabolism, and incident diabetes in the Strong Heart Study. Diabetes Care. 2015;38:620–7.PubMedPubMedCentralGoogle Scholar
  81. 81.
    Nizam S, Kato M, Yatsuya H, et al. Differences in urinary arsenic metabolites between diabetic and non-diabetic subjects in Bangladesh. Int J Environ Res Public Health. 2013;10:1006–19.PubMedPubMedCentralCrossRefGoogle Scholar
  82. 82.
    Pang Y, Peng RD, Jones MR, et al. Metal mixtures in urban and rural populations in the US: The Multi-Ethnic Study of Atherosclerosis and the Strong Heart Study. Environ Res. 2016;147:356–64.PubMedPubMedCentralCrossRefGoogle Scholar
  83. 83.
    Spratlen MJ, Grau-Perez M, Umans JG, et al. Targeted metabolomics to understand the association between arsenic metabolism and diabetes-related outcomes: preliminary evidence from the Strong Heart Family Study. Environ Res. 2018;168:146–57.PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Ana Navas-Acien
    • 1
    Email author
  • Miranda J. Spratlen
    • 1
  • Ahlam Abuawad
    • 1
  • Nancy J. LoIacono
    • 1
  • Anne K. Bozack
    • 1
  • Mary V. Gamble
    • 1
  1. 1.Department of Environmental Health SciencesColumbia University Mailman School of Public HealthNew YorkUSA

Personalised recommendations