Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

At a glance: The ONWARDS insulin icodec trials

A round-up of the ONWARDS phase 3 clinical trials evaluating the novel weekly insulin icodec in people with diabetes.
ADVANCED SEARCH
Log in
Top
BMC Public Health
Published in: BMC Public Health 1/2017

Open Access 01-12-2017 | Research article

Maternal blood cadmium, lead and arsenic levels, nutrient combinations, and offspring birthweight

Authors: Yiwen Luo, Lauren E. McCullough, Jung-Ying Tzeng, Thomas Darrah, Avner Vengosh, Rachel L. Maguire, Arnab Maity, Carmen Samuel-Hodge, Susan K. Murphy, Michelle A. Mendez, Cathrine Hoyo

Published in: BMC Public Health | Issue 1/2017

Login to get access

Abstract

Background

Cadmium (Cd), lead (Pb) and arsenic (As) are common environmental contaminants that have been associated with lower birthweight. Although some essential metals may mitigate exposure, data are inconsistent. This study sought to evaluate the relationship between toxic metals, nutrient combinations and birthweight among 275 mother-child pairs.

Methods

Non-essential metals, Cd, Pb, As, and essential metals, iron (Fe), zinc (Zn), selenium (Se), copper (Cu), calcium (Ca), magnesium (Mg), and manganese (Mn) were measured in maternal whole blood obtained during the first trimester using inductively coupled plasma mass spectrometry. Folate concentrations were measured by microbial assay. Birthweight was obtained from medical records. We used quantile regression to evaluate the association between toxic metals and nutrients due to their underlying wedge-shaped relationship. Ordinary linear regression was used to evaluate associations between birth weight and toxic metals.

Results

After multivariate adjustment, the negative association between Pb or Cd and a combination of Fe, Se, Ca and folate was robust, persistent and dose-dependent (p < 0.05). However, a combination of Zn, Cu, Mn and Mg was positively associated with Pb and Cd levels. While prenatal blood Cd and Pb were also associated with lower birthweight. Fe, Se, Ca and folate did not modify these associations.

Conclusion

Small sample size and cross-sectional design notwithstanding, the robust and persistent negative associations between some, but not all, nutrient combinations with these ubiquitous environmental contaminants suggest that only some recommended nutrient combinations may mitigate toxic metal exposure in chronically exposed populations. Larger longitudinal studies are required to confirm these findings.
Appendix
Available only for authorised users
Literature
1.
2.
Satarug S, Moore MR. Adverse health effects of chronic exposure to low-level cadmium in foodstuffs and cigarette smoke. Environ Health Perspect. 2004;112:1099–103.PubMedPubMedCentralCrossRef
3.
Satarug S, Moore MR. Emerging roles of cadmium and heme oxygenase in type-2 diabetes and cancer susceptibility. Tohoku J Exp Med. 2012;228:267–88.PubMedCrossRef
4.
Agarwal S, Zaman T, Tuzcu EM, Kapadia SR. Heavy metals and cardiovascular disease: results from the National Health and nutrition examination survey (NHANES) 1999–2006. Angiology. 2011;62:422–9.PubMedCrossRef
5.
Tellez-Plaza M, Guallar E, Howard BV, Navas-Acien A. Cadmium and cardiovascular risk. Epidemiology. 2013;24:784–5.PubMedCrossRef
6.
Chen L, Lei L, Jin T, Nordberg M, Nordberg GF. Plasma metallothionein antibody, urinary cadmium, and renal dysfunction in a Chinese type 2 diabetic population. Diabetes Care. 2006;29:2682–7.PubMedCrossRef
7.
Huang M, Choi SJ, Kim DW, et al. Evaluation of factors associated with cadmium exposure and kidney function in the general population. Environ Toxicol. 2013;28:563–70.PubMedCrossRef
8.
Liang Y, Lei L, Nilsson J, et al. Renal function after reduction in cadmium exposure: an 8-year follow-up of residents in cadmium-polluted areas. Environ Health Perspect. 2012;120:223–8.PubMedCrossRef
9.
10.
Christensen BC, Marsit CJ, Houseman EA, et al. Differentiation of lung adenocarcinoma, pleural mesothelioma, and nonmalignant pulmonary tissues using DNA methylation profiles. Cancer Res. 2009;69:6315–21.PubMedPubMedCentralCrossRef
11.
Gallagher CM, Chen JJ, Kovach JS. Environmental cadmium and breast cancer risk. Aging (Albany NY). 2010;2:804–14.CrossRef
12.
Benbrahim-Tallaa L, Tokar EJ, Diwan BA, Dill AL, Coppin JF, Waalkes MP. Cadmium malignantly transforms normal human breast epithelial cells into a basal-like phenotype. Environ Health Perspect. 2009;117:1847–52.PubMedPubMedCentralCrossRef
13.
Tokar EJ, Benbrahim-Tallaa L, Waalkes MP. Metal ions in human cancer development. Met Ions Life Sci. 2011;8:375–401.PubMed
14.
Ferraro PM, Sturniolo A, Naticchia A, D'Alonzo S, Gambaro G. Temporal trend of cadmium exposure in the United States population suggests gender specificities. Intern Med J. 2012;42:691–7.PubMedCrossRef
15.
Scinicariello F, Abadin HG, Murray HE. Association of low-level blood lead and blood pressure in NHANES 1999–2006. Environ Res. 2011;111:1249–57.PubMedCrossRef
16.
Nishijo M, Nakagawa H, Honda R, et al. Effects of maternal exposure to cadmium on pregnancy outcome and breast milk. Occup Environ Med. 2002;59:394–6. discussion 7PubMedPubMedCentralCrossRef
17.
Nishijo M, Tawara K, Honda R, Nakagawa H, Tanebe K, Saito S. Relationship between newborn size and mother's blood cadmium levels, Toyama, Japan. Arch Environ Health. 2004;59:22–5.PubMedCrossRef
18.
Salpietro CD, Gangemi S, Minciullo PL, et al. Cadmium concentration in maternal and cord blood and infant birth weight: a study on healthy non-smoking women. J Perinat Med. 2002;30:395–9.PubMedCrossRef
19.
Ronco AM, Arguello G, Munoz L, Gras N, Llanos M. Metals content in placentas from moderate cigarette consumers: correlation with newborn birth weight. Biometals. 2005;18:233–41.PubMedCrossRef
20.
Fei DL, Koestler DC, Li Z, et al. Association between in Utero arsenic exposure, placental gene expression, and infant birth weight: a US birth cohort study. Environmental health: a global access science source. 2013;12:58.CrossRef
21.
Rodosthenous RS, Burris HH, Svensson K, et al. Prenatal lead exposure and fetal growth: smaller infants have heightened susceptibility. Environ Int. 2017;99:228–33.PubMedCrossRef
22.
Jedrychowski W, Perera F, Jankowski J, et al. Gender specific differences in neurodevelopmental effects of prenatal exposure to very low-lead levels: the prospective cohort study in three-year olds. Early Hum Dev. 2009;85:503–10.PubMedPubMedCentralCrossRef
23.
Kaji M, Nishi Y. Lead and growth. Clinical pediatric endocrinology : case reports and clinical investigations: official journal of the Japanese Society for Pediatric Endocrinology. 2006;15:123–8.
24.
Al-Saleh I, Shinwari N, Mashhour A, Rabah A. Birth outcome measures and maternal exposure to heavy metals (lead, cadmium and mercury) in Saudi Arabian population. Int J Hyg Environ Health. 2014;217:205–18.PubMedCrossRef
25.
Gundacker C, Frohlich S, Graf-Rohrmeister K, et al. Perinatal lead and mercury exposure in Austria. Sci Total Environ. 2010;408:5744–9.PubMedCrossRef
26.
Jones L, Parker JD, Mendola P. Blood lead and mercury levels in pregnant women in the United States, 2003–2008. NCHS data brief. 2010;52:1–8.
27.
Koppen G, Den Hond E, Nelen V, et al. Organochlorine and heavy metals in newborns: results from the Flemish environment and health survey (FLEHS 2002–2006). Environ Int. 2009;35:1015–22.PubMedCrossRef
28.
Piasek M, Blanusa M, Kostial K, Laskey JW. Placental cadmium and progesterone concentrations in cigarette smokers. Reproductive toxicology (Elmsford, NY). 2001;15:673–81.CrossRef
29.
Shirai S, Suzuki Y, Yoshinaga J, Mizumoto Y. Maternal exposure to low-level heavy metals during pregnancy and birth size. J Environ Sci Health A Tox Hazard Subst Environ Eng. 2010;45:1468–74.PubMedCrossRef
30.
Faulk C, Barks A, Sanchez BN, et al. Perinatal lead (Pb) exposure results in sex-specific effects on food intake, fat, weight, and insulin response across the Murine life-course. PLoS One. 2014;9:e104273.PubMedPubMedCentralCrossRef
31.
Ogden CL, Carroll MD, Flegal KM. High body mass index for age among US children and adolescents, 2003–2006. JAMA. 2008;299:2401–5.PubMedCrossRef
32.
Ong KK. Catch-up growth in small for gestational age babies: good or bad? Curr Opin Endocrinol Diabetes Obes. 2007;14:30–4.PubMedCrossRef
33.
Ong KK, Ahmed ML, Emmett PM, Preece MA, Dunger DB. Association between postnatal catch-up growth and obesity in childhood: prospective cohort study. BMJ. 2000;320:967–71.PubMedPubMedCentralCrossRef
34.
Hu H, Kotha S, Brennan T. The role of nutrition in mitigating environmental insults: policy and ethical issues. Environ Health Perspect. 1995;103(Suppl 6):185–90.PubMedPubMedCentralCrossRef
35.
Gallagher CM, Chen JJ, Kovach JS. The relationship between body iron stores and blood and urine cadmium concentrations in US never-smoking, non-pregnant women aged 20–49 years. Environ Res. 2011;111:702–7.PubMedCrossRef
36.
Wildman RE, Mao S. Tissue-specific alterations in lipoprotein lipase activity in copper-deficient rats. Biol Trace Elem Res. 2001;80:221–9.PubMedCrossRef
37.
Bourque SL, Komolova M, Nakatsu K, Adams MA. Long-term circulatory consequences of perinatal iron deficiency in male Wistar rats. Hypertension. 2008;51:154–9.PubMedCrossRef
38.
Komolova M, Bourque SL, Nakatsu K, Adams MA. Sedentariness and increased visceral adiposity in adult perinatally iron-deficient rats. International journal of obesity (2005). 2008;32:1441–4.CrossRef
39.
Menzie CM, Yanoff LB, Denkinger BI, et al. Obesity-related hypoferremia is not explained by differences in reported intake of heme and nonheme iron or intake of dietary factors that can affect iron absorption. J Am Diet Assoc. 2008;108:145–8.PubMedPubMedCentralCrossRef
40.
Yanoff LB, Menzie CM, Denkinger B, et al. Inflammation and iron deficiency in the hypoferremia of obesity. International journal of obesity (2005). 2007;31:1412–9.CrossRef
41.
Ganeshan M, Sainath PB, Padmavathi IJ, et al. Maternal manganese restriction increases susceptibility to high-fat diet-induced dyslipidemia and altered adipose function in WNIN male rat offspring. Exp Diabetes Res. 2011;2011:486316.PubMedPubMedCentralCrossRef
42.
Guerrero-Romero F, Bermudez-Pena C, Rodriguez-Moran M. Severe hypomagnesemia and low-grade inflammation in metabolic syndrome. Magnes Res. 2011;24:45–53.PubMed
43.
Guerrero-Romero F, Rodriguez-Moran M. Low serum magnesium levels and metabolic syndrome. Acta Diabetol. 2002;39:209–13.PubMedCrossRef
44.
Guerrero-Romero F, Rodriguez-Moran M. Hypomagnesemia, oxidative stress, inflammation, and metabolic syndrome. Diabetes Metab Res Rev. 2006;22:471–6.PubMedCrossRef
45.
Jain CK, Gupta H, Chakrapani GJ. Enrichment and fractionation of heavy metals in bed sediments of river Narmada, India. Environ Monit Assess. 2008;141:35–47.PubMedCrossRef
46.
Jain CK, Rao VV, Prakash BA, Kumar KM, Yoshida M. Metal fractionation study on bed sediments of Hussainsagar Lake, Hyderabad, India. Environ Monit Assess. 2010;166:57–67.PubMedCrossRef
47.
Cheng HL, Griffin HJ, Bryant CE, Rooney KB, Steinbeck KS, O'Connor HT. Impact of diet and weight loss on iron and zinc status in overweight and obese young women. Asia Pac J Clin Nutr. 2013;22:574–82.PubMed
48.
Mistry HD, Kurlak LO, Young SD, et al. Maternal selenium, copper and zinc concentrations in pregnancy associated with small-for-gestational-age infants. Matern Child Nutr. 2014;10:327–34.PubMedCrossRef
49.
Rossman TG, Klein CB. Genetic and epigenetic effects of environmental arsenicals. Metallomics. 2011;3:1135–41.PubMedCrossRef
50.
Hall MN, Liu X, Slavkovich V, et al. Folate, Cobalamin, Cysteine, Homocysteine, and arsenic metabolism among children in Bangladesh. Environ Health Perspect. 2009;117:825–31.PubMedPubMedCentralCrossRef
51.
Gamble MV, Liu X, Slavkovich V, et al. Folic acid supplementation lowers blood arsenic. Am J Clin Nutr. 2007;86:1202–9.PubMedPubMedCentral
52.
Heindel JJ, Vandenberg LN. Developmental origins of health and disease: a paradigm for understanding disease cause and prevention. Curr Opin Pediatr. 2015;27:248–53.PubMedPubMedCentralCrossRef
53.
Liu Y, Murphy SK, Murtha AP, et al. Depression in pregnancy, infant birth weight and DNA methylation of imprint regulatory elements. Epigenetics. 2012;7:735–46.PubMedPubMedCentralCrossRef
54.
Horne DW, Patterson D. Lactobacillus casei microbiological assay of folic acid derivatives in 96-well microtiter plates. Clin Chem. 1988;34:2357–9.PubMed
55.
Darrah TH, Prutsman-Pfeiffer JJ, Poreda RJ, Ellen Campbell M, Hauschka PV, Hannigan RE. Incorporation of excess gadolinium into human bone from medical contrast agents. Metallomics. 2009;1:479–88.PubMedCrossRef
56.
57.
McLaughlin MP, Darrah TH, Holland PL. Palladium (II) and platinum (II) bind strongly to an engineered blue copper protein. Inorg Chem. 2011;50:11294–6.PubMedPubMedCentralCrossRef
58.
Sprauten M, Darrah TH, Peterson DR, et al. Impact of long-term serum platinum concentrations on neuro- and ototoxicity in Cisplatin-treated survivors of testicular cancer. J Clin Oncol. 2012;30:300–7.PubMedCrossRef
59.
Koenker R, Bassett G. Regression quantiles. Econometrica: journal of the Econometric Society. 1978;46:33–50.CrossRef
60.
Faulk C, Barks A, Liu K, Goodrich JM, Dolinoy DC. Early-life lead exposure results in dose- and sex-specific effects on weight and epigenetic gene regulation in weanling mice. Epigenomics. 2013;5:487–500.PubMedCrossRef
61.
Govarts E, Remy S, Bruckers L, et al. Combined effects of prenatal exposures to environmental chemicals on birth weight. Int J Environ Res Public Health. 2016;13
62.
Djukic-Cosic D, Ninkovic M, Malicevic Z, Plamenac-Bulat Z, Matovic V. Effect of supplemental magnesium on the kidney levels of cadmium, zinc, and copper of mice exposed to toxic levels of cadmium. Biol Trace Elem Res. 2006;114:281–91.PubMedCrossRef
63.
Arbuckle TE, Liang CL, Morisset AS, et al. Maternal and fetal exposure to cadmium, lead, manganese and mercury: the MIREC study. Chemosphere. 2016;163:270–82.PubMedCrossRef
64.
McKay JA, Mathers JC. Diet induced epigenetic changes and their implications for health. Acta Physiol. 2011;202:103–18.CrossRef
65.
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.PubMedPubMedCentralCrossRef
66.
67.
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.PubMedPubMedCentralCrossRef
68.
Deb D, Biswas A, Ghose A, Das A, Majumdar KK, Guha Mazumder DN. Nutritional deficiency and arsenical manifestations: a perspective study in an arsenic-endemic region of West Bengal, India. Public Health Nutr. 2013;16:1644–55.PubMedCrossRef
69.
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.PubMed
70.
Vahter M, Marafante E. Effects of low dietary intake of methionine, choline or proteins on the biotransformation of arsenite in the rabbit. Toxicol Lett. 1987;37:41–6.PubMedCrossRef
71.
Suarez-Ortegon MF, Mosquera M, Caicedo DM, De Plata CA, Mendez F. Nutrients intake as determinants of blood lead and cadmium levels in Colombian pregnant women. Am J Hum Biol. 2013;25:344–50.PubMedCrossRef
72.
73.
Whincup PH, Kaye SJ, Owen CG, et al. Birth weight and risk of type 2 diabetes: a systematic review. JAMA. 2008;300:2886–97.PubMedCrossRef
74.
Ezzahir N, Alberti C, Deghmoun S, et al. Time course of catch-up in adiposity influences adult anthropometry in individuals who were born small for gestational age. Pediatr Res. 2005;58:243–7.PubMedCrossRef
75.
Meas T, Deghmoun S, Armoogum P, Alberti C, Levy-Marchal C. Consequences of being born small for gestational age on body composition: an 8-year follow-up study. J Clin Endocrinol Metab. 2008;93:3804–9.PubMedPubMedCentralCrossRef
76.
Howe LD, Tilling K, Benfield L, et al. Changes in ponderal index and body mass index across childhood and their associations with fat mass and cardiovascular risk factors at age 15. PLoS One. 2010;5:e15186.PubMedPubMedCentralCrossRef
77.
Anderson EL, Howe LD, Fraser A, et al. Weight trajectories through infancy and childhood and risk of non-alcoholic fatty liver disease in adolescence: the ALSPAC study. J Hepatol. 2014;61:626–32.PubMedPubMedCentralCrossRef
78.
de Kroon ML, Renders CM, van Wouwe JP, van Buuren S, Hirasing RA. The Terneuzen birth cohort: BMI change between 2 and 6 years is most predictive of adult cardiometabolic risk. PLoS One. 2010;5:e13966.PubMedPubMedCentralCrossRef
79.
Gallagher CM, Meliker JR. Blood and urine cadmium, blood pressure, and hypertension: a systematic review and meta-analysis. Environ Health Perspect. 2010;118:1676–84.PubMedPubMedCentralCrossRef
80.
Wallia A, Allen NB, Badon S, El Muayed M. Association between urinary cadmium levels and prediabetes in the NHANES 2005–2010 population. Int J Hyg Environ Health. 2014;217:854–60.PubMedPubMedCentralCrossRef
81.
Tellez-Plaza M, Jones MR, Dominguez-Lucas A, Guallar E, Navas-Acien A. Cadmium exposure and clinical cardiovascular disease: a systematic review. Current atherosclerosis reports. 2013;15:356.PubMedCrossRef
82.
Karim MR, Rahman M, Islam K, et al. Increases in oxidized low-density lipoprotein and other inflammatory and adhesion molecules with a concomitant decrease in high-density lipoprotein in the individuals exposed to arsenic in Bangladesh. Toxicological sciences: an official journal of the Society of Toxicology. 2013;135:17–25.CrossRef
83.
Mendez MA, González-Horta C, Sánchez-Ramírez B, Ballinas-Casarrubias L, Hernández Cerón R, Viniegra Morales D, Baeza Terrazas FA, Ishida MC, Gutiérrez-Torres DS, Saunders RJ, Drobná Z, Fry RC, Buse JB, Loomis D, García-Vargas GG, Del Razo LM, Stýblo M. Chronic exposure to arsenic and markers of cardiometabolic risk: a cross-sectional study in Chihuahua, Mexico. Environ Health Perspect 2016.
84.
Kuo CC, Moon K, Thayer KA, Navas-Acien A. Environmental chemicals and type 2 diabetes: an updated systematic review of the epidemiologic evidence. Current diabetes reports. 2013;13:831–49.PubMedPubMedCentralCrossRef
85.
Schober SE, Mirel LB, Graubard BI, Brody DJ, Flegal KM. Blood lead levels and death from all causes, cardiovascular disease, and cancer: results from the NHANES III mortality study. Environ Health Perspect. 2006;114:1538–41.PubMedPubMedCentral
86.
Daniels SR, Greer FR. Lipid screening and cardiovascular health in childhood. Pediatrics. 2008;122:198–208.PubMedCrossRef
87.
Chinapaw MJ, Altenburg TM, van Eijsden M, Gemke RJ, Vrijkotte TG. Screen time and cardiometabolic function in Dutch 5–6 year olds: cross-sectional analysis of the ABCD-study. BMC Public Health. 2014;14:933.PubMedPubMedCentralCrossRef
88.
Falaschetti E, Hingorani AD, Jones A, et al. Adiposity and cardiovascular risk factors in a large contemporary population of pre-pubertal children. Eur Heart J. 2010;31:3063–72.PubMedPubMedCentralCrossRef
89.
Toschke AM, Reinehr T. Different anthropometric index changes in relation to cardiovascular risk profile change. Clin Nutr. 2008;27:457–63.PubMedCrossRef
90.
Calarge CA, Xie D, Fiedorowicz JG, Burns TL, Haynes WG. Rate of weight gain and cardiometabolic abnormalities in children and adolescents. J Pediatr. 2012;161:1010–5.PubMedPubMedCentralCrossRef
91.
Messiah SE, Arheart KL, Natale RA, Hlaing WM, Lipshultz SE, Miller TL. BMI, waist circumference, and selected cardiovascular disease risk factors among preschool-age children. Obesity. 2012;20:1942–9.PubMedCrossRef
92.
Eriksson JG, Kajantie E, Lampl M, Osmond C. Trajectories of body mass index among children who develop type 2 diabetes as adults. J Intern Med. 2015;
93.
Huang RC, de Klerk NH, Smith A, et al. Lifecourse childhood adiposity trajectories associated with adolescent insulin resistance. Diabetes Care. 2011;34:1019–25.PubMedPubMedCentralCrossRef
94.
Lawlor DA, Benfield L, Logue J, et al. Association between general and central adiposity in childhood, and change in these, with cardiovascular risk factors in adolescence: prospective cohort study. BMJ. 2010;341:c 6224.CrossRef
95.
Puder JJ, Schindler C, Zahner L, Kriemler S. Adiposity, fitness and metabolic risk in children: a cross-sectional and longitudinal study. International journal of pediatric obesity : IJPO: an official journal of the International Association for the Study of Obesity. 2011;6:e297–306.CrossRef
96.
Ong KK, Dunger DB. Birth weight, infant growth and insulin resistance. Eur J Endocrinol. 2004;151(Suppl 3):U131–9.PubMedCrossRef
97.
Juonala M, Viikari JS, Raitakari OT. Main findings from the prospective cardiovascular risk in young Finns study. Curr Opin Lipidol. 2013;24:57–64.PubMedCrossRef
98.
Laitinen TT, Pahkala K, Magnussen CG, et al. Ideal cardiovascular health in childhood and cardiometabolic outcomes in adulthood: the cardiovascular risk in young Finns study. Circulation. 2012;125:1971–8.PubMedCrossRef
99.
Berenson GS, Srnivasan SR. Cardiovascular risk factors in youth with implications for aging: the Bogalusa Heart study. Neurobiol Aging. 2005;26:303–7.PubMedCrossRef
100.
Chen W, Srinivasan SR, Li S, Xu J, Berenson GS. Metabolic syndrome variables at low levels in childhood are beneficially associated with adulthood cardiovascular risk: the Bogalusa Heart study. Diabetes Care. 2005;28:126–31.PubMedCrossRef
101.
Morrison JA, Glueck CJ, Wang P. Childhood risk factors predict cardiovascular disease, impaired fasting glucose plus type 2 diabetes mellitus, and high blood pressure 26 years later at a mean age of 38 years: the Princeton-lipid research clinics follow-up study. Metab Clin Exp. 2012;61:531–41.PubMedCrossRef
102.
Sun SS, Grave GD, Siervogel RM, Pickoff AA, Arslanian SS, Daniels SR. Systolic blood pressure in childhood predicts hypertension and metabolic syndrome later in life. Pediatrics. 2007;119:237–46.PubMedCrossRef
103.
Nguyen QM, Srinivasan SR, Xu JH, Chen W, Kieltyka L, Berenson GS. Utility of childhood glucose homeostasis variables in predicting adult diabetes and related cardiometabolic risk factors: the Bogalusa Heart study. Diabetes Care. 2010;33:670–5.PubMedCrossRef
104.
Nguyen QM, Srinivasan SR, Xu JH, Chen W, Berenson GS. Changes in risk variables of metabolic syndrome since childhood in pre-diabetic and type 2 diabetic subjects: the Bogalusa Heart study. Diabetes Care. 2008;31:2044–9.PubMedPubMedCentralCrossRef
105.
Nigam D, Shukla GS, Agarwal AK. Glutathione depletion and oxidative damage in mitochondria following exposure to cadmium in rat liver and kidney. Toxicol Lett. 1999;106:151–7.PubMedCrossRef
106.
Jurczuk M, Brzoska MM, Moniuszko-Jakoniuk J, Galazyn-Sidorczuk M, Kulikowska-Karpinska E. Antioxidant enzymes activity and lipid peroxidation in liver and kidney of rats exposed to cadmium and ethanol. Food and chemical toxicology: an international journal published for the British Industrial Biological Research Association. 2004;42:429–38.CrossRef
107.
Li R, Yuan C, Dong C, Shuang S, Choi MM. In vivo antioxidative effect of isoquercitrin on cadmium-induced oxidative damage to mouse liver and kidney. Naunyn Schmiedeberg's Arch Pharmacol. 2011;383:437–45.CrossRef
108.
Gerich JE. Role of the kidney in normal glucose homeostasis and in the hyperglycaemia of diabetes mellitus: therapeutic implications. Diabetic medicine: a journal of the British Diabetic Association. 2010;27:136–42.CrossRef
109.
Meyer C, Dostou JM, Gerich JE. Role of the human kidney in glucose counterregulation. Diabetes. 1999;48:943–8.PubMedCrossRef
110.
Meyer C, Dostou JM, Welle SL, Gerich JE. Role of human liver, kidney, and skeletal muscle in postprandial glucose homeostasis. Am J Physiol Endocrinol Metab. 2002;282:E419–27.PubMedCrossRef
111.
DeFronzo RA, Davidson JA, Del Prato S. The role of the kidneys in glucose homeostasis: a new path towards normalizing glycaemia. Diabetes Obes Metab. 2012;14:5–14.PubMedCrossRef
Metadata
Title
Maternal blood cadmium, lead and arsenic levels, nutrient combinations, and offspring birthweight
Authors
Yiwen Luo
Lauren E. McCullough
Jung-Ying Tzeng
Thomas Darrah
Avner Vengosh
Rachel L. Maguire
Arnab Maity
Carmen Samuel-Hodge
Susan K. Murphy
Michelle A. Mendez
Cathrine Hoyo
Publication date
01-12-2017
Publisher
BioMed Central
Published in
BMC Public Health / Issue 1/2017
Electronic ISSN: 1471-2458
DOI
https://doi.org/10.1186/s12889-017-4225-8

Other articles of this Issue 1/2017

BMC Public Health 1/2017 Go to the issue

Erratum

Erratum to: The GOOD life: Study protocol for a social norms intervention to reduce alcohol and other drug use among Danish adolescents

Study protocol

Comparing multidisciplinary and brief intervention in employees with different job relations on sick leave due to low back pain: protocol of a randomised controlled trial

Research article

Results and lessons learned from a prevention of weight gain program for low-income overweight and obese young mothers: Mothers In Motion

Research article

A multi-stakeholder evaluation of the Baltimore City virtual supermarket program

Research article

Rethinking physical activity communication: using focus groups to understand women’s goals, values, and beliefs to improve public health

Correction

Correction to: Decisional Balance Inventory (DBI) Adolescent Form for Smoking: Psychometric Properties of the Persian Version