Association between arsenic, cadmium, manganese, and lead levels in private wells and birth defects prevalence in North Carolina: a semi-ecologic study

BMC Public Health

Rebecca C Fry⁶  Robert E Meyer⁵  Andrew F Olshan⁴  Dianne Enright⁷  Amy H Herring¹  Joshua L Warren²  Tania A Desrosiers⁵  Alison P Sanders³ 

[1]Department of Biostatistics, Gillings School of Global Public Health, University of North Carolina, Chapel Hill, NC, USA

[2]Current affiliation: Department of Biostatistics, Yale School of Public Health, Yale University, New Haven, CT, USA

[3]Current affiliation: Department of Preventive Medicine, Icahn School of Medicine at Mount Sinai, New York, NY, USA

[4]Department of Epidemiology, Gillings School of Global Public Health, University of North Carolina, Chapel Hill, NC, USA

[5]Division of Public Health, North Carolina Birth Defects Monitoring Program, State Center for Health Statistics, Raleigh, NC, USA

[6]Department of Environmental Sciences and Engineering, Gillings School of Global Public Health, University of North Carolina, Chapel Hill, NC, USA

[7]Division of Public Health, Health and Spatial Analysis Branch, State Center for Health Statistics, Raleigh, NC, USA

关键词: Congenital anomalies;    Birth defects;    Drinking water;    Congenital heart defect;    Lead;    Manganese;    Cadmium;    Arsenic;    Metals;   

Others  :  1127038
DOI  :  10.1186/1471-2458-14-955

 received in 2014-02-19, accepted in 2014-09-09,  发布年份 2014

【 摘 要 】

Background

Toxic metals including arsenic, cadmium, manganese, and lead are known human developmental toxicants that are able to cross the placental barrier from mother to fetus. In this population-based study, we assess the association between metal concentrations in private well water and birth defect prevalence in North Carolina.

Methods

A semi-ecologic study was conducted including 20,151 infants born between 2003 and 2008 with selected birth defects (cases) identified by the North Carolina Birth Defects Monitoring Program, and 668,381 non-malformed infants (controls). Maternal residences at delivery and over 10,000 well locations measured for metals by the North Carolina Division of Public Health were geocoded. The average level of each metal was calculated among wells sampled within North Carolina census tracts. Individual exposure was assigned as the average metal level of the census tract that contained the geocoded maternal residence. Prevalence ratios (PR) with 95% confidence intervals (CI) were calculated to estimate the association between the prevalence of birth defects in the highest category (≥90^th percentile) of average census tract metal levels and compared to the lowest category (≤50^th percentile).

Results

Statewide, private well metal levels exceeded the EPA Maximum Contaminant Level (MCL) or secondary MCL for arsenic, cadmium, manganese, and lead in 2.4, 0.1, 20.5, and 3.1 percent of wells tested. Elevated manganese levels were statistically significantly associated with a higher prevalence of conotruncal heart defects (PR: 1.6 95% CI: 1.1-2.5).

Conclusions

These findings suggest an ecologic association between higher manganese concentrations in drinking water and the prevalence of conotruncal heart defects.

【 授权许可】

   
2014 Sanders et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

【 参考文献 】

• [1]ATSDR: Toxicological Profile for Arsenic. 2007. Atlanta, GA: CDC; 2007. [cited 2011 July 1]; Available from: http://www.atsdr.cdc.gov/ToxProfiles/TP.asp?id=22&tid=3 webcite
• [2]ATSDR: Toxicological Profile for Lead. Atlanta, GA: CDC; 2007. [cited 2011 July 1]
• [3]ATSDR: Toxicological Profile for Manganese. Atlanta, GA: CDC; 2008. [cited 2011 July 1]
• [4]ATSDR: Toxicological Profile for Cadmium. Atlanta, GA: CDC; 2008. [cited 2011 July 1]
• [5]Rudge CV, Rollin HB, Nogueira CM, Thomassen Y, Rudge MC, Odland JO: The placenta as a barrier for toxic and essential elements in paired maternal and cord blood samples of South African delivering women. J Environ Monit 2009, 11(7):1322-1330.
• [6]Salpietro CD, Gangemi S, Minciuollo PL, Briuglia S, Merlino MV, Stelitano A, Cristani M, Trombetta D, Saija A: Cadmium concentration in maternal and cord blood and infant birth weight: a study on healthy non-smoking women. J Perinat Med 2002, 30(5):395-399.
• [7]Fechter LD: Distribution of manganese in development. Neurotoxicology 1999, 20(2–3):197-201.
• [8]Vahter M: Effects of arsenic on maternal and fetal health. Annu Rev Nutr 2009, 29:381-399.
• [9]Wigle DT, Arbuckle TE, Turner MC, Berube A, Yang Q, Liu S, Krewski D: Epidemiologic evidence of relationships between reproductive and child health outcomes and environmental chemical contaminants. J Toxicol Environ Health B Crit Rev 2008, 11(5–6):373-517.
• [10]Bellinger DC: Teratogen update: lead and pregnancy. Birth Defects Res A Clin Mol Teratol 2005, 73(6):409-420.
• [11]Grazuleviciene R, Nadisauskiene R, Buinauskiene J, Grazulevicius T: Effects of elevated levels of manganese and iron in drinking water on birth outcomes. Pol J Environ Stud 2009, 18(5):819-825.
• [12]Axelrad DA, Bellinger DC, Ryan LM, Woodruff TJ: Dose–response relationship of prenatal mercury exposure and IQ: an integrative analysis of epidemiologic data. Environ Health Perspect 2007, 115(4):609-615.
• [13]Ericson JE, Crinella FM, Clarke-Stewart KA, Allhusen VD, Chan T, Robertson RT: Prenatal manganese levels linked to childhood behavioral disinhibition. Neurotoxicol Teratol 2007, 29(2):181-187.
• [14]Kim Y, Ha EH, Park H, Ha M, Kim Y, Hong YC, Kim EJ, Kim BN: Prenatal lead and cadmium co-exposure and infant neurodevelopment at 6 months of age: The Mothers and Children's Environmental Health (MOCEH) study. Neurotoxicology 2012, 35C:15-22.
• [15]Yu XD, Yan CH, Shen XM, Tian Y, Cao LL, Yu XG, Zhao L, Liu JX: Prenatal exposure to multiple toxic heavy metals and neonatal neurobehavioral development in Shanghai China. Neurotoxicol Teratol 2011, 33(4):437-443.
• [16]Petrini J, Damus K, Russell R, Poschman K, Davidoff MJ, Mattison D: Contribution of birth defects to infant mortality in the United States. Teratology 2002, 66(Suppl 1):S3-S6.
• [17]Mathews TJ, MacDorman MF: Infant mortality statistics from the 2005 period linked birth/infant death data set. Natl Vital Stat Rep 2008, 57:1-32.
• [18]Brent RL: Environmental causes of human congenital malformations: the pediatrician's role in dealing with these complex clinical problems caused by a multiplicity of environmental and genetic factors. Pediatrics 2004, 113(4 Suppl):957-968.
• [19]Zierler S, Theodore M, Cohen A, Rothman KJ: Chemical quality of maternal drinking water and congenital heart disease. Int J Epidemiol 1988, 17(3):589-594.
• [20]Engel RR, Smith AH: Arsenic in drinking water and mortality from vascular disease: an ecologic analysis in 30 counties in the United States. Arch Environ Health 1994, 49(5):418-427.
• [21]Aschengrau A, Zierler S, Cohen A: Quality of community drinking water and the occurrence of late adverse pregnancy outcomes. Arch Environ Health 1993, 48(2):105-113.
• [22]Brender JD, Suarez L, Felkner M, Gilani Z, Stinchcomb D, Moody K, Henry J, Hendricks K: Maternal exposure to arsenic, cadmium, lead, and mercury and neural tube defects in offspring. Environ Res 2006, 101(1):132-139.
• [23]Thompson J, Bannigan J: Cadmium: Toxic effects on the reproductive system and the embryo. Reprod Toxicol 2008, 25(3):304-315.
• [24]Holson JF, Desesso JM, Jacobson CF, Farr CH: Appropriate use of animal models in the assessment of risk during prenatal development: an illustration using inorganic arsenic. Teratology 2000, 62(1):51-71.
• [25]Gilani SH, Alibhai Y: Teratogenicity of metals to chick embryos. J Toxicol Environ Health 1990, 30(1):23-31.
• [26]Shalat SL, Walker DB, Finnell RH: Role of arsenic as a reproductive toxin with particular attention to neural tube defects. J Toxicol Environ Health 1996, 48(3):253-272.
• [27]Kenny JF, Barber NL, Hutson SS, Linsey KS, Lovelace JK, Maupin MA: Estimated use of Water use in the United States in 2005. Reston, VA: U.S. Geological Survey; 2009:1-60.
• [28]EPA: Arsenic in Drinking Water. Washington, DC: USEPA; 2006. [cited 2010 May 24]; Available from: http://epa.gov/safewater/arsenic/index.html webcite
• [29]Spangler AH, Spangler JG: Groundwater manganese and infant mortality rate by county in North Carolina: an ecological analysis. Ecohealth 2009, 6(4):596-600.
• [30]Sanders AP, Messier KP, Shehee M, Rudo K, Serre ML, Fry RC: Arsenic in North Carolina: public health implications. Environ Int 2012, 38(1):10-16.
• [31]Pippin CG, Butczynski M, Clayton J: Distribution of Total Arsenic in Groundwater in the North Carolina Piedmont, D.o.E.a.N.R.-G. Section. Mooresville, NC: NCDENR; 2003.
• [32]Kim D, Miranda ML, Tootoo J, Bradey P, Gelfand AE: Spatial modeling for groundwater arsenic levels in North Carolina. Environ Sci Technol 2011, 45(11):4824-4831.
• [33]SCHS: North Carolina Birth Defects Monitoring Program. 2013. Available from: http://www.schs.state.nc.us/units/bdmp/ webcite
• [34]NBDPN: State birth defects surveillance program data. BDRA (Part A) 2013, 97(10):p. S1-S172.
• [35]EPA: Drinking Water Contaminants: National Primary Drinking Water Regulations. 2012. [cited 2013 February 14]; Available from: http://water.epa.gov/drink/contaminants/index.cfm webcite
• [36]DeSimone LA, Hamilton PA, Gilliom RJ: The quality of our nation's waters - quality of water from domestic wells in principal aquifers of the United States, 1991-2004- overview and major findings. U S Geol Surv Circular 2009, 1332:48.
• [37]Bhagure GR, Mirgane SR: Heavy metal concentrations in groundwaters and soils of Thane Region of Maharashtra, India. Environ Monit Assess 2011, 173(1–4):643-652.
• [38]EPA: Actions You Can Take to Reduce Lead in Drinking Water. 1993. [cited 2013 June 2]; Available from: http://water.epa.gov/drink/info/lead/lead1.cfm webcite
• [39]Liu J, Jin L, Zhang L, Li Z, Wang L, Ye R, Zhang Y, Ren A: Placental concentrations of manganese and the risk of fetal neural tube defects. J Trace Elem Med Biol 2013, 27(4):322-325.
• [40]Gerber GB, Leonard A, Hantson P: Carcinogenicity, mutagenicity and teratogenicity of manganese compounds. Crit Rev Oncol Hematol 2002, 42(1):25-34.
• [41]Hafeman D, Factor-Litvak P, Cheng Z, van Geen A, Ahsan H: Association between manganese exposure through drinking water and infant mortality in Bangladesh. Environ Health Perspect 2007, 115(7):1107-1112.
• [42]Vigeh M, Yokoyama K, Ramezanzadeh F, Dahaghin M, Fakhriazad E, Seyedaghamiri Z, Araki S: Blood manganese concentrations and intrauterine growth restriction. Reprod Toxicol 2008, 25(2):219-223.
• [43]Zota AR, Ettinger AS, Bouchard M, Amarasiriwardena CJ, Schwartz J, Hu H, Wright RO: Maternal blood manganese levels and infant birth weight. Epidemiology 2009, 20(3):367-373.
• [44]Spencer A: Whole blood manganese levels in pregnancy and the neonate. Nutrition 1999, 15(10):731-734.
• [45]Takser L, Lafond J, Bouchard M, St-Amour G, Mergler D: Manganese levels during pregnancy and at birth: relation to environmental factors and smoking in a Southwest Quebec population. Environ Res 2004, 95(2):119-125.
• [46]Jiang Y, Zheng W: Cardiovascular toxicities upon manganese exposure. Cardiovasc Toxicol 2005, 5(4):345-354.
• [47]Bouchard MF: Manganese in drinking water: Bouchard responds. Environ Health Perspect 2011, 119(6):A241.
• [48]Elsner RJ, Spangler JG: Neurotoxicity of inhaled manganese: public health danger in the shower? Med Hypotheses 2005, 65(3):607-616.
• [49]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(2):190-205.
• [50]Toccalino PL, Norman JE, Scott JC: Chemical mixtures in untreated water from public-supply wells in the U.S.–occurrence, composition, and potential toxicity. Sci Total Environ 2012, 431:262-270.
• [51]Macdonell JE, Campbell H, Stone DH: Lead levels in domestic water supplies and neural tube defects in Glasgow. Arch Dis Child 2000, 82(1):50-53.
• [52]Jackson LW, Correa-Villasenor A, Lees PS, Dominici F, Stewart PA, Breysse PN, Matanoski G: Parental lead exposure and total anomalous pulmonary venous return. Birth Defects Res A Clin Mol Teratol 2004, 70(4):185-193.
• [53]Bound JP, Harvey PW, Francis BJ, Awwad F, Gatrell AC: Involvement of deprivation and environmental lead in neural tube defects: a matched case–control study. Arch Dis Child 1997, 76(2):107-112.
• [54]Cengiz B, Soylemez F, Ozturk E, Cavdar AO: Serum zinc, selenium, copper, and lead levels in women with second-trimester induced abortion resulting from neural tube defects: a preliminary study. Biol Trace Elem Res 2004, 97(3):225-235.
• [55]Irgens A, Kruger K, Skorve AH, Irgens LM: Reproductive outcome in offspring of parents occupationally exposed to lead in Norway. Am J Ind Med 1998, 34(5):431-437.
• [56]Kristensen P, Irgens LM, Daltveit AK, Andersen A: Perinatal outcome among children of men exposed to lead and organic solvents in the printing industry. Am J Epidemiol 1993, 137(2):134-144.
• [57]Webster WS, Messerle K: Changes in the mouse neuroepithelium associated with cadmium-induced neural tube defects. Teratology 1980, 21(1):79-88.
• [58]McClain RM, Becker BA: Teratogenicity, fetal toxicity, and placental transfer of lead nitrate in rats. Toxicol Appl Pharmacol 1975, 31(1):72-82.
• [59]Thompson J, Bannigan J: Effects of cadmium on formation of the ventral body wall in chick embryos and their prevention by zinc pretreatment. Teratology 2001, 64(2):87-97.
• [60]Thompson JM, Bannigan JG: Omphalocele induction in the chick embryo by administration of cadmium. J Pediatr Surg 2007, 42(10):1703-1709.
• [61]Grewal J, Carmichael SL, Ma C, Lammer EJ, Shaw GM: Maternal periconceptional smoking and alcohol consumption and risk for select congenital anomalies. Birth Defects Res A Clin Mol Teratol 2008, 82(7):519-526.
• [62]Liu-Mares W, Mackinnon JA, Sherman R, Fleming LE, Rocha-Lima C, Hu JJ, Lee DJ: Pancreatic cancer clusters and arsenic-contaminated drinking water wells in Florida. BMC Cancer 2013, 13:111. BioMed Central Full Text
• [63]Nieder AM, MacKinnon JA, Fleming LE, Kearney G, Hu JJ, Sherman RL, Huang Y, Lee DJ: Bladder cancer clusters in Florida: identifying populations at risk. J Urol 2009, 182(1):46-50. discussion 51
• [64]Katz EA, Shaw GM, Schaffer DM: Exposure assessment in epidemiologic studies of birth defects by industrial hygiene review of maternal interviews. Am J Ind Med 1994, 26(1):1-11.
• [65]Borja-Aburto VH, Bermudez-Castro O, Lacasana-Navarro M, Kuri P, Bustamante-Montes P, Torres-Meza V: Difficulties of the methods for studying environmental exposure and neural tube defects. Salud Publica Mex 1999, 41(Suppl 2):p. S124-p. S131.
• [66]Sanders AP, Flood K, Chiang S, Herring AH, Wolf L, Fry RC: Towards prenatal biomonitoring in North Carolina: assessing arsenic, cadmium, mercury, and lead levels in pregnant women. PLoS One 2012, 7(3):e31354.
• [67]Canfield MA, Ramadhani TA, Langlois PH, Waller DK: Residential mobility patterns and exposure misclassification in epidemiologic studies of birth defects. J Expo Sci Environ Epidemiol 2006, 16(6):538-543.
• [68]Forrester MB, Merz RD: Impact of excluding cases with known chromosomal abnormalities on the prevalence of structural birth defects, Hawaii, 1986–1999. Am J Med Genet A 2004, 128A(4):383-388.
• [69]Ahir BK, Sanders AP, Rager JE, Fry RC: Systems biology and birth defects prevention: blockade of the glucocorticoid receptor prevents arsenic-induced birth defects. Environ Health Perspect 2013, 121(3):332-338.