Heavy metals exposure levels and their correlation with different clinical forms of fetal growth restriction

Sally Sabra, Ebba Malmqvist, Alicia Saborit, Eduard Gratacós, Maria Dolores Gomez Roig, Sally Sabra, Ebba Malmqvist, Alicia Saborit, Eduard Gratacós, Maria Dolores Gomez Roig

Abstract

Background: Prenatal heavy metals exposure has shown a negative impact on birth weight. However, their influence on different clinical forms of fetal smallness was never assessed.

Objectives: To investigate whether there is a differential association between heavy metals exposure and fetal smallness subclassification into intrauterine growth restriction (IUGR) and small-for-gestational age (SGA).

Method: In this prospective case-control study, we included 178 mother-infant pairs; 96 of appropriate for gestational age (AGA) and 82 of small fetuses diagnosed in third trimester. The small ones were further subclassified into IUGR, n = 49 and SGA, n = 33. Cadmium (Cd), mercury (Hg), lead (Pb), arsenic (As) and zinc (Zn) levels were measured in the maternal and cord serum, and in the placentas of the three groups.

Results: Maternal serum level of Cd (p<0.001) was higher in the small fetuses compared to AGA. Fetal serum level of Cd (p<0.001) was increased in the small fetuses compared to AGA. Fetal serum level of Hg (p<0.05) showed an increase in SGA compared to both IUGR and AGA. Fetal serum level of Zn was increased in the AGA (p < 0.001) compared to each of the small fetuses groups. Only differences in the levels between the small fetuses' subgroups were detected in the fetal serum levels of Cd and Hg. Fetal birth weight was negatively correlated with the fetal serum level of Cd (p < 0.001). No differences in the placental heavy metal levels were observed among the groups.

Conclusion: Fetal serum levels of Cd showed differential correlation between small fetuses' clinical subclassification, which together with the increased Cd levels in both maternal and fetal serum of the small fetuses reinforce the negative influence of heavy metals on birth weight. These findings provide more opportunities to verify the role of heavy metals exposure in relation to small fetuses' subclassification.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Fig 1. Flow chart of the total…
Fig 1. Flow chart of the total number of recruited patients, number of excluded cases and our cohort three subgroups.
AGA: Appropriate for gestational age; IUGR: intrauterine growth restriction; SGA: small for gestational age.
Fig 2. Neonatal birth weights of the…
Fig 2. Neonatal birth weights of the three groups.
Mean birth weights of the AGA (white), IUGR (grey) and SGA (dashed) groups are presented, significant differences in the birth weight of the AGA compared to the IUGR and SGA (p

Fig 3

Comparison between the detected maternal…

Fig 3

Comparison between the detected maternal serum levels of Cd (A), Hg (B) and…

Fig 3
Comparison between the detected maternal serum levels of Cd (A), Hg (B) and As (C) in the three groups of our cohort. AGA: appropriate for gestational age; IUGR: intrauterine growth restriction; SGA: small for gestational age. Cd: cadmium; Hg: mercury; As: arsenic Kruskal-Wallis and Mann Whitney tests were used. * p

Fig 4

Comparison between the detected fetal…

Fig 4

Comparison between the detected fetal serum levels of Cd (A) and Hg (B)…

Fig 4
Comparison between the detected fetal serum levels of Cd (A) and Hg (B) in the three groups of our cohort. AGA: appropriate for gestational age; IUGR: intrauterine growth restriction; SGA: small for gestational age; Cd: cadmium; Hg: mercury. Kruskal-Wallis and Mann Whitney tests were used. * p
Similar articles
Cited by
References
    1. Bernstein IM, Horbar JD, Badger GJ, Ohlsson A, Golan A. Morbidity and mortality among very-low-birth-weight neonates with intrauterine growth restriction. The Vermont Oxford Network. Am J Obstet Gynecol. 2000. January; 182(1 Pt 1):198–206. - PubMed
    1. Brodsky D, Christou H. Current concepts in intrauterine growth restriction. J Intensive Care Med. 2004. Nov-Dec; 19(6):307–19. doi: 10.1177/0885066604269663 - DOI - PubMed
    1. Hunt CE. Small for gestational age infants and sudden infant death syndrome: a confluence of complex conditions. Arch Dis Child Fetal Neonatal Ed. 2007. November; 92(6):F428–9. doi: 10.1136/adc.2006.112243 - DOI - PMC - PubMed
    1. Bamfo J K and Odibo AO. Diagnosis and Management of Fetal Growth Restriction. J Pregnancy. 2011; 2011: 640715 doi: 10.1155/2011/640715 - DOI - PMC - PubMed
    1. Markel TA, Engelstad H, and Poindexter BB. Predicting Disease Severity of Necrotizing Enterocolitis: How to Identify Infants for Future Novel Therapies. J Clin Neonatol. 2014. Jan-Mar; 3(1): 1–9. doi: 10.4103/2249-4847.128717 - DOI - PMC - PubMed
Show all 89 references
MeSH terms
Grant support
This work has been funded with support of the Erasmus Programme of the European Union (framework agreement number: 2013-0040).
[x]
Cite
Copy Download .nbib
Format: AMA APA MLA NLM

NCBI Literature Resources

MeSH PMC Bookshelf Disclaimer

The PubMed wordmark and PubMed logo are registered trademarks of the U.S. Department of Health and Human Services (HHS). Unauthorized use of these marks is strictly prohibited.

Follow NCBI
Fig 3
Fig 3
Comparison between the detected maternal serum levels of Cd (A), Hg (B) and As (C) in the three groups of our cohort. AGA: appropriate for gestational age; IUGR: intrauterine growth restriction; SGA: small for gestational age. Cd: cadmium; Hg: mercury; As: arsenic Kruskal-Wallis and Mann Whitney tests were used. * p

Fig 4

Comparison between the detected fetal…

Fig 4

Comparison between the detected fetal serum levels of Cd (A) and Hg (B)…

Fig 4
Comparison between the detected fetal serum levels of Cd (A) and Hg (B) in the three groups of our cohort. AGA: appropriate for gestational age; IUGR: intrauterine growth restriction; SGA: small for gestational age; Cd: cadmium; Hg: mercury. Kruskal-Wallis and Mann Whitney tests were used. * p
Similar articles
Cited by
References
    1. Bernstein IM, Horbar JD, Badger GJ, Ohlsson A, Golan A. Morbidity and mortality among very-low-birth-weight neonates with intrauterine growth restriction. The Vermont Oxford Network. Am J Obstet Gynecol. 2000. January; 182(1 Pt 1):198–206. - PubMed
    1. Brodsky D, Christou H. Current concepts in intrauterine growth restriction. J Intensive Care Med. 2004. Nov-Dec; 19(6):307–19. doi: 10.1177/0885066604269663 - DOI - PubMed
    1. Hunt CE. Small for gestational age infants and sudden infant death syndrome: a confluence of complex conditions. Arch Dis Child Fetal Neonatal Ed. 2007. November; 92(6):F428–9. doi: 10.1136/adc.2006.112243 - DOI - PMC - PubMed
    1. Bamfo J K and Odibo AO. Diagnosis and Management of Fetal Growth Restriction. J Pregnancy. 2011; 2011: 640715 doi: 10.1155/2011/640715 - DOI - PMC - PubMed
    1. Markel TA, Engelstad H, and Poindexter BB. Predicting Disease Severity of Necrotizing Enterocolitis: How to Identify Infants for Future Novel Therapies. J Clin Neonatol. 2014. Jan-Mar; 3(1): 1–9. doi: 10.4103/2249-4847.128717 - DOI - PMC - PubMed
Show all 89 references
MeSH terms
Grant support
This work has been funded with support of the Erasmus Programme of the European Union (framework agreement number: 2013-0040).
[x]
Cite
Copy Download .nbib
Format: AMA APA MLA NLM
Fig 4
Fig 4
Comparison between the detected fetal serum levels of Cd (A) and Hg (B) in the three groups of our cohort. AGA: appropriate for gestational age; IUGR: intrauterine growth restriction; SGA: small for gestational age; Cd: cadmium; Hg: mercury. Kruskal-Wallis and Mann Whitney tests were used. * p

References

    1. Bernstein IM, Horbar JD, Badger GJ, Ohlsson A, Golan A. Morbidity and mortality among very-low-birth-weight neonates with intrauterine growth restriction. The Vermont Oxford Network. Am J Obstet Gynecol. 2000. January; 182(1 Pt 1):198–206.
    1. Brodsky D, Christou H. Current concepts in intrauterine growth restriction. J Intensive Care Med. 2004. Nov-Dec; 19(6):307–19. doi:
    1. Hunt CE. Small for gestational age infants and sudden infant death syndrome: a confluence of complex conditions. Arch Dis Child Fetal Neonatal Ed. 2007. November; 92(6):F428–9. doi:
    1. Bamfo J K and Odibo AO. Diagnosis and Management of Fetal Growth Restriction. J Pregnancy. 2011; 2011: 640715 doi:
    1. Markel TA, Engelstad H, and Poindexter BB. Predicting Disease Severity of Necrotizing Enterocolitis: How to Identify Infants for Future Novel Therapies. J Clin Neonatol. 2014. Jan-Mar; 3(1): 1–9. doi:
    1. Ismail H, Chang YL. Sequelae of Fetal Growth Restriction. J Med Ultrasound. 2012; 20(4): 191–200.
    1. Cosmi E, Fanelli T, Visentin S, Trevisanuto D, Zanardo V. Consequences in Infants That Were Intrauterine Growth Restricted. Review Article. J Pregnancy. 2011; Volume 2011 (2011), Article ID 364381, 6 pages. doi:
    1. Longo S, Bollani L, Decembrino L, Di Comite A, Angelini M, Stronati M. Short-term and long-term sequelae in intrauterine growth retardation (IUGR). J Matern Fetal Neonatal Med. 2013. February; 26(3):222–5. doi:
    1. Barker DJ, Winter PD, Osmond C, Margetts B, Simmonds SJ. Weight in infancy and death from ischaemic heart disease. Lancet. 1989. September 9;2(8663):577–80.
    1. Hanna CW, Bloom MS, Robinson WP, Kim D, Parsons PJ, vom Saal FS et al. DNA methylation changes in whole blood is associated with exposure to the environmental contaminants, mercury, lead, cadmium and bisphenol A, in women undergoing ovarian stimulation for IVF. Hum Reprod 2012; 27: 1401–1410. doi:
    1. Clarkson TW, Nordberg GF, Sager PR. Reproductive and developmental toxicity of metals. Scand J Work Environ Health. 1985. June; 11(3 Spec No):145–54.
    1. Kampa M, Castanas E. Human health effects of air pollution. Environ Pollut. 2008. January;151(2):362–7. doi:
    1. Singh R, Gautam N, Mishra A, Gupta R. Heavy metals and living systems: An overview. Indian J Pharmacol. 2011. May;43(3):246–53. doi:
    1. Tchounwou PB, Yedjou CG, Patlolla AK, Sutton DJ. Heavy metal toxicity and the environment. EXS. 2012;101:133–64. doi:
    1. Bose-O'Reilly S, McCarty KM, Steckling N, Lettmeier B. Mercury exposure and children's health. Curr Probl Pediatr Adolesc Health Care. 2010. September;40(8):186–215. doi:
    1. Talia Sanders, Yiming Liu, Virginia Buchner, Paul B. Tchounwou. Neurotoxic Effects and Biomarkers of Lead Exposure: A Review. Rev Environ Health. 2009. Jan–Mar; 24(1): 15–45.
    1. Hong YS, Song KH, Chung JY. Health effects of chronic arsenic exposure. J Prev Med Public Health. 2014. September;47(5):245–52. doi: Epub 2014 Sep 11.
    1. Tchounwou PB, Wilson B, Ishaque A. Important considerations in the development of public health advisories for arsenic and arsenic-containing compounds in drinking water. Rev Environ Health. 1999. Oct-Dec;14(4):211–29.
    1. Lafuente A, Márquez N, Pérez-Lorenzo M, Pazo D, Esquifino AI. Pubertal and postpubertal cadmium exposure differentially affects the hypothalamic-pituitary-testicular axis function in the rat. Food Chem Toxicol 2000; 38(10): 913–23.
    1. Kippler M, Hoque AM, Raqib R, Ohrvik H, Ekström EC, Vahter M. Accumulation of cadmium in human placenta interacts with the transport of micronutrients to the fetus. Toxicol Lett. 2010. February 1; 192(2):162–8. doi:
    1. Vejrup K, Brantsæter AL, Knutsen HK, Magnus P, Alexander J, Kvalem HE, Meltzer HM, Haugen M. Prenatal mercury exposure and infant birth weight in the Norwegian Mother and Child Cohort Study. Public Health Nutr. 2014. September;17(9):2071–80. doi:
    1. Xie X, Ding G, Cui C, Chen L, Gao Y, Zhou Y, et al. The effects of low-level prenatal lead exposure on birth outcomes. Environ Pollut. 2013. April; 175:30–4. doi:
    1. Yaping Jina, Shuhua Xib, Xin Lia, Chunwei Lua, Gexin Lia, Yuanyuan Xua, Chunqing Qua,Yuhong Niua, Guifan Suna. Arsenic speciation transported through the placenta from mother mice to their newborn pups. Environmental Research 101 (2006) 349–355. doi:
    1. He W, Greenwell RJ, Brooks DM, Calderón-Garciduenas L, Beall HD, Coffin JD. Arsenic exposure in pregnant mice disrupts placental vasculogenesis and causes spontaneous abortion. Toxicol Sci 2007;99:244–53. doi:
    1. Rahman A, Persson LA, Nermell B, El Arifeen S, Ekstrom EC, Smith AH. Arsenic exposure and risk of spontaneous abortion, stillbirth, and infant mortality. Epidemiology. 2010;21(6):797–804. doi:
    1. Raymond A Wuana and Felix E Okieimen. Heavy Metals in Contaminated Soils: A Review of Sources, Chemistry, Risks and Best Available Strategies for Remediation. ISRN Ecology,Volume 2011, doi:
    1. Uriu-Adams JY, Keen CL. Zinc and reproduction: effects of zinc deficiency on prenatal and early postnatal development. Birth Defects Res B Dev Reprod Toxicol. 2010. August; 89(4):313–25. doi:
    1. Butler Walker J, Houseman J, Seddon L, McMullen E, Tofflemire K, Mills C, et al. Maternal and umbilical cord blood levels of mercury, lead, cadmium, and essential trace elements in Arctic Canada. Environ Res. 2006. March; 100(3):295–318. doi:
    1. Taylor CM, Tilling K, Golding J, Emond AM. Low level lead exposure and pregnancy outcomes in an observational birth cohort study: dose–response relationships. BMC Res Notes. 2016. June 4; 9:291 doi:
    1. Osman K, Akesson A, Berglund M, Bremme K, Schütz A, Ask K, et al. Toxic and essential elements in placentas of Swedish women. Clin Biochem. 2000. March; 33(2):131–8.
    1. Rahbar MH, Samms-Vaughan M, Dickerson AS, Hessabi M, Bressler J, Desai CC, et al. Concentration of Lead, Mercury, Cadmium, Aluminum, Arsenic and Manganese in Umbilical Cord Blood of Jamaican Newborns. Int J Environ Res Public Health. 2015. April 23; 12(5):4481–501. doi:
    1. Kim BM, Ha M, Park HS, Lee BE, Kim YJ, Hong YC, et al. The Mothers and Children’s Environmental Health (MOCEH) study. The MOCEH Study Group. Eur J Epidemiol. 2009; 24(9):573–83. doi:
    1. Renzetti S, Just AC, Burris HH, Oken E, Amarasiriwardena C, Svensson K, et al. The association of lead exposure during pregnancy and childhood anthropometry in the Mexican PROGRESS cohort. Environ Res. 2017. January; 152: 226–232. doi:
    1. Zhang YL, Zhao YC, Wang JX, Zhu HD, Liu QF, Fan YG, Effect of Environmental Exposure to Cadmium on Pregnancy Outcome and Fetal Growth: A Study on Healthy Pregnant Women in China. J Environ Sci Health a Tox Hazard Subst Environ Eng. 2004; 39(9):2507–15.
    1. Jiang CB, Hsi HC, Fan CH, Chien LC. Fetal Exposure to Environmental Neurotoxins in Taiwan. PLoS One. 2014. October 9; 9(10):e109984 doi:
    1. Lin CM, Doyle P, Wang D, Hwang YH, Chen PC. Does prenatal cadmium exposure affect fetal and child growth? Occup Environ Med. 2011. September; 68(9):641–6. doi:
    1. Figueras F., Gratacós E. Update on the Diagnosis and Classification of Fetal Growth Restriction and Proposal of a Stage-Based Management Protocol. Fetal Diagn Ther 2014;36: 86–98. doi:
    1. Butt K, Lim K. Determination of gestational age by ultrasound. J Obstet Gynaecol Can. 2014. February;36(2):171–181. doi:
    1. Figueras F, Meler E, Iraola A, Eixarch E, Coll O, Figueras J, Francis A, Gratacos E, Gardosi J. Customized birthweight standards for a Spanish population. Eur J Obstet Gynecol Reprod Biol. 2008. January;136(1):20–4. doi:
    1. Cornelis R, Heinzow B, Herber RF, Christensen JM, Poulsen OM, Sabbioni E, et al. Sample Collection Guidelines for Trace Elements in Blood and Urine. J Trace Elem Med Biol. 1996. June;10(2):103–27.
    1. Latkoczy C, Günther D. Enhanced sensitivity in inductively coupled plasma sector field mass spectrometry for direct solid analysis using laser ablation (LA-ICP-SFMS). J. Anal. At. Spectrom., 2002,17, 1264–1270.
    1. Roels H, Hubermont G, Buchet JP, Lauwerys R. Placental transfer of lead, mercury, cadmium, and carbon monoxide in women. III. Factors influencing the accumulation of heavy metals in the placenta and the relationship between metal concentration in the placenta and in maternal and cord blood. Environ Res. 1978. July; 16(1–3):236–47.
    1. Truska P, Rosival L, Balazova G, Hinst J, Rippel A, Palusova O, et al. Blood and placental concentrations of cadmium, lead, and mercury in mothers and their newborns. J Hyg Epidemiol Microbiol Immunol. 1989; 33(2):141–7.
    1. Gundacker C, Hengstschlager M. The role of the placenta in fetal exposure to heavy metals. Wien. Med. Wochenschr. 2012; 162:201–206. doi:
    1. Caserta D, Graziano A, Lo Monte G, Bordi G, Moscarini M. Heavy metals and placental fetal-maternal barrier: A mini-review on the major concerns. Eur. Rev. Med. Pharmacol. Sci. 2013;17: 2198–2206.
    1. Frery N, Nessmann C, Girard F, Lafond J, Moreau T, Blot P, et al. Environmental exposure to cadmium and human birthweight. Toxicology. 1993. April 30; 79(2):109–18.
    1. Needham LL, Grandjean P, Heinzow B, Jørgensen PJ, Nielsen F, Patterson DG Jr, et al. Partition of environmental chemicals between maternal and fetal blood and tissues. Environ Sci Technol. 2011. February 1;45(3):1121–6. doi:
    1. Al-Saleh I, Shinwari N, Mashhour A, Mohamed Gel D, Rabah A. Heavy metals (lead, cadmium and mercury) in maternal, cord blood and placenta of healthy women. Int J Hyg Environ Health. 2011. March; 214(2):79–101. doi:
    1. Clare E Casey and Marion F Robinson. Copper, manganese, zinc, nickel, cadmium and lead in human foetal tissues. Br. J. Nutr. (1978), 39, 639
    1. Wier PJ, Miller RK, Maulik D, DiSant'Agnese PA. Toxicity of cadmium in the perfused human placenta. Toxicol. Appl. Pharmacol. 105, 156–171.
    1. Rentschler G, Kippler M, Axmon A, Raqib R, Skerfving S, Vahter M, Broberg K. Cadmium concentrations in human blood and urine are associated with polymorphisms in zinc transporter genes. Metallomics. 2014. April;6(4):885–91. doi:
    1. Angeli JK, Cruz Pereira CA, de Oliveira Faria T, Stefanon I, Padilha AS, Vassallo DV. Cadmium exposure induces vascular injury due to endothelial oxidative stress: the role of local angiotensin II and COX-2. Free Radic Biol Med. 2013. December;65:838–48. doi:
    1. Schroeder HA. Cadmium as a factor in hypertension. J Chronic Dis 1965; 18: 647–656.
    1. Sahman P. Trace elements and blood pressure. Ann Intern Med 1983; 98: 823–827.
    1. Kopp S J, Glonek T, Perry H M, Edanger M, Perry E F. Cardiovascular actions of cadmium at environmental exposure levels. Science 1982; 217: 837–839.
    1. Järup L. Hazards of heavy metal contamination. Br Med Bull. 2003;68:167–82.
    1. Peereboom-Stegeman JH, van der Velde WJ, Dessing JW.1983. Influence of cadmium on placental structure. Ecotoxicol Environ Saf. 1983. February;7(1):79–86.
    1. Frery N, Nessmann C, Girard F, Lafond J, Moreau T, Blot P, et al. Environmental exposure to cadmium and human birthweight. Toxicology. 1993. April 30; 79(2):109–18.
    1. Zhang Y. L. et al. Effect of environmental exposure to cadmium on pregnancy outcome and fetal growth: a study on healthy pregnant women in China. J Environ Sci Health A Tox Hazard Subst Environ Eng. 2004;39(9):2507–15.
    1. 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. March;217(2–3):205–18. doi:
    1. Bjerregaard P, Hansen JC. Effects of smoking and marine diet on birthweight in Greenland. Arctic Med Res. 1996. October; 55(4):156–64.
    1. Karagas MR, Choi AL, Oken E, Horvat M, Schoeny R, Kamai E et al. Evidence on the human health effects of low-level methylmercury exposure. Environ Health Perspect. 2012. June; 120(6):799–806. doi:
    1. Kim YM, Chung JY, An HS, Park SY, Kim BG, Bae JW, et al. Biomonitoring of Lead, Cadmium, Total Mercury, and Methylmercury Levels in Maternal Blood and in Umbilical Cord Blood at Birth in South Korea. Int J Environ Res Public Health. 2015. October 26;12(10):13482–93. doi:
    1. Lederman SA, Jones RL, Caldwell KL, Rauh V, Sheets SE, Tang D, et al. Relation between cord blood mercury levels and early child development in a World Trade Center cohort. Environ Health Perspect. 2008. August;116(8):1085–91. doi:
    1. Vejrup K, Brantsæter AL, Knutsen HK, Magnus P, Alexander J, Kvalem HE, et al. Prenatal mercury exposure and infant birth weight in the Norwegian Mother and Child Cohort Study Public Health Nutr. 2014. September; 17(9):2071–80. doi:
    1. Chen Z, Myers R, Wei T, Bind E, Kassim P, Wang G, et al. Placental transfer and concentrations of cadmium, mercury, lead, and selenium in mothers, newborns, and young children. J Expo Sci Environ Epidemiol. 2014. Sep-Oct; 24(5):537–44. doi:
    1. Lee BE, Hong YC, Park H. Interaction between GSTM1/GSTT1 polymorphism and blood mercury on birth weight. Environ Health Perspect. 2010. March; 118(3):437–43. doi:
    1. Hur J, Kim H, Ha EH, Park H, Ha M, Kim Y, Hong YC, Chang N. Birth weight of Korean infants is affected by the interaction of maternal iron intake and GSTM1 polymorphism. J Nutr. 2013. January; 143(1):67–73. doi:
    1. Harville EW, Hertz-Picciotto I, Schramm M, Watt-Morse M, Chantala K, Osterloh J, Parsons PJ, Rogan W. Factors influencing the difference between maternal and cord blood lead. Occup Environ Med. 2005. April; 62(4):263–9. doi:
    1. Harada M. Minamata disease: methylmercury poisoning in Japan caused by environmental pollution. Crit Rev Toxicol. 1995; 25:1–24. doi:
    1. Rice KM, Walker EM Jr, Wu M, Gillette C, Blough ER. Environmental Mercury and Its Toxic Effects. J Prev Med Public Health. 2014. March; 47(2):74–83. doi:
    1. Bjerregaard P & Hansen JC. Organochlorines and heavy metals in pregnant women from the Disko Bay area in Greenland. Sci Total Environ. 2000. January 17; 245(1–3):195–202.
    1. Grandjean P, Bjerve KS, Weihe P, Steuerwald U. Birthweight in a fishing community: significance of essential fatty acids and marine food contaminants. Int J Epidemiol. 2001. December;30 (6):1272–8.
    1. Lucas M, Dewailly E, Muckle G, Ayotte P, Bruneau S, Gingras S et al. Gestational age and birth weight in relation to n-3 fatty acids among Inuit (Canada). Lipids. 2004. July;39(7):617–26.
    1. Grandjean P, Landrigan PJ. Neurobehavioural effects of developmental toxicity. Lancet Neurol. 2014. March; 13(3):330–8. doi:
    1. Guo Y, Huo X, Li Y, Wu K, Liu J, Huang J, et al. 2010. Monitoring of lead, cadmium, chromium and nickel in placenta from an e-waste recycling town in China. Sci Total Environ 408:3113–3117. doi:
    1. Tekin D, Kayaaltı Z, Söylemezoğlu T. The effects of metallothionein 2A polymorphism on lead metabolism: are pregnant women with a heterozygote genotype for metallothionein 2A polymorphism and their newborns at risk of having higher blood lead levels? Int Arch Occup Environ Health. 2012. August;85(6):631–7. doi:
    1. Thomas S, Arbuckle TE, Fisher M, Fraser WD, Ettinger A, King W. Metals exposure and risk of small-for-gestational age birth in a Canadian birth cohort: The MIREC study. Environ Res. 2015. July;140:430–9. doi:
    1. Rahman A, Vahter M, Smith AH, Nermell B, Yunus M, El Arifeen S, et al. Arsenic exposure during pregnancy and size at birth: a prospective cohort study in Bangladesh. Am J Epidemiol. 2009. February 1;169(3):304–12. doi:
    1. Broberg K, Ahmed S, Engström K, Hossain MB, Jurkovic MS, Bottai M, et al. Arsenic exposure in early pregnancy alters genome-wide DNA methylation in cord blood, particularly in boys. J Dev Orig Health Dis. 2014. August;5(4):288–98. doi:
    1. Llanos MN, Ronco AM. M. Fetal growth restriction is related to placental levels of cadmium, lead and arsenic but not with antioxidant activities. Reprod Toxicol. 2009. January;27(1):88–92. doi:
    1. Wier PJ, Miller RK, Maulik D, DiSant'Agnese PA. Toxicity of cadmium in the perfused human placenta. Toxicol Appl Pharmacol. 1990. August;105(1):156–71.
    1. Piasek M, Blanusa M, Kostial K, Laskey JW. Placental cadmium and progesterone concentrations in cigarette smokers. Reprod Toxicol. 2001. Nov-Dec;15(6):673–81.
    1. Lagerkvist BI, Sandberg S, Frech W, Jin T, Nordberg GF. 1996. Is placenta a good indicator of cadmium and lead exposure? Arch Environ Health. 1996 Sep-Oct;51(5):389–94. doi:
    1. Burton GJ, Fowden AL. The placenta: a multifaceted, transient organ. Philos Trans R Soc Lond B Biol Sci. 2015. March 5;370(1663):20140066 doi:
    1. Kuhnert PM, Kuhnert BR, Bottoms SF, Erhard P. Cadmium levels in maternal blood, fetal cord blood, and placental tissues of pregnant women who smoke. Am J Obstet Gynecol. 1982. April 15;142(8):1021–5.
    1. Fiala J, Hrubá D, Rézl P. Cadmium and zinc concentrations in human placentas. Cent Eur J Public Health. 1998. August; 6(3):241–8.
    1. Rauh VA, Horton MK, Miller RL, Whyatt RM, Perera F. Neonatology and the Environment: Impact of Early Exposure to Airborne Environmental Toxicants on Infant and Child Neurodevelopment. Neoreviews. 2010;11:363–369. doi:
    1. Thomas S, Arbuckle TE, Fisher M, Fraser WD, Ettinger A, King W. Metals exposure and risk of small-for-gestational age birth in a Canadian birth cohort: The MIREC study. Environ Res. 2015. July;140:430–9. doi:

Source: PubMed

Sponsors and Collaborators

Medical Conditions

Drug Interventions

3
Subscribe