High-level toxic metal exposure has become rare in the recent years. Although, it has not known whether relatively lower exposure may adversely affect human reproductive system. Spontaneous abortion (SA) is a serious reproductive problem, which, in many cases, the cause(s) is not clearly understood. To assess the relationship between prenatal blood level of metals and SA risk, we compared blood concentration of some heavy metals in samples taken from mothers recruited in Tehran Environment and Neurodevelopmental Defects (TEND) study conducted on apparently healthy pregnant women in Tehran, Iran who subsequently experienced spontaneous abortion with mothers who their pregnancy ended to live births. During early gestation, 206 women were enrolled to the survey and followed up till fetal abortion or baby deliveries occur. Blood metal concentrations were measured using an inductively coupled plasma mass spectrometer. The mean blood levels of lead, antimony, and nickel were higher in SA than ongoing pregnancy; however, this difference was not statistically significant. When adjusted for covariates, the logistic regression analysis showed significant association between maternal age and the risk of SA in all models. Among toxic metals only antimony had a noticeable positive relation with the risk of SA (OR: 1.65, 95% CI:1.08–2.52, P value: 0.02). Pearson’s correlation coefficient showed significant (P < 0.05) positive correlations among prenatal blood metals levels, except for nickel. Although the present study failed to provide strong evidence for the effects of toxic metals on the occurrence of SA at the relatively low-levels, these metals should be avoided in women who plan pregnancy and/or during the early stages of gestation to prevent the chance of adverse effects.
This is a preview of subscription content, access via your institution.
Buy single article
Instant access to the full article PDF.
Tax calculation will be finalised during checkout.
Amadi CN, Igweze ZN, Orisakwe OE. Heavy metals in miscarriages and stillbirths in developing nations. Middle East Fertil Soc J. 2017;22(2):91–100.
Wang Z, Yu X, Geng M, Wang Z, Wang Q, Zeng X. Accumulation of heavy metal in scalp hair of people exposed in Beijing sewage discharge channel sewage irrigation area in Tianjin, China. Environ Sci Pollut Res Int. 2017;24(15):13741–8.
Omeljaniuk WJ, et al. Cadmium and Lead in women who miscarried. Clin Lab. 2018;64(1):59–67.
Johnson MA. High calcium intake blunts pregnancy-induced increases in maternal blood lead. Nutr Rev. 2001;59(5):152–6.
Rothenberg SJ, Kondrashov V, Manalo M, Manton WI, Khan F, Todd AC, et al. Seasonal variation in bone lead contribution to blood lead during pregnancy. Environ Res. 2001;85(3):191–4.
Nishioka E, Yokoyama K, Matsukawa T, Vigeh M, Hirayama S, Ueno T, et al. Evidence that birth weight is decreased by maternal lead levels below 5mug/dl in male newborns. Reprod Toxicol. 2014;47:21–6.
Vigeh M, Yokoyama K, Shinohara A, Afshinrokh M, Yunesian M. Early pregnancy blood lead levels and the risk of premature rupture of the membranes. Reprod Toxicol. 2010;30(3):477–80.
Vigeh M, Yokoyama K, Seyedaghamiri Z, Shinohara A, Matsukawa T, Chiba M, et al. Blood lead at currently acceptable levels may cause preterm labour. Occup Environ Med. 2011;68(3):231–4.
Lead poisoning in pregnant women who used Ayurvedic medications from India--New York City, 2011-2012. MMWR Morb Mortal Wkly Rep. 2012;61(33):641–6.
Hafez AS, Fahim HI, Badawy HA. Socioenvironmental predictors of abortion and stillbirths in an industrial community in Egypt. J Egypt Public Health Assoc. 2001;76(1–2):1–16.
Ikeh-Tawari EP, Anetor JI, Charles-Davies MA. Cadmium level in pregnancy, influence on neonatal birth weight and possible amelioration by some essential trace elements. Toxicol Int. 2013;20(1):108–12.
Henríquez-Hernández LA, Luzardo OP, Boada LD, González-Antuña A, Domínguez-Bencomo AI, Zumbado M, et al. Assessment of 22 inorganic elements in human amniotic fluid: a cross-sectional study conducted in Canary Islands (Spain). Int J Environ Health Res. 2019;29(2):130–9.
Nybo Andersen AM, Wohlfahrt J, Christens P, Olsen J, Melbye M. Maternal age and fetal loss: population based register linkage study. BMJ. 2000;320(7251):1708–12.
Weselak M, Arbuckle TE, Walker MC, Krewski D. The influence of the environment and other exogenous agents on spontaneous abortion risk. J Toxicol Environ Health B Crit Rev. 2008;11(3–4):221–41.
Taskinen HK. Effects of parental occupational exposures on spontaneous abortion and congenital malformation. Scand J Work Environ Health. 1990;16(5):297–314.
Mohammadyan M, Moosazadeh M, Borji A, Khanjani N, Rahimi Moghadam S. Investigation of occupational exposure to lead and its relation with blood lead levels in electrical solderers. Environ Monit Assess. 2019;191(3):126.
Anttila A, Sallmen M. Effects of parental occupational exposure to lead and other metals on spontaneous abortion. J Occup Environ Med. 1995;37(8):915–21.
Hertz-Picciotto I. The evidence that lead increases the risk for spontaneous abortion. Am J Ind Med. 2000;38(3):300–9.
Buck Louis GM, Smarr MM, Sundaram R, Steuerwald AJ, Sapra KJ, Lu Z, et al. Low-level environmental metals and metalloids and incident pregnancy loss. Reprod Toxicol. 2017;69:68–74.
McDermott S, Salzberg DC, Anderson AP, Shaw T, Lead J. Systematic review of chromium and nickel exposure during pregnancy and impact on child outcomes. J Toxicol Environ Health Part A. 2015;78(21–22):1348–68.
Wang R, Zhang L, Chen Y, Zhang S, Zhuang T, Wang L, et al. Elevated non-essential metals and the disordered metabolism of essential metals are associated to abnormal pregnancy with spontaneous abortion. Environ Int. 2020;144:106061.
Rzymski P, Niedzielski P, Poniedziałek B, Tomczyk K, Rzymski P. Identification of toxic metals in human embryonic tissues. Arch Med Sci. 2018;14(2):415–21.
Zeng LX, Yan H, Chen ZJ. Study on the current status and risk factors of spontaneous abortion of women at reproductive age in rural areas of Xianyang district, Shaanxi province. Zhonghua Liu Xing Bing Xue Za Zhi. 2007;28(1):19–23.
Vigeh M, Yokoyama K, Ramezanzadeh F, Dahaghin M, Sakai T, Morita Y, et al. Lead and other trace metals in preeclampsia: a case-control study in Tehran, Iran. Environ Res. 2006;100(2):268–75.
Zhang G, Wang X, Zhang X, Li Q, Xu S, Huang L, et al. Antimony in urine during early pregnancy correlates with increased risk of gestational diabetes mellitus: a prospective cohort study. Environ Int. 2019;123:164–70.
Miah MT, Ayaz FM, Maniruzzaman M, Ahasan MN, Bari S, Mawla SM, et al. Kala azar in Pregnancy. Mymensingh Med J. 2010;19(4):529–32.
Amini H, Schindler C, Hosseini V, Yunesian M, Künzli N. Land use regression models for Alkylbenzenes in a middle eastern megacity: Tehran study of exposure prediction for environmental Health Research (Tehran SEPEHR). Environ Sci Technol. 2017;51(15):8481–90.
Vigeh M, Yokoyama K, Kitamura F, Afshinrokh M, Beygi A, Niroomanesh S. Early pregnancy blood lead and spontaneous abortion. Women Health. 2010;50(8):756–66.
Faikoglu R, et al. Significance of maternal plasma lead level in early pregnancy loss. J Environ Sci Health A Tox Hazard Subst Environ Eng. 2006;41(3):501–6.
Borella P, Picco P, Masellis G. Lead content in abortion material from urban women in early pregnancy. Int Arch Occup Environ Health. 1986;57(2):93–9.
Tabacova S, Balabaeva L. Environmental pollutants in relation to complications of pregnancy. Environ Health Perspect. 1993;101(Suppl 2):27–31.
Bellinger DC. Teratogen update: lead and pregnancy. Birth Defects Res A Clin Mol Teratol. 2005;73(6):409–20.
Borja-Aburto VH, Hertz-Picciotto I, Lopez MR, Farias P, Rios C, Blanco J. Blood lead levels measured prospectively and risk of spontaneous abortion. Am J Epidemiol. 1999;150(6):590–7.
Kim SH, Chun J, Ko KH, Sung TJ. Effect of antenatal azithromycin for Ureaplasma spp. on neonatal outcome at </=30 weeks' gestational age. Pediatr Int. 2019;61(1):58–62.
Zhao R, Wu Y, Zhao F, Lv Y, Huang D, Wei J, et al. The risk of missed abortion associated with the levels of tobacco, heavy metals and phthalate in hair of pregnant woman: a case control study in Chinese women. Medicine (Baltimore). 2017;96(51):e9388.
Chen C, Wang N, Zhai H, Nie X, Sun H, Han B, et al. Associations of blood lead levels with reproductive hormone levels in men and postmenopausal women: results from the SPECT-China study. Sci Rep. 2016;6:37809.
Sokol RZ, Wang S, Wan YJY, Stanczyk FZ, Gentzschein E, Chapin RE. Long-term, low-dose lead exposure alters the gonadotropin-releasing hormone system in the male rat. Environ Health Perspect. 2002;110(9):871–4.
Lee TW, Kim DH, Ryu JY. The effects of exposure to lead, cadmium and mercury on follicle-stimulating hormone levels in men and postmenopausal women: data from the second Korean National Environmental Health Survey (2012-2014). Ann Occup Environ Med. 2019;31:e21.
Gallagher CM, Moonga BS, Kovach JS. Cadmium, follicle-stimulating hormone, and effects on bone in women age 42-60 years, NHANES III. Environ Res. 2010;110(1):105–11.
Wakeel A, Xu M, Gan Y. Chromium-induced reactive oxygen species accumulation by altering the enzymatic antioxidant system and associated cytotoxic, genotoxic, ultrastructural, and photosynthetic changes in plants. Int J Mol Sci. 2020;21(3):728.
Vaziri ND, Khan M. Interplay of reactive oxygen species and nitric oxide in the pathogenesis of experimental lead-induced hypertension. Clin Exp Pharmacol Physiol. 2007;34(9):920–5.
Magnus MC, et al. Role of maternal age and pregnancy history in risk of miscarriage: prospective register based study. BMJ. 2019;364:l869.
de la Rochebrochard E, Thonneau P. Paternal age and maternal age are risk factors for miscarriage; results of a multicentre European study. Hum Reprod. 2002;17(6):1649–56.
Rakhra G, Masih D, Vats A, Vijay A, Ashraf MZ, Singh SN. Study of metal-metal interactions and their biomarkers using an intestinal human cell line. Biol Trace Elem Res. 2020;195(1):95–104.
This research project was financially supported by Institute for Environmental Research, Tehran University of Medical Sciences, Iran by (Grant No. 25759-46-02-94), and Iran National Sciences Foundation (INFS) by (Grant No.93050433) and a Grant-in-Aid for Scientific Research from the Japan Society for the Promotion of Science (Grant No. 15H05288). The authors acknowledge all participants and administrations of hospitals and health care centers for their cooperation.
This research project was financially supported by Institute for Environmental Research, Tehran University of Medical Sciences, Iran by (Grant No. 25759-46-02-94), and Iran National Sciences Foundation (INFS) by (Grant No.93050433) and a Grant-in-Aid for Scientific Research from the Japan Society for the Promotion of Science (Grant No. 15H05288).
Conflict of interest
The authors declare that there are no conflicts of interest in this study.
The TUMS Ethical Committees reviewed and approved the study design, procedures, and informed consent format (permission No:IR.TUMS.REC.1394.1180).
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
About this article
Cite this article
Vigeh, M., Yunesian, M., Matsukawa, T. et al. Prenatal blood levels of some toxic metals and the risk of spontaneous abortion. J Environ Health Sci Engineer (2021). https://doi.org/10.1007/s40201-020-00608-3
- Toxic metal
- Spontaneous abortion