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Maternal Cadmium Levels During Pregnancy and the Relationship with Preeclampsia and Fetal Biometric Parameters

  • Fan Wang
  • Fengyun Fan
  • Lianyun Wang
  • Wen Ye
  • Qiong Zhang
  • Shuangshuang Xie
Article

Abstract

Preeclampsia, which is caused by multiple factors, still remains one of the most serious complications of pregnancy. This study was designed to determine cadmium levels in women with preeclampsia compared to those of normotensive women. In this case-control study, maternal blood, umbilical cord blood, and placental cadmium levels were measured by an inductively coupled plasma mass spectrometry system in 51 women presenting consecutively with preeclampsia and 51 normotensive pregnant women. Groups were matched for maternal age, parity, and gestational age. Birth outcomes were recorded, such as gestational age at delivery, birth weight, and Apgar score. Median (interquartile range [IQR]) blood cadmium concentration was 1.21 μg/L (0.76–1.84 μg/L) and 1.09 μg/L (0.72–1.31 μg/L) in women with preeclampsia and normotensive, respectively; values for placental cadmium levels of women with preeclampsia and normotensive were 3.61 μg/kg (2.19–4.37 μg/kg) and 4.28 μg/kg (3.06–5.71 μg/kg), respectively. We observed a statistically significant increase in blood and placental cadmium levels in women with preeclampsia compared to healthy pregnant women. After adjusting for pre-pregnancy body mass index, maternal age, parity, gestational age at sample collection, and maternal calcium and magnesium levels, the odds ratio of having preeclampsia in the high tertile was markedly increased (odds ratio, 7.83 [95% CI, 1.64–37.26]) compared with the low tertile. Interestingly, there was no difference in the cadmium level in umbilical cord blood between the groups. Within the preeclamptic group, higher cadmium status was significantly associated with decreased birth weight. Our study suggested that elevated cadmium level in the maternal circulation could potentially increase the risk of preeclampsia. The results also demonstrate that higher cadmium status may contribute to fetal growth restriction in preeclamptic patients.

Keywords

Cadmium Preeclampsia Pregnancy Fetal growth restriction 

Notes

Funding Information

This study was supported by the National Natural Science Foundation of China (No. 81501280), the Natural Science Foundation of Zhejiang Province (No. LY15H040012), and the Wenzhou Science and Technology Bureau Foundation (No. Y20150048), China.

Compliance with Ethical Standards

The study was approved by the Ethics Committee of The Second Affiliated Hospital of Wenzhou Medical University and written consent was obtained from all participants.

Conflict of Interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    Roberts JM, August PA, Bakris G, Barton JR, Bernstein IM, Druzin M, Gaiser RR, Granger JP, Jeyabalan A, Johnson DD, Karumanchi S, Lindheimer M, Owens MY, Saade GR, Sibai BM, Spong CY, Tsigas E, Joseph GF, O’Reilly N, Politzer A, Son S, Ngaiza K (2013) Hypertension in pregnancy. Report of the American College of Obstetricians and Gynecologists’ Task Force on Hypertension in Pregnancy. Obstet Gynecol 122(5):1122–1131.  https://doi.org/10.1097/01.aog.0000437382.03963.88 CrossRefGoogle Scholar
  2. 2.
    Williams PJ, Broughton Pipkin F (2011) The genetics of pre-eclampsia and other hypertensive disorders of pregnancy. Best Pract Res Clin Obstet Gynaecol 25(4):405–417.  https://doi.org/10.1016/j.bpobgyn.2011.02.007 CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Nilsson E, Salonen Ros H, Cnattingius S, Lichtenstein P (2004) The importance of genetic and environmental effects for pre-eclampsia and gestational hypertension: a family study. BJOG Int J Obstet Gynaecol 111(3):200–206.  https://doi.org/10.1111/j.1471-0528.2004.00042.x CrossRefGoogle Scholar
  4. 4.
    Laresgoiti-Servitje E, Gomez-Lopez N, Olson DM (2010) An immunological insight into the origins of pre-eclampsia. Hum Reprod Update 16(5):510–524.  https://doi.org/10.1093/humupd/dmq007 CrossRefPubMedGoogle Scholar
  5. 5.
    Faroon O, Ashizawa A, Wright S, Tucker P, Jenkins K, Ingerman L, Rudisill C (2012) Agency for Toxic Substances and Disease Registry (ATSDR) Toxicological Profiles. In:Toxicological Profile for Cadmium. Agency for Toxic Substances and Disease Registry (US), Atlanta (GA)Google Scholar
  6. 6.
    Li Q, Hsia J, Yang G (2011) Prevalence of smoking in China in 2010. N Engl J Med 364(25):2469–2470.  https://doi.org/10.1056/NEJMc1102459 CrossRefPubMedGoogle Scholar
  7. 7.
    Wang L, Cui X, Cheng H, Chen F, Wang J, Zhao X, Lin C, Pu X (2015) A review of soil cadmium contamination in China including a health risk assessment. Environ Sci Pollut Res Int 22(21):16441–16452.  https://doi.org/10.1007/s11356-015-5273-1 CrossRefPubMedGoogle Scholar
  8. 8.
    Thompson J, Bannigan J (2008) Cadmium: toxic effects on the reproductive system and the embryo. Reprod Toxicol (Elmsford, NY) 25(3):304–315.  https://doi.org/10.1016/j.reprotox.2008.02.001 CrossRefGoogle Scholar
  9. 9.
    Kantola M, Purkunen R, Kröger P, Tooming A, Juravskaja J, Pasanen M, Saarikoski S, Vartiainen T (2000) Accumulation of cadmium, zinc, and copper in maternal blood and developmental placental tissue: differences between Finland, Estonia, and St. Petersburg. Environ Res 83(1):54–66.  https://doi.org/10.1006/enrs.1999.4043 CrossRefPubMedGoogle Scholar
  10. 10.
    Kukongviriyapan U, Apaijit K, Kukongviriyapan V (2016) Oxidative stress and cardiovascular dysfunction associated with cadmium exposure: beneficial effects of curcumin and tetrahydrocurcumin. Tohoku J Exp Med 239(1):25–38.  https://doi.org/10.1620/tjem.239.25 CrossRefPubMedGoogle Scholar
  11. 11.
    Houston MC (2007) The role of mercury and cadmium heavy metals in vascular disease, hypertension, coronary heart disease, and myocardial infarction. Altern Ther Health Med 13(2):S128–S133PubMedGoogle Scholar
  12. 12.
    Chisolm J, Handorf C (1987) Increased absorption of and sensitivity to cadmium during late pregnancy: is there a relationship between markedly decreased maternal cadmium binding protein (metallothionein) and pregnancy-induced hypertension? Med Hypotheses 24(4):347–351CrossRefPubMedGoogle Scholar
  13. 13.
    Wang H, Wang Y, Bo Q-L, Ji Y-L, Liu L, Hu Y-F, Chen Y-H, Zhang J, Zhao L-L, Xu D-X (2016) Maternal cadmium exposure reduces placental zinc transport and induces fetal growth restriction in mice. Reprod Toxicol 63:174–182.  https://doi.org/10.1016/j.reprotox.2016.06.010 CrossRefPubMedGoogle Scholar
  14. 14.
    Ahsan T, Banu S, Nahar Q, Ahsan M, Khan MNI, Islam SN (2013) Serum trace elements levels in preeclampsia and eclampsia: correlation with the pregnancy disorder. Biol Trace Elem Res 152(3):327–332.  https://doi.org/10.1007/s12011-013-9637-4 CrossRefPubMedGoogle Scholar
  15. 15.
    (2013) Hypertension in pregnancy. Report of the American College of Obstetricians and Gynecologists’ Task Force on Hypertension in Pregnancy. Obstet Gynecol 122(5):1122–1131.  https://doi.org/10.1097/01.aog.0000437382.03963.88
  16. 16.
    Zhu L, Zhang R, Zhang S, Shi W, Yan W, Wang X, Lyu Q, Liu L, Zhou Q, Qiu Q (2015) Chinese neonatal birth weight curve for different gestational age. Chin J Pediatr 53(2):97–103Google Scholar
  17. 17.
    Sakamoto M, Yasutake A, Domingo JL, Chan HM, Kubota M, Murata K (2013) Relationships between trace element concentrations in chorionic tissue of placenta and umbilical cord tissue: potential use as indicators for prenatal exposure. Environ Int 60:106–111.  https://doi.org/10.1016/j.envint.2013.08.007 CrossRefPubMedGoogle Scholar
  18. 18.
    Johnston JE, Valentiner E, Maxson P, Miranda ML, Fry RC (2014) Maternal cadmium levels during pregnancy associated with lower birth weight in infants in a North Carolina cohort. PLoS One 9(10):e109661.  https://doi.org/10.1371/journal.pone.0109661 CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Abdelouahab N, Huel G, Suvorov A, Foliguet B, Goua V, Debotte G, Sahuquillo J, Charles M-A, Takser L (2010) Monoamine oxidase activity in placenta in relation to manganese, cadmium, lead, and mercury at delivery. Neurotoxicology and teratology 32(2):256–261.  https://doi.org/10.1016/j.ntt.2009.08.010 CrossRefPubMedGoogle Scholar
  20. 20.
    Kippler M, Hoque AW, Raqib R, Öhrvik H, Ekström E-C, Vahter M (2010) Accumulation of cadmium in human placenta interacts with the transport of micronutrients to the fetus. Toxicology letters 192(2):162–168.  https://doi.org/10.1016/j.toxlet.2009.10.018 CrossRefPubMedGoogle Scholar
  21. 21.
    Lin C-M, Doyle P, Wang D, Hwang Y-H, Chen P-C (2011) Does prenatal cadmium exposure affect fetal and child growth? Occupational and environmental medicine 68(9):641–646.  https://doi.org/10.1136/oem.2010.059758 CrossRefPubMedGoogle Scholar
  22. 22.
    Al-Saleh I, Shinwari N, Mashhour A, Mohamed GED, Rabah A (2011) Heavy metals (lead, cadmium and mercury) in maternal, cord blood and placenta of healthy women. International journal of hygiene and environmental health 214(2):79–101.  https://doi.org/10.1016/j.ijheh.2010.10.001 CrossRefPubMedGoogle Scholar
  23. 23.
    García-Esquinas E, Pérez-Gómez B, Fernández-Navarro P, Fernández MA, De Paz C, Pérez-Meixeira AM, Gil E, Iriso A, Sanz JC, Astray J (2013) Lead, mercury and cadmium in umbilical cord blood and its association with parental epidemiological variables and birth factors. BMC public health 13(1):841.  https://doi.org/10.1186/1471-2458-13-841 CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Sun H, Chen W, Wang D, Jin Y, Chen X, Xu Y (2014) The effects of prenatal exposure to low-level cadmium, lead and selenium on birth outcomes. Chemosphere 108:33–39.  https://doi.org/10.1016/j.chemosphere.2014.02.080 CrossRefPubMedGoogle Scholar
  25. 25.
    Chen Z, Myers R, Wei T, Bind E, Kassim P, Wang G, Ji Y, Hong X, Caruso D, Bartell T (2014) Placental transfer and concentrations of cadmium, mercury, lead, and selenium in mothers, newborns, and young children. Journal of Exposure Science and Environmental Epidemiology 24(5):537–544.  https://doi.org/10.1038/jes.2014.26 CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Röllin HB, Kootbodien T, Channa K, Odland JØ (2015) Prenatal exposure to cadmium, placental permeability and birth outcomes in coastal populations of South Africa. PloS one 10(11):e0142455.  https://doi.org/10.1371/journal.pone.0142455 CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Fagerstedt S, Kippler M, Scheynius A, Gutzeit C, Mie A, Alm J, Vahter M (2015) Anthroposophic lifestyle influences the concentration of metals in placenta and cord blood. Environmental research 136:88–96.  https://doi.org/10.1016/j.envres.2014.08.044 CrossRefPubMedGoogle Scholar
  28. 28.
    Kim Y-M, Chung J-Y, An HS, Park SY, Kim B-G, Bae JW, Han M, Cho YJ, Hong Y-S (2015) Biomonitoring of lead, cadmium, total mercury, and methylmercury levels in maternal blood and in umbilical cord blood at birth in South Korea. International journal of environmental research and public health 12(10):13482–13493.  https://doi.org/10.3390/ijerph121013482 CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Olszowski T, Baranowska-Bosiacka I, Rębacz-Maron E, Gutowska I, Jamioł D, Prokopowicz A, Goschorska M, Chlubek D (2016) Cadmium Concentration in Mother’s Blood, Milk, and Newborn’s Blood and Its Correlation with Fatty Acids, Anthropometric Characteristics, and Mother’s Smoking Status. Biological trace element research 174(1):8–20.  https://doi.org/10.1007/s12011-016-0683-6 CrossRefPubMedGoogle Scholar
  30. 30.
    King KE, Darrah TH, Money E, Meentemeyer R, Maguire RL, Nye MD, Michener L, Murtha AP, Jirtle R, Murphy SK (2015) Geographic clustering of elevated blood heavy metal levels in pregnant women. BMC public health 15(1):1035.  https://doi.org/10.1186/s12889-015-2379-9 CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Fu J, Zhou Q, Liu J, Liu W, Wang T, Zhang Q, Jiang G (2008) High levels of heavy metals in rice (Oryzasativa L.) from a typical E-waste recycling area in southeast China and its potential risk to human health. Chemosphere 71(7):1269–1275.  https://doi.org/10.1016/j.chemosphere.2007.11.065 CrossRefPubMedGoogle Scholar
  32. 32.
    Morgan H, Sherlock J (1984) Cadmium intake and cadmium in the human kidney. Food Additives & Contaminants 1(1):45–51.  https://doi.org/10.1080/02652038409385822 CrossRefGoogle Scholar
  33. 33.
    Occupational Safety and Health Administration DoL (2003) Occupational safety and health standards: toxic and hazardous substances: cadmium. Code of Federal Regulations 29:135–229 CFR 1910.1027Google Scholar
  34. 34.
    Schulz C, Angerer J, Ewers U, Kolossa-Gehring M (2007) The German human biomonitoring commission. International journal of hygiene and environmental health 210(3):373–382.  https://doi.org/10.1016/j.ijheh.2007.01.035 CrossRefPubMedGoogle Scholar
  35. 35.
    Laine JE, Ray P, Bodnar W, Cable PH, Boggess K, Offenbacher S, Fry RC (2015) Placental Cadmium Levels Are Associated with Increased Preeclampsia Risk. PloS one 10(9):e0139341.  https://doi.org/10.1371/journal.pone.0139341 CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Ebrahim K, Ashtarinezhad A (2015) The association of amniotic fluid cadmium levels with the risk of preeclampsia, prematurity and low birth weight. Iranian Journal of Neonatology IJN 6(2):1–6.  https://doi.org/10.22038/ijn.2015.4482 Google Scholar
  37. 37.
    Kosanovic M, Jokanovic M, Jevremovic M, Dobric S, Bokonjic D (2002) Maternal and fetal cadmium and selenium status in normotensive and hypertensive pregnancy. Biological trace element research 89(2):97–103.  https://doi.org/10.1385/BTER:89:2:97 CrossRefPubMedGoogle Scholar
  38. 38.
    Kolusari A, Kurdoglu M, Yildizhan R, Adali E, Edirne T, Cebi A, Demir H, Yoruk I (2008) Catalase activity, serum trace element and heavy metal concentrations, and vitamin A, D and E levels in pre-eclampsia. Journal of International Medical Research 36(6):1335–1341.  https://doi.org/10.1177/147323000803600622 CrossRefPubMedGoogle Scholar
  39. 39.
    Vigeh M, Yokoyama K, Ramezanzadeh F, Dahaghin M, Sakai T, Morita Y, Kitamura F, Sato H, Kobayashi Y (2006) Lead and other trace metals in preeclampsia: a case-control study in Tehran, Iran. Environmental research 100(2):268–275.  https://doi.org/10.1016/j.envres.2005.05.005 CrossRefPubMedGoogle Scholar
  40. 40.
    Osorio-Yanez C, Gelaye B, Miller RS, Enquobahrie DA, Baccarelli AA, Qiu C, Williams MA (2016) Associations of Maternal Urinary Cadmium with Trimester-Specific Blood Pressure in Pregnancy: Role of Dietary Intake of Micronutrients. Biological trace element research 174(1):71–81.  https://doi.org/10.1007/s12011-016-0705-4 CrossRefPubMedGoogle Scholar
  41. 41.
    Kosanovic M, Jokanovic M (2007) The association of exposure to cadmium through cigarette smoke with pregnancy-induced hypertension in a selenium deficient population. Environmental toxicology and pharmacology 24(1):72–78.  https://doi.org/10.1016/j.etap.2007.02.004 CrossRefPubMedGoogle Scholar
  42. 42.
    Wang F, Zhang Q, Zhang X, Luo S, Ye D, Guo Y, Chen S, Huang Y (2014) Preeclampsia induced by cadmium in rats is related to abnormal local glucocorticoid synthesis in placenta. Reproductive Biology and Endocrinology 12(1):77.  https://doi.org/10.1186/1477-7827-12-77 CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Zhang Q, Huang Y, Zhang K, Huang Y, Yan Y, Wang F, Wu J, Wang X, Xu Z, Chen Y (2016) Cadmium-induced immune abnormality is a key pathogenic event in human and rat models of preeclampsia. Environmental Pollution 218:770–782.  https://doi.org/10.1016/j.envpol.2016.07.073 CrossRefPubMedGoogle Scholar
  44. 44.
    Kippler M, Tofail F, Gardner R, Rahman A, Hamadani JD, Bottai M, Vahter M (2012) Maternal cadmium exposure during pregnancy and size at birth: a prospective cohort study. Environmental health perspectives 120(2):284–289.  https://doi.org/10.1289/ehp.1103711 CrossRefPubMedGoogle Scholar
  45. 45.
    McTernan C, Draper N, Nicholson H, Chalder S, Driver P, Hewison M, Kilby M, Stewart P (2001) Reduced placental 11β-hydroxysteroid dehydrogenase type 2 mRNA levels in human pregnancies complicated by intrauterine growth restriction: an analysis of possible mechanisms. The Journal of Clinical Endocrinology & Metabolism 86(10):4979–4983.  https://doi.org/10.1210/jcem.86.10.7893 Google Scholar
  46. 46.
    Ikeh-Tawari EP, Anetor JI, Charles-Davies M (2013) Cadmium level in pregnancy, influence on neonatal birth weight and possible amelioration by some essential trace elements. Toxicology international 20(1):108–112.  https://doi.org/10.4103/0971-6580.111558 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Fan Wang
    • 1
  • Fengyun Fan
    • 1
  • Lianyun Wang
    • 1
  • Wen Ye
    • 1
  • Qiong Zhang
    • 1
  • Shuangshuang Xie
    • 1
  1. 1.Department of Gynecology and ObstetricsThe Second Affiliated Hospital and Yuying Children’s Hospital of Wenzhou Medical UniversityWenzhouChina

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