Skip to main content
Top
Published in: Environmental Health and Preventive Medicine 1/2019

Open Access 01-12-2019 | Research article

Associations between metal concentrations in whole blood and placenta previa and placenta accreta: the Japan Environment and Children’s Study (JECS)

Authors: Mayumi Tsuji, Eiji Shibata, David J. Askew, Seiichi Morokuma, Yukiyo Aiko, Ayako Senju, Shunsuke Araki, Masafumi Sanefuji, Yasuhiro Ishihara, Rie Tanaka, Koichi Kusuhara, Toshihiro Kawamoto, Japan Environment and Children’s Study Group

Published in: Environmental Health and Preventive Medicine | Issue 1/2019

Login to get access

Abstract

Background

Placenta previa and placenta accreta associate with high morbidity and mortality for both mothers and fetus. Metal exposure may have relationships with placenta previa and placenta accreta. This study analyzed the associations between maternal metal (cadmium [Cd], lead [Pb], mercury [Hg], selenium [Se], and manganese [Mn]) concentrations and placenta previa and placenta accreta.

Methods

We recruited 17,414 women with singleton pregnancies. Data from a self-administered questionnaire regarding the first trimester and medical records after delivery were analyzed. Maternal blood samples were collected to measure metal concentrations. The subjects were classified into four quartiles (Q1, Q2, Q3, and Q4) according to metal concentrations.

Results

The odds ratio for placenta previa was significantly higher among subjects with Q4 Cd than those with Q1 Cd. The odds ratio for placenta previa was significantly higher for subjects with Q2 Pb than those with Q1 Pb.

Conclusion

Participants with placenta previa had higher Cd concentrations. However, this study was cross-sectional and lacked important information related to Cd concentration, such as detailed smoking habits and sources of Cd intake. In addition, the subjects in this study comprised ordinary pregnant Japanese women, and it was impossible to observe the relationship between a wide range of Cd exposure and placenta previa. Therefore, epidemiological and experimental studies are warranted to verify the relationship between Cd exposure and pregnancy abnormalities.
Appendix
Available only for authorised users
Literature
1.
go back to reference Lee HJ, Lee YJ, Ahn EH, Kim HC, Jung SH, Chang SW, et al. Risk factors for massive postpartum bleeding in pregnancies in which incomplete placenta previa are located on the posterior uterine wall. Obstet Gynecol Sci. 2017;60(6):520–6.PubMedCentralCrossRefPubMed Lee HJ, Lee YJ, Ahn EH, Kim HC, Jung SH, Chang SW, et al. Risk factors for massive postpartum bleeding in pregnancies in which incomplete placenta previa are located on the posterior uterine wall. Obstet Gynecol Sci. 2017;60(6):520–6.PubMedCentralCrossRefPubMed
2.
go back to reference Comstock CH. Antenatal diagnosis of placenta accreta: a review. Ultrasound Obstet Gynecol. 2005;26(1):89–96.CrossRefPubMed Comstock CH. Antenatal diagnosis of placenta accreta: a review. Ultrasound Obstet Gynecol. 2005;26(1):89–96.CrossRefPubMed
3.
go back to reference Wehrum MJ, Buhimschi IA, Salafia C, Thung S, Bahtiyar MO, Werner EF, et al. Accreta complicating complete placenta previa is characterized by reduced systemic levels of vascular endothelial growth factor and by epithelial-to-mesenchymal transition of the invasive trophoblast. Am J Obstet Gynecol. 2011;204(5):411.e1–e11.CrossRef Wehrum MJ, Buhimschi IA, Salafia C, Thung S, Bahtiyar MO, Werner EF, et al. Accreta complicating complete placenta previa is characterized by reduced systemic levels of vascular endothelial growth factor and by epithelial-to-mesenchymal transition of the invasive trophoblast. Am J Obstet Gynecol. 2011;204(5):411.e1–e11.CrossRef
4.
go back to reference Sumigama S, Itakura A, Ota T, Okada M, Kotani T, Hayakawa H, et al. Placenta previa increta/percreta in Japan: a retrospective study of ultrasound findings, management and clinical course. J Obstet Gynaecol Res. 2007;33(5):606–11.CrossRefPubMed Sumigama S, Itakura A, Ota T, Okada M, Kotani T, Hayakawa H, et al. Placenta previa increta/percreta in Japan: a retrospective study of ultrasound findings, management and clinical course. J Obstet Gynaecol Res. 2007;33(5):606–11.CrossRefPubMed
5.
go back to reference Miller DA, Chollet JA, Goodwin TM. Clinical risk factors for placenta previa-placenta accreta. Am J Obstet Gynecol. 1997;177(1):210–4.CrossRefPubMed Miller DA, Chollet JA, Goodwin TM. Clinical risk factors for placenta previa-placenta accreta. Am J Obstet Gynecol. 1997;177(1):210–4.CrossRefPubMed
6.
go back to reference Okai T, Saito S, Kawarabayashi T, Takeda S, Hiramatsu Y, Minakami H. Perinatal committee. Acta Obstet Gynaecol Jpn. 2009;61(7):1543–67. Okai T, Saito S, Kawarabayashi T, Takeda S, Hiramatsu Y, Minakami H. Perinatal committee. Acta Obstet Gynaecol Jpn. 2009;61(7):1543–67.
7.
go back to reference Usta IM, Hobeika EM, Musa AA, Gabriel GE, Nassar AH. Placenta previa-accreta: risk factors and complications. Am J Obstet Gynecol. 2005;193(3 Pt 2):1045–9.CrossRefPubMed Usta IM, Hobeika EM, Musa AA, Gabriel GE, Nassar AH. Placenta previa-accreta: risk factors and complications. Am J Obstet Gynecol. 2005;193(3 Pt 2):1045–9.CrossRefPubMed
8.
go back to reference Ogawa K, Urayama KY, Tanigaki S, Sago H, Sato S, Saito S, et al. Association between very advanced maternal age and adverse pregnancy outcomes: a cross sectional Japanese study. BMC Pregnancy Childbirth. 2017;17(1):349.PubMedCentralCrossRefPubMed Ogawa K, Urayama KY, Tanigaki S, Sago H, Sato S, Saito S, et al. Association between very advanced maternal age and adverse pregnancy outcomes: a cross sectional Japanese study. BMC Pregnancy Childbirth. 2017;17(1):349.PubMedCentralCrossRefPubMed
9.
go back to reference Kimber SJ, Spanswick C. Blastocyst implantation: the adhesion cascade. Semin Cell Dev Biol. 2000;11(2):77–92.CrossRefPubMed Kimber SJ, Spanswick C. Blastocyst implantation: the adhesion cascade. Semin Cell Dev Biol. 2000;11(2):77–92.CrossRefPubMed
10.
go back to reference Uchida H, Maruyama T, Masuda H, Uchida S, Miki F, Hihara H, et al. How to create an embryo penetration route. Am J Reprod Immunol. 2016;75(3):326–32.CrossRefPubMed Uchida H, Maruyama T, Masuda H, Uchida S, Miki F, Hihara H, et al. How to create an embryo penetration route. Am J Reprod Immunol. 2016;75(3):326–32.CrossRefPubMed
11.
go back to reference Imakawa K, Bai R, Fujiwara H, Ideta A, Aoyagi Y, Kusama K. Continuous model of conceptus implantation to the maternal endometrium. J Endocrinol. 2017;233(1):R53–r65.CrossRefPubMed Imakawa K, Bai R, Fujiwara H, Ideta A, Aoyagi Y, Kusama K. Continuous model of conceptus implantation to the maternal endometrium. J Endocrinol. 2017;233(1):R53–r65.CrossRefPubMed
12.
go back to reference Marshall NE, Fu R, Guise JM. Impact of multiple cesarean deliveries on maternal morbidity: a systematic review. Am J Obstet Gynecol. 2011;205(3):262.e1–8.CrossRef Marshall NE, Fu R, Guise JM. Impact of multiple cesarean deliveries on maternal morbidity: a systematic review. Am J Obstet Gynecol. 2011;205(3):262.e1–8.CrossRef
13.
go back to reference Faiz AS, Ananth CV. Etiology and risk factors for placenta previa: an overview and meta-analysis of observational studies. J Matern Fetal Neonatal Med. 2003;13(3):175–90.CrossRefPubMed Faiz AS, Ananth CV. Etiology and risk factors for placenta previa: an overview and meta-analysis of observational studies. J Matern Fetal Neonatal Med. 2003;13(3):175–90.CrossRefPubMed
14.
go back to reference Shobeiri F, Jenabi E. Smoking and placenta previa: a meta-analysis. J Matern Fetal Neonatal Med. 2017;30(24):2985–90.CrossRefPubMed Shobeiri F, Jenabi E. Smoking and placenta previa: a meta-analysis. J Matern Fetal Neonatal Med. 2017;30(24):2985–90.CrossRefPubMed
15.
go back to reference Michikawa T, Morokuma S, Yamazaki S, Fukushima K, Kato K, Nitta H. Exposure to air pollutants during the early weeks of pregnancy, and placenta praevia and placenta accreta in the western part of Japan. Environ Int. 2016;92-93:464–70.CrossRefPubMed Michikawa T, Morokuma S, Yamazaki S, Fukushima K, Kato K, Nitta H. Exposure to air pollutants during the early weeks of pregnancy, and placenta praevia and placenta accreta in the western part of Japan. Environ Int. 2016;92-93:464–70.CrossRefPubMed
16.
go back to reference Prins JR, Hylkema MN, Erwich JJ, Huitema S, Dekkema GJ, Dijkstra FE, et al. Smoking during pregnancy influences the maternal immune response in mice and humans. Am J Obstet Gynecol. 2012;207(1):76.e1–14.CrossRef Prins JR, Hylkema MN, Erwich JJ, Huitema S, Dekkema GJ, Dijkstra FE, et al. Smoking during pregnancy influences the maternal immune response in mice and humans. Am J Obstet Gynecol. 2012;207(1):76.e1–14.CrossRef
17.
go back to reference Simhan HN, Caritis SN, Hillier SL, Krohn MA. Cervical anti-inflammatory cytokine concentrations among first-trimester pregnant smokers. Am J Obstet Gynecol. 2005;193(6):1999–2003.CrossRefPubMed Simhan HN, Caritis SN, Hillier SL, Krohn MA. Cervical anti-inflammatory cytokine concentrations among first-trimester pregnant smokers. Am J Obstet Gynecol. 2005;193(6):1999–2003.CrossRefPubMed
18.
go back to reference Sheldon IM, Owens SE, Turner ML. Innate immunity and the sensing of infection, damage and danger in the female genital tract. J Reprod Immunol. 2017;119:67–73.CrossRefPubMed Sheldon IM, Owens SE, Turner ML. Innate immunity and the sensing of infection, damage and danger in the female genital tract. J Reprod Immunol. 2017;119:67–73.CrossRefPubMed
19.
go back to reference Chen X, Man GCW, Liu Y, Wu F, Huang J, Li TC, et al. Physiological and pathological angiogenesis in endometrium at the time of embryo implantation. Am J Reprod Immunol. 2017;78:e12693.CrossRef Chen X, Man GCW, Liu Y, Wu F, Huang J, Li TC, et al. Physiological and pathological angiogenesis in endometrium at the time of embryo implantation. Am J Reprod Immunol. 2017;78:e12693.CrossRef
20.
go back to reference Matsumoto H, Sato E. Uterine angiogenesis in mice uterine angiogenesis during implantation and decidualization in mice. Reprod Med Biol. 2006;5:81–6.PubMedCentralPubMed Matsumoto H, Sato E. Uterine angiogenesis in mice uterine angiogenesis during implantation and decidualization in mice. Reprod Med Biol. 2006;5:81–6.PubMedCentralPubMed
21.
go back to reference Chen ZY, Yao Y. A synergistic negative effect of gestational smoke-exposure and small litter size on rat placental efficiency, vascularisation and angiogenic factors mRNA expression. PLoS One. 2017;12(7):e0181348.PubMedCentralCrossRefPubMed Chen ZY, Yao Y. A synergistic negative effect of gestational smoke-exposure and small litter size on rat placental efficiency, vascularisation and angiogenic factors mRNA expression. PLoS One. 2017;12(7):e0181348.PubMedCentralCrossRefPubMed
22.
go back to reference Rogers JM. Tobacco and pregnancy: overview of exposures and effects. Birth Defects Res C Embryo Today. 2008;84(1):1–15.CrossRefPubMed Rogers JM. Tobacco and pregnancy: overview of exposures and effects. Birth Defects Res C Embryo Today. 2008;84(1):1–15.CrossRefPubMed
23.
go back to reference Rzymski P, Niedzielski P, Rzymski P, Tomczyk K, Kozak L, Poniedzialek B. Metal accumulation in the human uterus varies by pathology and smoking status. Fertil Steril. 2016;105(6):1511–8.e3.CrossRefPubMed Rzymski P, Niedzielski P, Rzymski P, Tomczyk K, Kozak L, Poniedzialek B. Metal accumulation in the human uterus varies by pathology and smoking status. Fertil Steril. 2016;105(6):1511–8.e3.CrossRefPubMed
24.
go back to reference Rzymski P, Tomczyk K, Rzymski P, Poniedzialek B, Opala T, Wilczak M. Impact of heavy metals on the female reproductive system. Ann Agric Environ Med. 2015;22(2):259–64.CrossRefPubMed Rzymski P, Tomczyk K, Rzymski P, Poniedzialek B, Opala T, Wilczak M. Impact of heavy metals on the female reproductive system. Ann Agric Environ Med. 2015;22(2):259–64.CrossRefPubMed
25.
go back to reference Helmestam M, Stavreus-Evers A, Olovsson M. Cadmium chloride alters mRNA levels of angiogenesis related genes in primary human endometrial endothelial cells grown in vitro. Reprod Toxicol. 2010;30(3):370–6.CrossRefPubMed Helmestam M, Stavreus-Evers A, Olovsson M. Cadmium chloride alters mRNA levels of angiogenesis related genes in primary human endometrial endothelial cells grown in vitro. Reprod Toxicol. 2010;30(3):370–6.CrossRefPubMed
26.
go back to reference Saghiri MA, Orangi J, Asatourian A, Sorenson CM, Sheibani N. Functional role of inorganic trace elements in angiogenesis part III: (Ti, Li, Ce, As, Hg, Va, Nb and Pb). Crit Rev Oncol Hematol. 2016;98:290–301.CrossRefPubMed Saghiri MA, Orangi J, Asatourian A, Sorenson CM, Sheibani N. Functional role of inorganic trace elements in angiogenesis part III: (Ti, Li, Ce, As, Hg, Va, Nb and Pb). Crit Rev Oncol Hematol. 2016;98:290–301.CrossRefPubMed
27.
go back to reference Mamon MAC, Ramos GB. Maternal selenium-supplementation at various stages of periconception period: influence on murine blastocyst morphology and implantation status. J Anim Sci Technol. 2017;59:7.PubMedCentralCrossRefPubMed Mamon MAC, Ramos GB. Maternal selenium-supplementation at various stages of periconception period: influence on murine blastocyst morphology and implantation status. J Anim Sci Technol. 2017;59:7.PubMedCentralCrossRefPubMed
28.
go back to reference Anchordoquy JP, Anchordoquy JM, Sirini MA, Testa JA, Peral-Garcia P, Furnus CC. The importance of manganese in the cytoplasmic maturation of cattle oocytes: blastocyst production improvement regardless of cumulus cells presence during in vitro maturation. Zygote. 2016;24(1):139–48.CrossRefPubMed Anchordoquy JP, Anchordoquy JM, Sirini MA, Testa JA, Peral-Garcia P, Furnus CC. The importance of manganese in the cytoplasmic maturation of cattle oocytes: blastocyst production improvement regardless of cumulus cells presence during in vitro maturation. Zygote. 2016;24(1):139–48.CrossRefPubMed
29.
go back to reference Church SL, Farmer DR, Nelson DM. Induction of manganese superoxide dismutase in cultured human trophoblast during in vitro differentiation. Dev Biol. 1992;149(1):177–84.CrossRefPubMed Church SL, Farmer DR, Nelson DM. Induction of manganese superoxide dismutase in cultured human trophoblast during in vitro differentiation. Dev Biol. 1992;149(1):177–84.CrossRefPubMed
30.
go back to reference Kawamoto T, Nitta H, Murata K, Toda E, Tsukamoto N, Hasegawa M, et al. Rationale and study design of the Japan environment and children’s study (JECS). BMC Public Health. 2014;14:25.PubMedCentralCrossRefPubMed Kawamoto T, Nitta H, Murata K, Toda E, Tsukamoto N, Hasegawa M, et al. Rationale and study design of the Japan environment and children’s study (JECS). BMC Public Health. 2014;14:25.PubMedCentralCrossRefPubMed
31.
go back to reference Michikawa T, Nitta H, Nakayama SF, Ono M, Yonemoto J, Tamura K, et al. The Japan Environment and Children’s Study (JECS): a preliminary report on selected characteristics of approximately 10 000 pregnant women recruited during the first year of the study. J Epidemiol. 2015;25(6):452–8.CrossRefPubMed Michikawa T, Nitta H, Nakayama SF, Ono M, Yonemoto J, Tamura K, et al. The Japan Environment and Children’s Study (JECS): a preliminary report on selected characteristics of approximately 10 000 pregnant women recruited during the first year of the study. J Epidemiol. 2015;25(6):452–8.CrossRefPubMed
32.
go back to reference Michikawa T, Nitta H, Nakayama SF, Yamazaki S, Isobe T, Tamura K, et al. Baseline profile of participants in the Japan environment and Children's study (JECS). J Epidemiol. 2018;28(2):99–104.PubMedCentralCrossRefPubMed Michikawa T, Nitta H, Nakayama SF, Yamazaki S, Isobe T, Tamura K, et al. Baseline profile of participants in the Japan environment and Children's study (JECS). J Epidemiol. 2018;28(2):99–104.PubMedCentralCrossRefPubMed
33.
go back to reference Tsuji M, Shibata E, Morokuma S, Tanaka R, Senju A, Araki S, et al. The association between whole blood concentrations of heavy metals in pregnant women and premature births: the Japan Environment and Children’s Study (JECS). Environ Res. 2018;166:562–9.CrossRefPubMed Tsuji M, Shibata E, Morokuma S, Tanaka R, Senju A, Araki S, et al. The association between whole blood concentrations of heavy metals in pregnant women and premature births: the Japan Environment and Children’s Study (JECS). Environ Res. 2018;166:562–9.CrossRefPubMed
34.
go back to reference Currie LA. Detection and quantification limits: origins and historical overview. Anal Chim Acta. 1999;391:127–34.CrossRef Currie LA. Detection and quantification limits: origins and historical overview. Anal Chim Acta. 1999;391:127–34.CrossRef
35.
go back to reference Hubinont C, Mhallem M, Baldin P, Debieve F, Bernard P, Jauniaux E. A clinico-pathologic study of placenta percreta. Int J Gynaecol Obstet. 2018;140(3):365–9.CrossRefPubMed Hubinont C, Mhallem M, Baldin P, Debieve F, Bernard P, Jauniaux E. A clinico-pathologic study of placenta percreta. Int J Gynaecol Obstet. 2018;140(3):365–9.CrossRefPubMed
36.
go back to reference Oyelese Y, Smulian JC. Placenta previa, placenta accreta, and vasa previa. Obstet Gynecol. 2006;107(4):927–41.CrossRefPubMed Oyelese Y, Smulian JC. Placenta previa, placenta accreta, and vasa previa. Obstet Gynecol. 2006;107(4):927–41.CrossRefPubMed
37.
go back to reference Arao T, Ishikawa S, Murakami M, Abe K, Maejima Y, Makino T. Heavy metal contamination of agricultural soil and countermeasures in Japan. Paddy Water Environ. 2010;8(3):247–57.CrossRef Arao T, Ishikawa S, Murakami M, Abe K, Maejima Y, Makino T. Heavy metal contamination of agricultural soil and countermeasures in Japan. Paddy Water Environ. 2010;8(3):247–57.CrossRef
38.
go back to reference Ciobanu C, Slencu BG, Cuciureanu R. Estimation of dietary intake of cadmium and lead through food consumption. Rev Med Chir Soc Med Nat Iasi. 2012;116(2):617–23.PubMed Ciobanu C, Slencu BG, Cuciureanu R. Estimation of dietary intake of cadmium and lead through food consumption. Rev Med Chir Soc Med Nat Iasi. 2012;116(2):617–23.PubMed
39.
go back to reference Ashraf MW. Levels of heavy metals in popular cigarette brands and exposure to these metals via smoking. ScientificWorldJournal. 2012;2012:729430.PubMedCentralPubMed Ashraf MW. Levels of heavy metals in popular cigarette brands and exposure to these metals via smoking. ScientificWorldJournal. 2012;2012:729430.PubMedCentralPubMed
40.
go back to reference Matsuda Y, Hayashi K, Shiozaki A, Kawamichi Y, Satoh S, Saito S. Comparison of risk factors for placental abruption and placenta previa: case-cohort study. J Obstet Gynaecol Res. 2011;37(6):538–46.CrossRefPubMed Matsuda Y, Hayashi K, Shiozaki A, Kawamichi Y, Satoh S, Saito S. Comparison of risk factors for placental abruption and placenta previa: case-cohort study. J Obstet Gynaecol Res. 2011;37(6):538–46.CrossRefPubMed
41.
go back to reference Ikeda M, Ohashi F, Fukui Y, Sakuragi S, Moriguchi J. Cadmium, chromium, lead, manganese and nickel concentrations in blood of women in non-polluted areas in Japan, as determined by inductively coupled plasma-sector field-mass spectrometry. Int Arch Occup Environ Health. 2011;84(2):139–50.CrossRefPubMed Ikeda M, Ohashi F, Fukui Y, Sakuragi S, Moriguchi J. Cadmium, chromium, lead, manganese and nickel concentrations in blood of women in non-polluted areas in Japan, as determined by inductively coupled plasma-sector field-mass spectrometry. Int Arch Occup Environ Health. 2011;84(2):139–50.CrossRefPubMed
43.
go back to reference Nishijo M, Suwazono Y, Ruangyuttikarn W, Nambunmee K, Swaddiwudhipong W, Nogawa K, et al. Risk assessment for Thai population: benchmark dose of urinary and blood cadmium levels for renal effects by hybrid approach of inhabitants living in polluted and non-polluted areas in Thailand. BMC Public Health. 2014;14:702.PubMedCentralCrossRefPubMed Nishijo M, Suwazono Y, Ruangyuttikarn W, Nambunmee K, Swaddiwudhipong W, Nogawa K, et al. Risk assessment for Thai population: benchmark dose of urinary and blood cadmium levels for renal effects by hybrid approach of inhabitants living in polluted and non-polluted areas in Thailand. BMC Public Health. 2014;14:702.PubMedCentralCrossRefPubMed
44.
go back to reference Nawrot TS, Staessen JA, Roels HA, Munters E, Cuypers A, Richart T, et al. Cadmium exposure in the population: from health risks to strategies of prevention. Biometals. 2010;23(5):769–82.CrossRefPubMed Nawrot TS, Staessen JA, Roels HA, Munters E, Cuypers A, Richart T, et al. Cadmium exposure in the population: from health risks to strategies of prevention. Biometals. 2010;23(5):769–82.CrossRefPubMed
46.
go back to reference Kataoka Y, Watanabe T, Shiramasa Y, Matsuda R. Surveillance of cadmium level in octopus, squid, clam, short-necked clam and chocolate. Shokuhin Eiseigaku Zasshi J Food Hyg Soc Jpn. 2012;53(3):146–51.CrossRef Kataoka Y, Watanabe T, Shiramasa Y, Matsuda R. Surveillance of cadmium level in octopus, squid, clam, short-necked clam and chocolate. Shokuhin Eiseigaku Zasshi J Food Hyg Soc Jpn. 2012;53(3):146–51.CrossRef
47.
go back to reference Yamagami T, Ezaki T, Moriguchi J, Fukui Y, Okamoto S, Ukai H, et al. Low-level cadmium exposure in Toyama City and its surroundings in Toyama prefecture, Japan, with references to possible contribution of shellfish intake to increase urinary cadmium levels. Sci Total Environ. 2006;362(1–3):56–67.CrossRefPubMed Yamagami T, Ezaki T, Moriguchi J, Fukui Y, Okamoto S, Ukai H, et al. Low-level cadmium exposure in Toyama City and its surroundings in Toyama prefecture, Japan, with references to possible contribution of shellfish intake to increase urinary cadmium levels. Sci Total Environ. 2006;362(1–3):56–67.CrossRefPubMed
48.
go back to reference Akesson A, Berglund M, Schutz A, Bjellerup P, Bremme K, Vahter M. Cadmium exposure in pregnancy and lactation in relation to iron status. Am J Public Health. 2002;92(2):284–7.PubMedCentralCrossRefPubMed Akesson A, Berglund M, Schutz A, Bjellerup P, Bremme K, Vahter M. Cadmium exposure in pregnancy and lactation in relation to iron status. Am J Public Health. 2002;92(2):284–7.PubMedCentralCrossRefPubMed
49.
go back to reference Ito M, Takamori A, Yoneda S, Shiozaki A, Tsuchida A, Matsumura K, et al. Fermented foods and preterm birth risk from a prospective large cohort study: the Japan Environment and Children’s study. Environ Health Prev Med. 2019;24(1):25.PubMedCentralCrossRefPubMed Ito M, Takamori A, Yoneda S, Shiozaki A, Tsuchida A, Matsumura K, et al. Fermented foods and preterm birth risk from a prospective large cohort study: the Japan Environment and Children’s study. Environ Health Prev Med. 2019;24(1):25.PubMedCentralCrossRefPubMed
50.
go back to reference Nomura K, Karita K, Araki A, Nishioka E, Muto G, Iwai-Shimada M, et al. For making a declaration of countermeasures against the falling birth rate from the Japanese Society for Hygiene: summary of discussion in the working group on academic research strategy against an aging society with low birth rate. Environ Health Prev Med. 2019;24(1):14.PubMedCentralCrossRefPubMed Nomura K, Karita K, Araki A, Nishioka E, Muto G, Iwai-Shimada M, et al. For making a declaration of countermeasures against the falling birth rate from the Japanese Society for Hygiene: summary of discussion in the working group on academic research strategy against an aging society with low birth rate. Environ Health Prev Med. 2019;24(1):14.PubMedCentralCrossRefPubMed
Metadata
Title
Associations between metal concentrations in whole blood and placenta previa and placenta accreta: the Japan Environment and Children’s Study (JECS)
Authors
Mayumi Tsuji
Eiji Shibata
David J. Askew
Seiichi Morokuma
Yukiyo Aiko
Ayako Senju
Shunsuke Araki
Masafumi Sanefuji
Yasuhiro Ishihara
Rie Tanaka
Koichi Kusuhara
Toshihiro Kawamoto
Japan Environment and Children’s Study Group
Publication date
01-12-2019
Publisher
BioMed Central
Published in
Environmental Health and Preventive Medicine / Issue 1/2019
Print ISSN: 1342-078X
Electronic ISSN: 1347-4715
DOI
https://doi.org/10.1186/s12199-019-0795-7

Other articles of this Issue 1/2019

Environmental Health and Preventive Medicine 1/2019 Go to the issue