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Inverse association between maternal serum concentrations of trace elements and risk of spontaneous preterm birth: a nested case–control study in China
Published online by Cambridge University Press: 08 January 2024
Abstract
Few studies have evaluated the joint effect of trace elements on spontaneous preterm birth (SPTB). This study aimed to examine the relationships between the individual or mixed maternal serum concentrations of Fe, Cu, Zn, Se, Sr and Mo during pregnancy, and risk of SPTB. Inductively coupled plasma MS was employed to determine maternal serum concentrations of the six trace elements in 192 cases with SPTB and 282 controls with full-term delivery. Multivariate logistic regression, weighted quantile sum regression (WQSR) and Bayesian kernel machine regression (BKMR) were used to evaluate the individual and joint effects of trace elements on SPTB. The median concentrations of Sr and Mo were significantly higher in controls than in SPTB group (P < 0·05). In multivariate logistic regression analysis, compared with the lowest quartile levels of individual trace elements, the third- and fourth-quartile Sr or Mo concentrations were significantly associated with reduced risk of SPTB with adjusted OR (aOR) of 0·432 (95 CI < 0·05). In multivariate logistic regression analysis, compared with the lowest quartile levels of individual trace elements, the third- and fourth-quartile Sr or Mo concentrations were significantly associated with reduced risk of SPTB with adjusted aOR of 0·432 (95 % CI 0·247, 0·756), 0·386 (95 % CI 0·213, 0·701), 0·512 (95 % CI 0·297, 0·883) and 0·559 (95 % CI 0·321, 0·972), respectively. WQSR revealed the inverse combined effect of the trace elements mixture on SPTB (aOR = 0·368, 95 % CI 0·228, 0·593). BKMR analysis confirmed the overall mixture of the trace elements was inversely associated with the risk of SPTB, and the independent effect of Sr and Mo was significant. Our findings suggest that the risk of SPTB decreased with concentrations of the six trace elements, with Sr and Mo being the major contributors.
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- Research Article
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- © The Author(s), 2024. Published by Cambridge University Press on behalf of The Nutrition Society
Footnotes
†
These authors contributed equally to this work
References
WHO (1977) Recommended definitions, terminology and format for statistical tables related to the perinatal period and use of a new certificate for cause of perinatal deaths. Modifications recommended by FIGO as amended October 14, 1976. Acta Obstet Gynecol Scand 56, 247–253.Google Scholar
Chawanpaiboon, S, Vogel, JP, Moller, AB, et al. (2019) Global, regional, and national estimates of levels of preterm birth in 2014: a systematic review and modelling analysis. Lancet Glob Health 7, e37–e46.CrossRefGoogle ScholarPubMed
Deng, K, Liang, J, Mu, Y, et al. (2021) Preterm births in China between 2012 and 2018: an observational study of more than 9 million women. Lancet Glob Health 9, e1226–e1241.CrossRefGoogle Scholar
Goldenberg, RL, Culhane, JF, Iams, JD, et al. (2008) Epidemiology and causes of preterm birth. Lancet 371, 75–84.CrossRefGoogle ScholarPubMed
Zou, L, Wang, X, Ruan, Y, et al. (2014) Preterm birth and neonatal mortality in China in 2011. Int J Gynaecol Obstet 127, 243–247.CrossRefGoogle Scholar
Liu, L, Oza, S, Hogan, D, et al. (2016) Global, regional, and national causes of under-5 mortality in 2000–15: an updated systematic analysis with implications for the sustainable development goals. Lancet 388, 3027–3035.CrossRefGoogle ScholarPubMed
Blencowe, H, Cousens, S, Chou, D, et al. (2013) Born too soon: the global epidemiology of 15 million preterm births. Reprod Health 10, S2.CrossRefGoogle ScholarPubMed
Jain, VG, Monangi, N, Zhang, G, et al. (2022) Genetics, epigenetics, and transcriptomics of preterm birth. Am J Reprod Immunol 88, e13600.CrossRefGoogle ScholarPubMed
Ferguson, KK & Chin, HB (2017) Environmental chemicals and preterm birth: biological mechanisms and the state of the science. Curr Epidemiol Rep 4, 56–71.CrossRefGoogle ScholarPubMed
Etzel, RA (2020) Is the environment associated with preterm birth? JAMA Netw Open 3, e202239.CrossRefGoogle Scholar
Tiensuu, H, Haapalainen, AM, Karjalainen, MK, et al. (2019) Risk of spontaneous preterm birth and fetal growth associates with fetal SLIT2. PLoS Genet 15, e1008107.CrossRefGoogle ScholarPubMed
Gernand, AD, Schulze, KJ, Stewart, CP, et al. (2016) Micronutrient deficiencies in pregnancy worldwide: health effects and prevention. Nat Rev Endocrinol 12, 274–289.CrossRefGoogle ScholarPubMed
Lewicka, I, Kocylowski, R, Grzesiak, M, et al. (2017) Selected trace elements concentrations in pregnancy and their possible role – literature review. Ginekol Pol 88, 509–514.CrossRefGoogle ScholarPubMed
Wolf, HT, Hegaard, HK, Huusom, LD, et al. (2017) Multivitamin use and adverse birth outcomes in high-income countries: a systematic review and meta-analysis. Am J Obstet Gynecol 217, 404. e401–404. e430.CrossRefGoogle ScholarPubMed
Pena-Rosas, JP, De-Regil, LM, Garcia-Casal, MN, et al. (2015) Daily oral iron supplementation during pregnancy. The Cochrane Database of Systematic Review 2015, issue 7, CD004736.CrossRefGoogle Scholar
Mosha, D, Liu, E, Hertzmark, E, et al. (2017) Dietary iron and calcium intakes during pregnancy are associated with lower risk of prematurity, stillbirth and neonatal mortality among women in Tanzania. Public Health Nutr 20, 678–686.CrossRefGoogle ScholarPubMed
Oaks, BM, Jorgensen, JM, Baldiviez, LM, et al. (2019) Prenatal iron deficiency and replete iron status are associated with adverse birth outcomes, but associations differ in Ghana and Malawi. J Nutr 149, 513–521.CrossRefGoogle ScholarPubMed
Shao, Y, Mao, B, Qiu, J, et al. (2021) Association between iron supplementation, dietary iron intake and risk of moderate preterm birth: a birth cohort study in China. Iran J Public Health 50, 1177–1187.Google ScholarPubMed
Ren, M, Zhao, J, Wang, B, et al. (2022) Associations between hair levels of trace elements and the risk of preterm birth among pregnant women: a prospective nested case-control study in Beijing Birth Cohort (BBC), China. Environ Int 158, 106965.CrossRefGoogle ScholarPubMed
Li, Z, Liang, C, Huang, K, et al. (2018) Umbilical serum copper status and neonatal birth outcomes: a prospective cohort study. Biol Trace Elem Res 183, 200–208.CrossRefGoogle ScholarPubMed
Wang, H, Hu, YF, Hao, JH, et al. (2016) Maternal serum zinc concentration during pregnancy is inversely associated with risk of preterm birth in a Chinese population. J Nutr 146, 509–515.CrossRefGoogle ScholarPubMed
Huang, H, Wei, Y, Xia, Y, et al. (2021) Child marriage, maternal serum metal exposure, and risk of preterm birth in rural Bangladesh: evidence from mediation analysis. J Expo Sci Environ Epidemiol 31, 571–580.CrossRefGoogle ScholarPubMed
Rayman, MP, Wijnen, H, Vader, H, et al. (2011) Maternal selenium status during early gestation and risk for preterm birth. CMAJ 183, 549–555.CrossRefGoogle ScholarPubMed
Okunade, KS, Olowoselu, OF, Osanyin, GE, et al. (2018) Selenium deficiency and pregnancy outcome in pregnant women with HIV in Lagos, Nigeria. Int J Gynaecol Obstet 142, 207–213.CrossRefGoogle ScholarPubMed
Barman, M, Brantsaeter, AL, Nilsson, S, et al. (2020) Maternal dietary selenium intake is associated with increased gestational length and decreased risk of preterm delivery. Br J Nutr 123, 209–219.CrossRefGoogle ScholarPubMed
Monangi, N, Xu, H, Khanam, R, et al. (2021) Association of maternal prenatal selenium concentration and preterm birth: a multicountry meta-analysis. BMJ Glob Health 6, e005856.CrossRefGoogle ScholarPubMed
Brabin, B, Gies, S, Roberts, SA, et al. (2019) Excess risk of preterm birth with periconceptional iron supplementation in a malaria endemic area: analysis of secondary data on birth outcomes in a double blind randomized controlled safety trial in Burkina Faso. Malar J 18, 161.CrossRefGoogle Scholar
Yuan, X, Hu, H, Zhang, M, et al. (2019) Iron deficiency in late pregnancy and its associations with birth outcomes in Chinese pregnant women: a retrospective cohort study. Nutr Metab (Lond) 16, 30.CrossRefGoogle ScholarPubMed
Xu, R, Meng, X, Pang, Y, et al. (2022) Associations of maternal exposure to 41 metals/metalloids during early pregnancy with the risk of spontaneous preterm birth: does oxidative stress or DNA methylation play a crucial role? Environ Int 158, 106966.CrossRefGoogle ScholarPubMed
Kim, SS, Meeker, JD, Carroll, R, et al. (2018) Urinary trace metals individually and in mixtures in association with preterm birth. Environ Int 121, 582–590.CrossRefGoogle ScholarPubMed
Wilson, RL, Bianco-Miotto, T, Leemaqz, SY, et al. (2018) Early pregnancy maternal trace mineral status and the association with adverse pregnancy outcome in a cohort of Australian women. J Trace Elem Med Biol 46, 103–109.CrossRefGoogle Scholar
Hao, Y, Pang, Y, Yan, H, et al. (2019) Association of maternal serum copper during early pregnancy with the risk of spontaneous preterm birth: a nested case-control study in China. Environ Int 122, 237–243.CrossRefGoogle ScholarPubMed
Liu, J, Ruan, F, Cao, S, et al. (2022) Associations between prenatal multiple metal exposure and preterm birth: comparison of four statistical models. Chemosphere 289, 133015.CrossRefGoogle ScholarPubMed
Ashrap, P, Watkins, DJ, Mukherjee, B, et al. (2020) Maternal blood metal and metalloid concentrations in association with birth outcomes in Northern Puerto Rico. Environ Int 138, 105606.CrossRefGoogle ScholarPubMed
Chiudzu, G, Choko, AT, Maluwa, A, et al. (2020) Maternal serum concentrations of selenium, copper, and zinc during pregnancy are associated with risk of spontaneous preterm birth: a case-control study from Malawi. J Pregnancy 2020, 9435972.CrossRefGoogle ScholarPubMed
Huang, H, Wei, L, Chen, X, et al. (2021) Cord serum elementomics profiling of 56 elements depicts risk of preterm birth: evidence from a prospective birth cohort in rural Bangladesh. Environ Int 156, 106731.CrossRefGoogle ScholarPubMed
Carducci, B, Keats, EC & Bhutta, ZA (2021) Zinc supplementation for improving pregnancy and infant outcome. The Cochrane Database of Systematic Review 2021, issue 3, CD000230.Google Scholar
Tsuji, M, Shibata, E, Morokuma, S, et al. (2018) 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 166, 562–569.CrossRefGoogle ScholarPubMed
Braun, JM, Gennings, C, Hauser, R, et al. (2016) What can epidemiological studies tell us about the impact of chemical mixtures on human health? Environ Health Perspect 124, A6–A9.CrossRefGoogle ScholarPubMed
Carrico, C, Gennings, C, Wheeler, DC, et al. (2015) Characterization of weighted quantile sum regression for highly correlated data in a risk analysis setting. J Agric Biol Environ Stat 20, 100–120.CrossRefGoogle Scholar
Czarnota, J, Gennings, C & Wheeler, DC (2015) Assessment of weighted quantile sum regression for modeling chemical mixtures and cancer risk. Cancer Inform 14, 159–171.Google ScholarPubMed
Bobb, JF, Valeri, L, Claus Henn, B, et al. (2015) Bayesian kernel machine regression for estimating the health effects of multi–pollutant mixtures. Biostatistics 16, 493–508.CrossRefGoogle ScholarPubMed
Bobb, JF, Claus Henn, B, Valeri, L, et al. (2018) Statistical software for analyzing the health effects of multiple concurrent exposures via Bayesian kernel machine regression. Environ Health 17, 67.CrossRefGoogle ScholarPubMed
Zoroddu, MA, Aaseth, J, Crisponi, G, et al. (2019) The essential metals for humans: a brief overview. J Inorg Biochem 195, 120–129.CrossRefGoogle ScholarPubMed
Barneo-Caragol, C, Martinez-Morillo, E, Rodriguez-Gonzalez, S, et al. (2018) Strontium and oxidative stress in normal pregnancy. J Trace Elem Med Biol 45, 57–63.CrossRefGoogle ScholarPubMed
Schaafsma, A, de Vries, PJ & Saris, WH (2001) Delay of natural bone loss by higher intakes of specific minerals and vitamins. Crit Rev Food Sci Nutr 41, 225–249.CrossRefGoogle ScholarPubMed
Pors Nielsen, S (2004) The biological role of strontium. Bone 35, 583–588.CrossRefGoogle ScholarPubMed
Yu, HY & Zhang, KL (2011) Links between environmental geochemistry and rate of birth defects: Shanxi Province, China. Sci Total Environ 409, 447–451.CrossRefGoogle ScholarPubMed
Li, Z, Wang, B, Huo, W, et al. (2017) Are concentrations of alkaline earth elements in maternal hair associated with risk of neural tube defects? Sci Total Environ 609, 694–700.CrossRefGoogle ScholarPubMed
Shenkin, AM (2003) Dietary reference values for vitamin A, vitamin K, arsenic, boron, chromium, copper, iodine, iron, manganese, molybdenum, nickel, silicon, vanadium and zinc. J Hum Nutr Diet 16, 199–200.CrossRefGoogle Scholar
Khayat, S, Fanaei, H & Ghanbarzehi, A (2017) Minerals in pregnancy and lactation: a review article. J Clin Diagn Res 11, QE01–QE05.CrossRefGoogle Scholar
Zhao, L, Wang, S, Liu, M, et al. (2023) Maternal urinary metal(loid)s and risk of preterm birth: a cohort study in the Tibetan Plateau. Environ Pollut 333, 122085.CrossRefGoogle ScholarPubMed
Tian, T, Yin, S, Jin, L, et al. (2021) Single and mixed effects of metallic elements in maternal serum during pregnancy on risk for fetal neural tube defects: a Bayesian kernel regression approach. Environ Pollut 285, 117203.CrossRefGoogle ScholarPubMed
Yin, S, Wang, C, Wei, J, et al. (2020) Selected essential trace elements in maternal serum and risk for fetal orofacial clefts. Sci Total Environ 712, 136542.CrossRefGoogle ScholarPubMed
Odland, JO, Nieboer, E, Romanova, N, et al. (2001) Factor analysis of essential and toxic elements in human placentas from deliveries in arctic and subarctic areas of Russia and Norway. J Environ Monit 3, 177–184.CrossRefGoogle ScholarPubMed
Sultana, Z, Maiti, K, Aitken, J, et al. (2017) Oxidative stress, placental ageing-related pathologies and adverse pregnancy outcomes. Am J Reprod Immunol 77, e12653.CrossRefGoogle ScholarPubMed
Moore, TA, Ahmad, IM & Zimmerman, MC (2018) Oxidative stress and preterm birth: an integrative review. Biol Res Nurs 20, 497–512.CrossRefGoogle ScholarPubMed
El-Megharbel, SM, Hamza, RZ & Refat, MS (2015) Synthesis, spectroscopic and thermal studies of Mg(II), Ca(II), Sr(II) and Ba(II) diclofenac sodium complexes as anti-inflammatory drug and their protective effects on renal functions impairment and oxidative stress. Spectrochim Acta A Mol Biomol Spectrosc 135, 915–928.CrossRefGoogle Scholar
Yalin, S, Sagir, O, Comelekoglu, U, et al. (2012) Strontium ranelate treatment improves oxidative damage in osteoporotic rat model. Pharmacol Rep 64, 396–402.CrossRefGoogle ScholarPubMed
Bai, Y, Feng, W, Wang, S, et al. (2016) Essential metals zinc, selenium, and strontium protect against chromosome damage caused by polycyclic aromatic hydrocarbons exposure. Environ Sci Technol 50, 951–960.CrossRefGoogle ScholarPubMed
Kim, SS, Meeker, JD, Keil, AP, et al. (2019) Exposure to 17 trace metals in pregnancy and associations with urinary oxidative stress biomarkers. Environ Res 179, 108854.CrossRefGoogle ScholarPubMed
Zhang, M, Liu, C, Li, WD, et al. (2022) Individual and mixtures of metal exposures in associations with biomarkers of oxidative stress and global DNA methylation among pregnant women. Chemosphere 293, 133662.CrossRefGoogle ScholarPubMed
Foteva, V, Fisher, JJ, Qiao, Y, et al. (2023) Does the micronutrient molybdenum have a role in gestational complications and placental health? Nutrients 15, 3348.CrossRefGoogle ScholarPubMed
Wei, SQ, Fraser, W & Luo, ZC (2010) Inflammatory cytokines and spontaneous preterm birth in asymptomatic women: a systematic review. Obstet Gynecol 116, 393–401.CrossRefGoogle ScholarPubMed
Negishi, Y, Shima, Y, Kato, M, et al. (2022) Inflammation in preterm birth: novel mechanism of preterm birth associated with innate and acquired immunity. J Reprod Immunol 154, 103748.CrossRefGoogle ScholarPubMed
Berksoy Hayta, S, Durmus, K, Altuntas, EE, et al. (2018) The reduction in inflammation and impairment in wound healing by using strontium chloride hexahydrate. Cutan Ocul Toxicol 37, 24–28.CrossRefGoogle ScholarPubMed
Pilmane, M, Salma-Ancane, K, Loca, D, et al. (2017) Strontium and strontium ranelate: historical review of some of their functions. Mater Sci Eng C Mater Biol Appl 78, 1222–1230.CrossRefGoogle ScholarPubMed
Burris, HH, Baccarelli, AA, Wright, RO, et al. (2016) Epigenetics: linking social and environmental exposures to preterm birth. Pediatr Res 79, 136–140.CrossRefGoogle ScholarPubMed
Maitre, L, Bustamante, M, Hernandez-Ferrer, C, et al. (2022) Multi-omics signatures of the human early life exposome. Nat Commun 13, 7024.CrossRefGoogle ScholarPubMed
Koh, EJ, Yu, SY, Kim, SH, et al. (2021) Prenatal exposure to heavy metals affects gestational age by altering DNA methylation patterns. Nanomater (Basel) 11, 2871.CrossRefGoogle ScholarPubMed
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