Skip to main content
Top
Published in: BMC Pregnancy and Childbirth 1/2020

Open Access 01-12-2020 | Research article

Maternal plasma lipid levels across pregnancy and the risks of small-for-gestational age and low birth weight: a cohort study from rural Gambia

Authors: Sandra G. Okala, Ebrima A. Sise, Fatou Sosseh, Andrew M. Prentice, Laura A. Woollett, Sophie E. Moore

Published in: BMC Pregnancy and Childbirth | Issue 1/2020

Login to get access

Abstract

Background

Sub-optimal maternal lipid levels during pregnancy may be implicated in the pathophysiological mechanisms leading to low birth weight (LBW) and small-for-gestational-age (SGA). We aimed to determine whether maternal lipid levels across pregnancy were associated with birth weight and the risks of LBW and SGA in rural Gambia.

Methods

This secondary analysis of the ENID trial involved 573 pregnant women with term deliveries. Plasma levels of total cholesterol (TC), high-density lipoprotein cholesterol (HDL-c), low-density lipoprotein cholesterol (LDL-c), and triglycerides (TG) were analyzed at enrolment (mean (SD) = 13.9 (3.3) weeks gestation), 20 and 30 weeks gestation as continuous variables and percentile groups. Regression models with adjustment for confounders were used to examine associations between gestational lipid levels and birth weight and the risks of LBW (birth weight < 2500 g) and SGA (<10th percentile INTERGROWTH-21ST for birth weight).

Results

There were 7.9% LBW and 32.5% SGA infants. At enrolment, every unit increase in HDL-c was associated with a 2.7% (P = 0.011) reduction in relative risk of LBW. At 20 weeks gestation, every unit increase in TC levels was associated with a 1.3% reduction in relative risk of LBW (P = 0.002). Low (<10th percentile) HDL-c at enrolment or at 20 weeks gestation was associated with a 2.6 (P = 0.007) and 3.0 (P = 0.003) times greater risk of LBW, respectively, compared with referent (10th─90th) HDL-c. High (>90th percentile) LDL-c at 30 weeks gestation was associated with a 55% lower risk of SGA compared with referent LDL-c (P = 0.017). Increased levels of TC (β = 1.3, P = 0.027) at 20 weeks gestation and of TC (β = 1.2, P = 0.006) and LDL-c (β = 1.5, P = 0.002) at 30 weeks gestation were all associated with higher birth weight.

Conclusions

In rural Gambia, lipid levels during pregnancy were associated with infant birth weight and the risks of LBW and SGA. Associations varied by lipid class and changed across pregnancy, indicating an adaptive process by which maternal lipids may influence fetal growth and birth outcomes.

Trial registration

This trial was registered as ISRCTN49285450 on: 12/11/2009.
Appendix
Available only for authorised users
Literature
1.
go back to reference Risnes KR, Vatten LJ, Baker JL, Jameson K, Sovio U, Kajantie E, et al. Birthweight and mortality in adulthood: a systematic review and meta-analysis. Int J Epidemiol. 2011;40(3):647–61.CrossRefPubMed Risnes KR, Vatten LJ, Baker JL, Jameson K, Sovio U, Kajantie E, et al. Birthweight and mortality in adulthood: a systematic review and meta-analysis. Int J Epidemiol. 2011;40(3):647–61.CrossRefPubMed
2.
go back to reference Catov JM, Dodge R, Yamal JM, Roberts JM, Piller LB, Ness RB. Prior preterm or small-for-gestational-age birth related to maternal metabolic syndrome. Obstet Gynecol. 2011;117(2 Pt 1):225–32.CrossRefPubMedPubMedCentral Catov JM, Dodge R, Yamal JM, Roberts JM, Piller LB, Ness RB. Prior preterm or small-for-gestational-age birth related to maternal metabolic syndrome. Obstet Gynecol. 2011;117(2 Pt 1):225–32.CrossRefPubMedPubMedCentral
3.
go back to reference Bonamy AK, Parikh NI, Cnattingius S, Ludvigsson JF, Ingelsson E. Birth characteristics and subsequent risks of maternal cardiovascular disease: effects of gestational age and fetal growth. Circulation. 2011;124(25):2839–46.CrossRefPubMed Bonamy AK, Parikh NI, Cnattingius S, Ludvigsson JF, Ingelsson E. Birth characteristics and subsequent risks of maternal cardiovascular disease: effects of gestational age and fetal growth. Circulation. 2011;124(25):2839–46.CrossRefPubMed
5.
go back to reference Saigal S, Doyle LW. An overview of mortality and sequelae of preterm birth from infancy to adulthood. Lancet. 2008;371(9608):261–9.CrossRefPubMed Saigal S, Doyle LW. An overview of mortality and sequelae of preterm birth from infancy to adulthood. Lancet. 2008;371(9608):261–9.CrossRefPubMed
6.
go back to reference Garcia-Basteiro AL, Quinto L, Macete E, Bardaji A, Gonzalez R, Nhacolo A, et al. Infant mortality and morbidity associated with preterm and small-for-gestational-age births in southern Mozambique: a retrospective cohort study. PLoS One. 2017;12(2):e0172533.CrossRefPubMedPubMedCentral Garcia-Basteiro AL, Quinto L, Macete E, Bardaji A, Gonzalez R, Nhacolo A, et al. Infant mortality and morbidity associated with preterm and small-for-gestational-age births in southern Mozambique: a retrospective cohort study. PLoS One. 2017;12(2):e0172533.CrossRefPubMedPubMedCentral
7.
go back to reference Blencowe H, Cousens S, Jassir FB, Say L, Chou D, Mathers C, et al. National, regional, and worldwide estimates of stillbirth rates in 2015, with trends from 2000: a systematic analysis. Lancet Glob Health. 2016;4(2):e98–e108. Blencowe H, Cousens S, Jassir FB, Say L, Chou D, Mathers C, et al. National, regional, and worldwide estimates of stillbirth rates in 2015, with trends from 2000: a systematic analysis. Lancet Glob Health. 2016;4(2):e98–e108.
8.
go back to reference Lee AC, Kozuki N, Cousens S, Stevens GA, Blencowe H, Silveira MF, et al. Estimates of burden and consequences of infants born small for gestational age in low and middle income countries with INTERGROWTH-21(st) standard: analysis of CHERG datasets. Bmj. 2017;358:j3677.CrossRefPubMedPubMedCentral Lee AC, Kozuki N, Cousens S, Stevens GA, Blencowe H, Silveira MF, et al. Estimates of burden and consequences of infants born small for gestational age in low and middle income countries with INTERGROWTH-21(st) standard: analysis of CHERG datasets. Bmj. 2017;358:j3677.CrossRefPubMedPubMedCentral
9.
go back to reference Kramer MS. Determinants of low birth weight: methodological assessment and meta-analysis. Bull World Health Organ. 1987;65(5):663–737.PubMedPubMedCentral Kramer MS. Determinants of low birth weight: methodological assessment and meta-analysis. Bull World Health Organ. 1987;65(5):663–737.PubMedPubMedCentral
10.
go back to reference Jin WY, Lin SL, Hou RL, Chen XY, Han T, Jin Y, et al. Associations between maternal lipid profile and pregnancy complications and perinatal outcomes: a population-based study from China. BMC Pregnancy Childbirth. 2016;16:60.CrossRefPubMedPubMedCentral Jin WY, Lin SL, Hou RL, Chen XY, Han T, Jin Y, et al. Associations between maternal lipid profile and pregnancy complications and perinatal outcomes: a population-based study from China. BMC Pregnancy Childbirth. 2016;16:60.CrossRefPubMedPubMedCentral
11.
13.
go back to reference Grimes SB, Wild R. Effect of pregnancy on lipid metabolism and lipoprotein levels; 2018. Grimes SB, Wild R. Effect of pregnancy on lipid metabolism and lipoprotein levels; 2018.
14.
go back to reference Edison RJ, Berg K, Remaley A, Kelley R, Rotimi C, Stevenson RE, et al. Adverse birth outcome among mothers with low serum cholesterol. Pediatrics. 2007;120(4):723–33.CrossRefPubMed Edison RJ, Berg K, Remaley A, Kelley R, Rotimi C, Stevenson RE, et al. Adverse birth outcome among mothers with low serum cholesterol. Pediatrics. 2007;120(4):723–33.CrossRefPubMed
15.
go back to reference Okunade KSOA. Predictive significance of low maternal serum cholesterol concentrations in early pregnancy on low birth weight in term neonates. Afr J Med Health Sci. 2017;16:94–8.CrossRef Okunade KSOA. Predictive significance of low maternal serum cholesterol concentrations in early pregnancy on low birth weight in term neonates. Afr J Med Health Sci. 2017;16:94–8.CrossRef
16.
go back to reference Kulkarni SR, Kumaran K, Rao SR, Chougule SD, Deokar TM, Bhalerao AJ, et al. Maternal lipids are as important as glucose for fetal growth: findings from the Pune maternal nutrition study. Diabetes Care. 2013;36(9):2706–13.CrossRefPubMedPubMedCentral Kulkarni SR, Kumaran K, Rao SR, Chougule SD, Deokar TM, Bhalerao AJ, et al. Maternal lipids are as important as glucose for fetal growth: findings from the Pune maternal nutrition study. Diabetes Care. 2013;36(9):2706–13.CrossRefPubMedPubMedCentral
17.
go back to reference Geraghty AA, Alberdi G, O'Sullivan EJ, O'Brien EC, Crosbie B, Twomey PJ, et al. Maternal and fetal blood lipid concentrations during pregnancy differ by maternal body mass index: findings from the ROLO study. BMC Pregnancy Childbirth. 2017;17(1):360.CrossRefPubMedPubMedCentral Geraghty AA, Alberdi G, O'Sullivan EJ, O'Brien EC, Crosbie B, Twomey PJ, et al. Maternal and fetal blood lipid concentrations during pregnancy differ by maternal body mass index: findings from the ROLO study. BMC Pregnancy Childbirth. 2017;17(1):360.CrossRefPubMedPubMedCentral
18.
go back to reference Vrijkotte TG, Algera SJ, Brouwer IA, van Eijsden M, Twickler MB. Maternal triglyceride levels during early pregnancy are associated with birth weight and postnatal growth. J Pediatr. 2011;159(5):736–42.e1.CrossRefPubMed Vrijkotte TG, Algera SJ, Brouwer IA, van Eijsden M, Twickler MB. Maternal triglyceride levels during early pregnancy are associated with birth weight and postnatal growth. J Pediatr. 2011;159(5):736–42.e1.CrossRefPubMed
19.
go back to reference Di Cianni G, Miccoli R, Volpe L, Lencioni C, Ghio A, Giovannitti MG, et al. Maternal triglyceride levels and newborn weight in pregnant women with normal glucose tolerance. Diabet Med. 2005;22(1):21–5.CrossRefPubMed Di Cianni G, Miccoli R, Volpe L, Lencioni C, Ghio A, Giovannitti MG, et al. Maternal triglyceride levels and newborn weight in pregnant women with normal glucose tolerance. Diabet Med. 2005;22(1):21–5.CrossRefPubMed
20.
go back to reference Kramer MS, Kahn SR, Dahhou M, Otvos J, Genest J, Platt RW, et al. Maternal lipids and small for gestational age birth at term. J Pediatr. 2013;163(4):983–8.CrossRefPubMed Kramer MS, Kahn SR, Dahhou M, Otvos J, Genest J, Platt RW, et al. Maternal lipids and small for gestational age birth at term. J Pediatr. 2013;163(4):983–8.CrossRefPubMed
21.
go back to reference Moore SE, Fulford AJ, Darboe MK, Jobarteh ML, Jarjou LM, Prentice AM. A randomized trial to investigate the effects of pre-natal and infant nutritional supplementation on infant immune development in rural Gambia: the ENID trial: early nutrition and immune development. BMC Pregnancy Childbirth. 2012;12:107.CrossRefPubMedPubMedCentral Moore SE, Fulford AJ, Darboe MK, Jobarteh ML, Jarjou LM, Prentice AM. A randomized trial to investigate the effects of pre-natal and infant nutritional supplementation on infant immune development in rural Gambia: the ENID trial: early nutrition and immune development. BMC Pregnancy Childbirth. 2012;12:107.CrossRefPubMedPubMedCentral
22.
go back to reference Hennig BJ, Unger SA, Dondeh BL, Hassan J, Hawkesworth S, Jarjou L, et al. Cohort profile: the kiang west longitudinal population study (KWLPS)-a platform for integrated research and health care provision in rural Gambia. Int J Epidemiol. 2017;46(2):e13.PubMed Hennig BJ, Unger SA, Dondeh BL, Hassan J, Hawkesworth S, Jarjou L, et al. Cohort profile: the kiang west longitudinal population study (KWLPS)-a platform for integrated research and health care provision in rural Gambia. Int J Epidemiol. 2017;46(2):e13.PubMed
23.
go back to reference UNICEF, Organization WH, University UN. Composition of a multi-micronutrient supplement to be used in pilot programmes among pregnant women in developing countries: report of a United Nations Children's Fund (UNICEF), World Health Organization (WHO) and United Nations University workshop. 1999. UNICEF, Organization WH, University UN. Composition of a multi-micronutrient supplement to be used in pilot programmes among pregnant women in developing countries: report of a United Nations Children's Fund (UNICEF), World Health Organization (WHO) and United Nations University workshop. 1999.
24.
go back to reference Villar J, Altman DG, Purwar M, Noble JA, Knight HE, Ruyan P, et al. The objectives, design and implementation of the INTERGROWTH-21st Project. Bjog. 2013;120(Suppl 2):9–26 v.CrossRefPubMed Villar J, Altman DG, Purwar M, Noble JA, Knight HE, Ruyan P, et al. The objectives, design and implementation of the INTERGROWTH-21st Project. Bjog. 2013;120(Suppl 2):9–26 v.CrossRefPubMed
25.
go back to reference Johnson W, Elmrayed SA, Sosseh F, Prentice AM, Moore SE. Preconceptional and gestational weight trajectories and risk of delivering a small-for-gestational-age baby in rural Gambia12. Am J Clin Nutr. 2017;105(6):1474–82.PubMedPubMedCentral Johnson W, Elmrayed SA, Sosseh F, Prentice AM, Moore SE. Preconceptional and gestational weight trajectories and risk of delivering a small-for-gestational-age baby in rural Gambia12. Am J Clin Nutr. 2017;105(6):1474–82.PubMedPubMedCentral
26.
go back to reference Pusukuru R, Shenoi AS, Kyada PK, Ghodke B, Mehta V, Bhuta K, et al. Evaluation of lipid profile in second and third trimester of pregnancy. J Clin Diagn Res. 2016;10(3):QC12–6.PubMedPubMedCentral Pusukuru R, Shenoi AS, Kyada PK, Ghodke B, Mehta V, Bhuta K, et al. Evaluation of lipid profile in second and third trimester of pregnancy. J Clin Diagn Res. 2016;10(3):QC12–6.PubMedPubMedCentral
28.
go back to reference Wiznitzer A, Mayer A, Novack V, Sheiner E, Gilutz H, Malhotra A, et al. Association of lipid levels during gestation with preeclampsia and gestational diabetes mellitus: a population-based study. Am J Obstet Gynecol. 2009;201(5):482.e1–8.CrossRef Wiznitzer A, Mayer A, Novack V, Sheiner E, Gilutz H, Malhotra A, et al. Association of lipid levels during gestation with preeclampsia and gestational diabetes mellitus: a population-based study. Am J Obstet Gynecol. 2009;201(5):482.e1–8.CrossRef
29.
go back to reference Stefulj J, Panzenboeck U, Becker T, Hirschmugl B, Schweinzer C, Lang I, et al. Human endothelial cells of the placental barrier efficiently deliver cholesterol to the fetal circulation via ABCA1 and ABCG1. Circ Res. 2009;104(5):600–8.CrossRefPubMed Stefulj J, Panzenboeck U, Becker T, Hirschmugl B, Schweinzer C, Lang I, et al. Human endothelial cells of the placental barrier efficiently deliver cholesterol to the fetal circulation via ABCA1 and ABCG1. Circ Res. 2009;104(5):600–8.CrossRefPubMed
30.
go back to reference Rebholz SL, Burke KT, Yang Q, Tso P, Woollett LA. Dietary fat impacts fetal growth and metabolism: uptake of chylomicron remnant core lipids by the placenta. Am J Physiol Endocrinol Metab. 2011;301(2):E416–25.CrossRefPubMedPubMedCentral Rebholz SL, Burke KT, Yang Q, Tso P, Woollett LA. Dietary fat impacts fetal growth and metabolism: uptake of chylomicron remnant core lipids by the placenta. Am J Physiol Endocrinol Metab. 2011;301(2):E416–25.CrossRefPubMedPubMedCentral
31.
go back to reference Baardman ME, Erwich JJ, Berger RM, Hofstra RM, Kerstjens-Frederikse WS, Lutjohann D, et al. The origin of fetal sterols in second-trimester amniotic fluid: endogenous synthesis or maternal-fetal transport? Am J Obstet Gynecol. 2012;207(3):202.e19–25.CrossRef Baardman ME, Erwich JJ, Berger RM, Hofstra RM, Kerstjens-Frederikse WS, Lutjohann D, et al. The origin of fetal sterols in second-trimester amniotic fluid: endogenous synthesis or maternal-fetal transport? Am J Obstet Gynecol. 2012;207(3):202.e19–25.CrossRef
32.
go back to reference Siddiqi HK, Kiss D, Rader D. HDL-cholesterol and cardiovascular disease: rethinking our approach. Curr Opin Cardiol. 2015;30(5):536–42.CrossRefPubMed Siddiqi HK, Kiss D, Rader D. HDL-cholesterol and cardiovascular disease: rethinking our approach. Curr Opin Cardiol. 2015;30(5):536–42.CrossRefPubMed
33.
go back to reference Barter P, Gotto AM, LaRosa JC, Maroni J, Szarek M, Grundy SM, et al. HDL cholesterol, very low levels of LDL cholesterol, and cardiovascular events. N Engl J Med. 2007;357(13):1301–10.CrossRefPubMed Barter P, Gotto AM, LaRosa JC, Maroni J, Szarek M, Grundy SM, et al. HDL cholesterol, very low levels of LDL cholesterol, and cardiovascular events. N Engl J Med. 2007;357(13):1301–10.CrossRefPubMed
34.
go back to reference Curb JD, Abbott RD, Rodriguez BL, Masaki K, Chen R, Sharp DS, et al. A prospective study of HDL-C and cholesteryl ester transfer protein gene mutations and the risk of coronary heart disease in the elderly. J Lipid Res. 2004;45(5):948–53.CrossRefPubMed Curb JD, Abbott RD, Rodriguez BL, Masaki K, Chen R, Sharp DS, et al. A prospective study of HDL-C and cholesteryl ester transfer protein gene mutations and the risk of coronary heart disease in the elderly. J Lipid Res. 2004;45(5):948–53.CrossRefPubMed
35.
go back to reference Boghossian NS, Mendola P, Liu A, Robledo C, Yeung EH. Maternal serum markers of lipid metabolism in relation to neonatal anthropometry. J Perinatol. 2017;37(6):629–35.CrossRefPubMedPubMedCentral Boghossian NS, Mendola P, Liu A, Robledo C, Yeung EH. Maternal serum markers of lipid metabolism in relation to neonatal anthropometry. J Perinatol. 2017;37(6):629–35.CrossRefPubMedPubMedCentral
36.
go back to reference Mudd LM, Holzman CB, Catov JM, Senagore PK, Evans RW. Maternal lipids at mid-pregnancy and the risk of preterm delivery. Acta Obstet Gynecol Scand. 2012;91(6):726–35.CrossRefPubMedPubMedCentral Mudd LM, Holzman CB, Catov JM, Senagore PK, Evans RW. Maternal lipids at mid-pregnancy and the risk of preterm delivery. Acta Obstet Gynecol Scand. 2012;91(6):726–35.CrossRefPubMedPubMedCentral
37.
go back to reference Barrett HL, Dekker Nitert M, McIntyre HD, Callaway LK. Maternal lipids in pre-eclampsia: innocent bystander or culprit? Hypertens Pregnancy. 2014;33(4):508–23.CrossRefPubMed Barrett HL, Dekker Nitert M, McIntyre HD, Callaway LK. Maternal lipids in pre-eclampsia: innocent bystander or culprit? Hypertens Pregnancy. 2014;33(4):508–23.CrossRefPubMed
38.
go back to reference Rebholz SL, Melchior JT, Davidson WS, Jones HN, Welge JA, Prentice AM, et al. Studies in genetically modified mice implicate maternal HDL as a mediator of fetal growth. FASEB J. 2018;32(2):717–27.CrossRefPubMed Rebholz SL, Melchior JT, Davidson WS, Jones HN, Welge JA, Prentice AM, et al. Studies in genetically modified mice implicate maternal HDL as a mediator of fetal growth. FASEB J. 2018;32(2):717–27.CrossRefPubMed
39.
go back to reference Sulaiman WN, Caslake MJ, Delles C, Karlsson H, Mulder MT, Graham D, et al. Does high-density lipoprotein protect vascular function in healthy pregnancy? Clin Sci (Lond). 2016;130(7):491–7.CrossRef Sulaiman WN, Caslake MJ, Delles C, Karlsson H, Mulder MT, Graham D, et al. Does high-density lipoprotein protect vascular function in healthy pregnancy? Clin Sci (Lond). 2016;130(7):491–7.CrossRef
40.
go back to reference Ramsay JE, Ferrell WR, Crawford L, Wallace AM, Greer IA, Sattar N. Divergent metabolic and vascular phenotypes in pre-eclampsia and intrauterine growth restriction: relevance of adiposity. J Hypertens. 2004;22(11):2177–83.CrossRefPubMed Ramsay JE, Ferrell WR, Crawford L, Wallace AM, Greer IA, Sattar N. Divergent metabolic and vascular phenotypes in pre-eclampsia and intrauterine growth restriction: relevance of adiposity. J Hypertens. 2004;22(11):2177–83.CrossRefPubMed
41.
go back to reference Wyne KL, Woollett LA. Transport of maternal LDL and HDL to the fetal membranes and placenta of the Golden Syrian hamster is mediated by receptor-dependent and receptor-independent processes. J Lipid Res. 1998;39(3):518–30.PubMed Wyne KL, Woollett LA. Transport of maternal LDL and HDL to the fetal membranes and placenta of the Golden Syrian hamster is mediated by receptor-dependent and receptor-independent processes. J Lipid Res. 1998;39(3):518–30.PubMed
42.
go back to reference Schmid KE, Davidson WS, Myatt L, Woollett LA. Transport of cholesterol across a BeWo cell monolayer: implications for net transport of sterol from maternal to fetal circulation. J Lipid Res. 2003;44(10):1909–18.CrossRefPubMed Schmid KE, Davidson WS, Myatt L, Woollett LA. Transport of cholesterol across a BeWo cell monolayer: implications for net transport of sterol from maternal to fetal circulation. J Lipid Res. 2003;44(10):1909–18.CrossRefPubMed
43.
go back to reference Misra VK, Trudeau S, Perni U. Maternal serum lipids during pregnancy and infant birth weight: the influence of prepregnancy BMI. Obesity (Silver Spring). 2011;19(7):1476–81.CrossRef Misra VK, Trudeau S, Perni U. Maternal serum lipids during pregnancy and infant birth weight: the influence of prepregnancy BMI. Obesity (Silver Spring). 2011;19(7):1476–81.CrossRef
44.
go back to reference Enquobahrie DA, Williams MA, Butler CL, Frederick IO, Miller RS, Luthy DA. Maternal plasma lipid concentrations in early pregnancy and risk of preeclampsia. Am J Hypertens. 2004;17(7):574–81.CrossRefPubMed Enquobahrie DA, Williams MA, Butler CL, Frederick IO, Miller RS, Luthy DA. Maternal plasma lipid concentrations in early pregnancy and risk of preeclampsia. Am J Hypertens. 2004;17(7):574–81.CrossRefPubMed
45.
go back to reference Dempsey JC, Williams MA, Leisenring WM, Shy K, Luthy DA. Maternal birth weight in relation to plasma lipid concentrations in early pregnancy. Am J Obstet Gynecol. 2004;190(5):1359–68.CrossRefPubMed Dempsey JC, Williams MA, Leisenring WM, Shy K, Luthy DA. Maternal birth weight in relation to plasma lipid concentrations in early pregnancy. Am J Obstet Gynecol. 2004;190(5):1359–68.CrossRefPubMed
46.
go back to reference Laughon SK, McLain AC, Sundaram R, Catov JM, Louis GMB. Maternal lipid change in relation to length of gestation: a prospective cohort study with preconception enrollment of women. Gynecol Obstet Investig. 2014;77(1):6–13.CrossRef Laughon SK, McLain AC, Sundaram R, Catov JM, Louis GMB. Maternal lipid change in relation to length of gestation: a prospective cohort study with preconception enrollment of women. Gynecol Obstet Investig. 2014;77(1):6–13.CrossRef
47.
go back to reference Schaefer-Graf UM, Graf K, Kulbacka I, Kjos SL, Dudenhausen J, Vetter K, et al. Maternal lipids as strong determinants of fetal environment and growth in pregnancies with gestational diabetes mellitus. Diabetes Care. 2008;31(9):1858–63.CrossRefPubMedPubMedCentral Schaefer-Graf UM, Graf K, Kulbacka I, Kjos SL, Dudenhausen J, Vetter K, et al. Maternal lipids as strong determinants of fetal environment and growth in pregnancies with gestational diabetes mellitus. Diabetes Care. 2008;31(9):1858–63.CrossRefPubMedPubMedCentral
48.
go back to reference Herrera E. Lipid metabolism in pregnancy and its consequences in the fetus and newborn. Endocrine. 2002;19(1):43–55.CrossRefPubMed Herrera E. Lipid metabolism in pregnancy and its consequences in the fetus and newborn. Endocrine. 2002;19(1):43–55.CrossRefPubMed
50.
go back to reference Wilkinson AL, Pedersen SH, Urassa M, Michael D, Andreasen A, Todd J, et al. Maternal systemic or cord blood inflammation is associated with birth anthropometry in a Tanzanian prospective cohort. Trop Med Int Health. 2017;22(1):52–62.CrossRefPubMed Wilkinson AL, Pedersen SH, Urassa M, Michael D, Andreasen A, Todd J, et al. Maternal systemic or cord blood inflammation is associated with birth anthropometry in a Tanzanian prospective cohort. Trop Med Int Health. 2017;22(1):52–62.CrossRefPubMed
51.
go back to reference Hasan SMT, Khan MA, Ahmed T. Inadequate maternal weight gain in the third trimester increases the risk of intrauterine growth restriction in rural Bangladesh. PloS one. 2019;14(2):e0212116-e.CrossRef Hasan SMT, Khan MA, Ahmed T. Inadequate maternal weight gain in the third trimester increases the risk of intrauterine growth restriction in rural Bangladesh. PloS one. 2019;14(2):e0212116-e.CrossRef
52.
go back to reference Verkauskiene R, Beltrand J, Claris O, Chevenne D, Deghmoun S, Dorgeret S, et al. Impact of fetal growth restriction on body composition and hormonal status at birth in infants of small and appropriate weight for gestational age. Eur J Endocrinol. 2007;157(5):605–12.CrossRefPubMed Verkauskiene R, Beltrand J, Claris O, Chevenne D, Deghmoun S, Dorgeret S, et al. Impact of fetal growth restriction on body composition and hormonal status at birth in infants of small and appropriate weight for gestational age. Eur J Endocrinol. 2007;157(5):605–12.CrossRefPubMed
53.
go back to reference Larsson A, Ottosson P, Törnqvist C, Olhager E. Body composition and growth in full-term small for gestational age and large for gestational age Swedish infants assessed with air displacement plethysmography at birth and at 3-4 months of age. PLoS One. 2019;14(5):e0207978. https://doi.org/10.1371/journal.pone.0207978. Larsson A, Ottosson P, Törnqvist C, Olhager E. Body composition and growth in full-term small for gestational age and large for gestational age Swedish infants assessed with air displacement plethysmography at birth and at 3-4 months of age. PLoS One. 2019;14(5):e0207978. https://​doi.​org/​10.​1371/​journal.​pone.​0207978.
Metadata
Title
Maternal plasma lipid levels across pregnancy and the risks of small-for-gestational age and low birth weight: a cohort study from rural Gambia
Authors
Sandra G. Okala
Ebrima A. Sise
Fatou Sosseh
Andrew M. Prentice
Laura A. Woollett
Sophie E. Moore
Publication date
01-12-2020
Publisher
BioMed Central
Published in
BMC Pregnancy and Childbirth / Issue 1/2020
Electronic ISSN: 1471-2393
DOI
https://doi.org/10.1186/s12884-020-2834-1

Other articles of this Issue 1/2020

BMC Pregnancy and Childbirth 1/2020 Go to the issue