Hostname: page-component-8448b6f56d-t5pn6 Total loading time: 0 Render date: 2024-04-25T03:57:29.065Z Has data issue: false hasContentIssue false
  • English
  • Français

Cardiovascular risk factors in those born preterm – systematic review and meta-analysis

Published online by Cambridge University Press:  08 October 2020

Prabha H. Andraweera Open the ORCID record for Prabha H. Andraweera [Opens in a new window] ,
Bradley Condon ,
Gemma Collett ,
Stefania Gentilcore Open the ORCID record for Stefania Gentilcore [Opens in a new window]  and
Zohra S. Lassi
Prabha H. Andraweera*
Affiliation:
Adelaide Medical School and The Robinson Research Institute, The University of Adelaide, Adelaide, Australia
Bradley Condon
Affiliation:
Adelaide Medical School and The Robinson Research Institute, The University of Adelaide, Adelaide, Australia
Gemma Collett
Affiliation:
Adelaide Medical School and The Robinson Research Institute, The University of Adelaide, Adelaide, Australia
Stefania Gentilcore
Affiliation:
Adelaide Medical School and The Robinson Research Institute, The University of Adelaide, Adelaide, Australia
Zohra S. Lassi
Affiliation:
Adelaide Medical School and The Robinson Research Institute, The University of Adelaide, Adelaide, Australia
*
Address for correspondence: Prabha Andraweera, Discipline of Obstetrics and Gynaecology, Adelaide Medical School and The Robinson Research Institute, The University of Adelaide, Adelaide, Australia Email prabha.andraweera@adelaide.edu.au
Get access Rights & Permissions [Opens in a new window]

Abstract

Emerging evidence demonstrates a link between preterm birth (PTB) and later life cardiovascular disease (CVD). We conducted a systematic review and meta-analysis to compare conventional CVD risk factors between those born preterm and at term. PubMed, CINAHL, SCOPUS, and EMBASE databases were searched. The review protocol is registered in PROSPERO (CRD42018095005). CVD risk factors including systolic blood pressure (SBP), diastolic blood pressure (DBP), body mass index, lipid profile, blood glucose, and fasting insulin among those born preterm (<37 weeks’ gestation) were compared with those born at term (≥37 weeks’ gestation). Subgroup analyses based on gender, age, gestational at birth (<32 weeks’ gestation and <28 weeks’ gestation), and PTB associated with small for gestational age or average for gestational age were also performed. Fifty-six studies provided data on 308,987 individuals. Being born preterm was associated with 3.26 mmHg (95% confidence interval [CI] 2.08 to 4.44) higher mean SBP and 1.32 mmHg (95% CI: 0.61 to 2.04) higher mean DBP compared to being born at term. Subgroup analyses demonstrated that SBP was higher among (a) preterm compared to term groups from early adolescence until adulthood; (b) females born preterm but not among males born preterm compared to term controls; and (c) those born at <32 weeks or <28 weeks compared to term. Our meta-analyses demonstrate higher SBP and DBP among those born preterm compared to term. The difference in SBP is evident from early adolescence until adulthood.

Keywords

Pretermcardiovascular riskoffspringsystematic reviewmeta-analysis
Type
Review
Information
Journal of Developmental Origins of Health and Disease , Volume 12 , Issue 4 , August 2021 , pp. 539 - 554
Check for updates
Copyright
© The Author(s), 2020. Published by Cambridge University Press in association with International Society for Developmental Origins of Health and Disease

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

McAloon, CJ, Boylan, LM, Hamborg, T, et al. The changing face of cardiovascular disease 2000–2012: an analysis of the world health organisation global health estimates data. Int J Cardiol. 2016; 224, 256–264.CrossRefGoogle ScholarPubMed
Blackmore, HL, Ozanne, SE. Programming of cardiovascular disease across the life-course. J Mol Cell Cardiol. 2015;83:122–130.CrossRefGoogle ScholarPubMed
Purisch, SE, Gyamfi-Bannerman, C. Epidemiology of preterm birth. Semin Perinatol. 2017;41(7):387–391.CrossRefGoogle ScholarPubMed
Kajantie, E, Hovi, P. Is very preterm birth a risk factor for adult cardiometabolic disease? Semin Fetal Neonatal Med. 2014; 19(2), 112–117.CrossRefGoogle ScholarPubMed
Saigal, S, Doyle, LW. An overview of mortality and sequelae of preterm birth from infancy to adulthood. Lancet. 2008; 371(9608), 261–269.CrossRefGoogle Scholar
Li, S, Zhang, M, Tian, H, Liu, Z, Yin, X, Xi, B. Preterm birth and risk of type 1 and type 2 diabetes: systematic review and meta-analysis. Obes Rev. 2014; 15(10), 804–811.CrossRefGoogle ScholarPubMed
Markopoulou, P, Papanikolaou, E, Analytis, A, Zoumakis, E, Siahanidou, T. Preterm birth as a risk factor for metabolic syndrome and cardiovascular disease in adult life: a systematic review and meta-analysis. J Pediatr. 2019; 210, 69–80, e65.Google Scholar
Moher, D, Liberati, A, Tetzlaff, J, Altman, DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009; 6(7), e1000097.CrossRefGoogle ScholarPubMed
Quinn, JA, Munoz, FM, Gonik, B, et al. Preterm birth: case definition & guidelines for data collection, analysis, and presentation of immunisation safety data. Vaccine. 2016; 34(49), 6047–6056.CrossRefGoogle ScholarPubMed
Wells, GA SB, O’Connell, D, Peterson, J, Welch, V, Losos, M. Newcastle-Ottawa quality assessment scale. Ottawa Hospital Research Institute. 2013.Google Scholar
Takeshima, N, Sozu, T, Tajika, A, Ogawa, Y, Hayasaka, Y, Furukawa, TA. Which is more generalizable, powerful and interpretable in meta-analyses, mean difference or standardized mean difference? BMC Med Res Methodol. 2014; 14, 30.CrossRefGoogle ScholarPubMed
Higgins, JP, Thompson, SG, Deeks, JJ, Altman, DG. Measuring inconsistency in meta-analyses. BMJ (Clinical Research Ed). 2003; 327(7414), 557–560.CrossRefGoogle ScholarPubMed
Sterne, JA, Egger, M, Smith, GD. Systematic reviews in health care: Investigating and dealing with publication and other biases in meta-analysis. BMJ (Clinical Research Ed). 2001; 323(7304), 101–105.CrossRefGoogle ScholarPubMed
Alves, PJ, Araujo Junior, E, Henriques, AC, Carvalho, FH. Preterm at birth is not associated with greater cardiovascular risk in adolescence. J Matern Fetal Neonatal Med. 2016; 29(20), 3351–3357.Google Scholar
Barros, FC, Victora, CG. Increased blood pressure in adolescents who were small for gestational age at birth: a cohort study in Brazil. Int J Epidemiol. 1999; 28(4), 676–681.CrossRefGoogle ScholarPubMed
Bayrakci, US, Schaefer, F, Duzova, A, Yigit, S, Bakkaloglu, A. Abnormal circadian blood pressure regulation in children born preterm. J Pediatr. 2007; 151(4), 399–403.CrossRefGoogle ScholarPubMed
Bonamy, AK, Bendito, A, Martin, H, Andolf, E, Sedin, G, Norman, M. Preterm birth contributes to increased vascular resistance and higher blood pressure in adolescent girls. Pediatr Res. 2005; 58(5), 845–849.CrossRefGoogle ScholarPubMed
Bonamy, AK, Martin, H, Jorneskog, G, Norman, M. Lower skin capillary density, normal endothelial function and higher blood pressure in children born preterm. J Intern Med. 2007; 262(6), 635–642.CrossRefGoogle ScholarPubMed
Cheung, YF, Wong, KY, Lam, BC, Tsoi, NS. Relation of arterial stiffness with gestational age and birth weight. Arch Dis Child. 2004; 89(3), 217–221.CrossRefGoogle ScholarPubMed
Doyle, LW, Faber, B, Callanan, C, Morley, R. Blood pressure in late adolescence and very low birth weight. Pediatrics. 2003; 111(2), 252–257.CrossRefGoogle ScholarPubMed
Edwards, MO, Watkins, WJ, Kotecha, SJ, et al. Higher systolic blood pressure with normal vascular function measurements in preterm-born children. Acta Paediatr (Oslo, Norway: 1992). 2014; 103(9), 904–912.CrossRefGoogle ScholarPubMed
Evensen, KA, Steinshamn, S, Tjonna, AE, et al. Effects of preterm birth and fetal growth retardation on cardiovascular risk factors in young adulthood. Early Hum Dev. 2009; 85(4), 239–245.CrossRefGoogle ScholarPubMed
Hack, M, Schluchter, M, Cartar, L, Rahman, M. Blood pressure among very low birth weight (<1.5 kg) young adults. Pediatr Res. 2005; 58(4), 677–684.CrossRefGoogle ScholarPubMed
Hovi, P, Andersson, S, Raikkonen, K, et al. Ambulatory blood pressure in young adults with very low birth weight. J Pediatr. 2010; 156(1), 54–59, e51.CrossRefGoogle ScholarPubMed
Irving, RJ, Belton, NR, Elton, RA, Walker, BR. Adult cardiovascular risk factors in premature babies. Lancet. 2000; 355(9221), 2135–2136.CrossRefGoogle ScholarPubMed
Jarvelin, MR, Sovio, U, King, V, et al. Early life factors and blood pressure at age 31 years in the 1966 northern Finland birth cohort. Hypertension. 2004; 44(6), 838–846.CrossRefGoogle ScholarPubMed
Johansson, S, Iliadou, A, Bergvall, N, Tuvemo, T, Norman, M, Cnattingius, S. Risk of high blood pressure among young men increases with the degree of immaturity at birth. Circulation. 2005; 112(22), 3430–3436.CrossRefGoogle ScholarPubMed
Joshi, S, Wilson, DG, Kotecha, S, Pickerd, N, Fraser, AG, Kotecha, S. Cardiovascular function in children who had chronic lung disease of prematurity. Arch Dis Child Fetal Neonatal Ed. 2014; 99(5), F373–F379.CrossRefGoogle ScholarPubMed
Keijzer-Veen, MG, Dulger, A, Dekker, FW, Nauta, J, van der Heijden, BJ. Very preterm birth is a risk factor for increased systolic blood pressure at a young adult age. Pediatr Nephrol (Berlin, Germany). 2010; 25(3), 509–516.CrossRefGoogle Scholar
Kistner, A, Celsi, G, Vanpee, M, Jacobson, SH. Increased blood pressure but normal renal function in adult women born preterm. Pediatr Nephrol (Berlin, Germany). 2000; 15(3–4), 215–220.CrossRefGoogle ScholarPubMed
Kowalski, RR, Beare, R, Doyle, LW, Smolich, JJ, Cheung, MM. Elevated blood pressure with reduced left ventricular and aortic dimensions in adolescents born extremely preterm. J Pediatr. 2016; 172, 75–80, e72.CrossRefGoogle ScholarPubMed
Lewandowski, AJ, Davis, EF, Yu, G, et al. Elevated blood pressure in preterm-born offspring associates with a distinct antiangiogenic state and microvascular abnormalities in adult life. Hypertension. 2015; 65(3), 607–614.CrossRefGoogle ScholarPubMed
McEniery, CM, Bolton, CE, Fawke, J, et al. Cardiovascular consequences of extreme prematurity: the EPICure study. J Hypertens. 2011; 29(7), 1367–1373.CrossRefGoogle ScholarPubMed
Mohlkert, LA, Hallberg, J, Broberg, O, et al. Preterm arteries in childhood: dimensions, intima-media thickness, and elasticity of the aorta, coronaries, and carotids in 6-y-old children born extremely preterm. Pediatr Res. 2017; 81(2), 299–306.CrossRefGoogle ScholarPubMed
Morsing, E, Liuba, P, Fellman, V, Marsal, K, Brodszki, J. Cardiovascular function in children born very preterm after intrauterine growth restriction with severely abnormal umbilical artery blood flow. Eur J Prev Cardiol. 2014; 21(10), 1257–1266.CrossRefGoogle ScholarPubMed
Ramirez-Velez, R, Correa-Bautista, JE, Villa-Gonzalez, E, Martinez-Torres, J, Hackney, AC, Garcia-Hermoso, A. Effects of preterm birth and fetal growth retardation on life-course cardiovascular risk factors among schoolchildren from Colombia: the FUPRECOL study. Early Hum Dev. 2017; 106–107, 53–58.CrossRefGoogle ScholarPubMed
Schubert, U, Muller, M, Abdul-Khaliq, H, Norman, M, Bonamy, AK. Relative intima-media thickening after preterm birth. Acta Paediatr (Oslo, Norway: 1992). 2013; 102(10), 965–969.CrossRefGoogle ScholarPubMed
Singhal, A, Kattenhorn, M, Cole, TJ, Deanfield, J, Lucas, A. Preterm birth, vascular function, and risk factors for atherosclerosis. Lancet. 2001; 358(9288), 1159–1160.CrossRefGoogle ScholarPubMed
Skilton, MR, Viikari, JS, Juonala, M, et al. Fetal growth and preterm birth influence cardiovascular risk factors and arterial health in young adults: the Cardiovascular Risk in Young Finns Study. Arterioscler Thromb Vasc Biol. 2011; 31(12), 2975–2981.CrossRefGoogle ScholarPubMed
Steen, E, Bonamy, AK, Norman, M, Hellstrom-Westas, L. Preterm birth may be a larger risk factor for increased blood pressure than intrauterine growth restriction. Acta Paediatr (Oslo, Norway: 1992). 2015; 104(11), 1098–1103.CrossRefGoogle ScholarPubMed
Tauzin, L, Rossi, P, Grosse, C, et al. Increased systemic blood pressure and arterial stiffness in young adults born prematurely. J Dev Orig Health Dis. 2014; 5(6), 448–452.CrossRefGoogle ScholarPubMed
Thomas, EL, Parkinson, JR, Hyde, MJ, et al. Aberrant adiposity and ectopic lipid deposition characterize the adult phenotype of the preterm infant. Pediatr Res. 2011; 70(5), 507–512.CrossRefGoogle ScholarPubMed
Vohr, BR, Allan, W, Katz, KH, Schneider, KC, Ment, LR. Early predictors of hypertension in prematurely born adolescents. Acta Paediatr (Oslo, Norway: 1992). 2010; 99(12), 1812–1818.CrossRefGoogle ScholarPubMed
Vollsaeter, M, Halvorsen, T, Markestad, T, et al. Renal function and blood pressure in 11 year old children born extremely preterm or small for gestational age. PLoS One. 2018; 13(10), e0205558.CrossRefGoogle ScholarPubMed
Chan, PY, Morris, JM, Leslie, GI, Kelly, PJ, Gallery, ED. The long-term effects of prematurity and intrauterine growth restriction on cardiovascular, renal, and metabolic function. International J Pediatr. 2010; 2010, 280402.CrossRefGoogle ScholarPubMed
Cooper, R, Atherton, K, Power, C. Gestational age and risk factors for cardiovascular disease: evidence from the 1958 British birth cohort followed to mid-life. Int J Epidemiol. 2009; 38(1), 235–244.CrossRefGoogle ScholarPubMed
Hovi, P, Vohr, B, Ment, LR, et al. Blood pressure in young adults born at very low birth weight: adults born preterm international collaboration. Hypertension. 2016; 68(4), 880–887.CrossRefGoogle ScholarPubMed
Lee, H, Dichtl, S, Mormanova, Z, Pozza, RD, Genzel-Boroviczeny, O. In adolescence, extreme prematurity is associated with significant changes in the microvasculature, elevated blood pressure and increased carotid intima-media thickness. Arch Dis Child. 2014; 99(10), 907–911.CrossRefGoogle ScholarPubMed
Bassareo, PP, Fanos, V, Puddu, M, et al. Reduced brachial flow-mediated vasodilation in young adult ex extremely low birth weight preterm: a condition predictive of increased cardiovascular risk? J Matern-Fetal Neonatal Med. 2010; 23(Suppl 3), 121–124.CrossRefGoogle ScholarPubMed
Gianni, ML, Roggero, P, Piemontese, P, et al. Boys who are born preterm show a relative lack of fat-free mass at 5 years of age compared to their peers. Acta Paediatr (Oslo, Norway: 1992). 2015; 104(3), e119–123.CrossRefGoogle ScholarPubMed
Hack, M, Schluchter, M, Cartar, L, Rahman, M, Cuttler, L, Borawski, E. Growth of very low birth weight infants to age 20 years. Pediatrics. 2003; 112(1 Pt 1), e30–38.CrossRefGoogle ScholarPubMed
Huke, V, Rudloff, S, Brugger, M, Strauch, K, Berthold, LD, Landmann, E. Prematurity is not associated with intra-abdominal adiposity in 5- to 7-year-old children. J Pediatr. 2013; 163(5), 1301–1306.CrossRefGoogle Scholar
Mathai, S, Derraik, JG, Cutfield, WS, et al. Increased adiposity in adults born preterm and their children. PLoS One. 2013; 8(11), e81840.CrossRefGoogle ScholarPubMed
Oren, A, Vos, LE, Bos, WJ, et al. Gestational age and birth weight in relation to aortic stiffness in healthy young adults: two separate mechanisms? Am J Hypertens. 2003; 16(1), 76–79.CrossRefGoogle ScholarPubMed
Saigal, S, Stoskopf, B, Streiner, D, Paneth, N, Pinelli, J, Boyle, M. Growth trajectories of extremely low birth weight infants from birth to young adulthood: a longitudinal, population-based study. Pediatr Res. 2006; 60(6), 751–758.CrossRefGoogle ScholarPubMed
Shimizu, T, Fujii, T, Iwasaki, J, et al. Abdominal aortic intima-media thickness in preschool children born preterm. Pediatr Cardiol. 2014; 35(1), 121–125.CrossRefGoogle ScholarPubMed
Darendeliler, F, Bas, F, Bundak, R, et al. Insulin resistance and body composition in preterm born children during prepubertal ages. Clin Endocrinol (Oxf). 2008; 68(5), 773–779.CrossRefGoogle ScholarPubMed
Hui, LL, Lam, HS, Leung, GM, Schooling, CM. Late prematurity and adiposity in adolescents: evidence from “Children of 1997” birth cohort. Obesity (Silver Spring, Md). 2015; 23(11), 2309–2314.CrossRefGoogle ScholarPubMed
Hovi, P, Turanlahti, M, Strang-Karlsson, S, et al. Intima-media thickness and flow-mediated dilatation in the Helsinki study of very low birth weight adults. Pediatrics. 2011; 127(2), e304–311.CrossRefGoogle ScholarPubMed
Kajantie, E, Strang-Karlsson, S, Hovi, P, et al. Insulin sensitivity and secretory response in adults born preterm: the Helsinki Study of Very Low Birth Weight Adults. J Clin Endocrinol Metab. 2015; 100(1), 244–250.CrossRefGoogle ScholarPubMed
Hofman, PL, Regan, F, Jackson, WE, et al. Premature birth and later insulin resistance. N Eng J Med. 2004; 351(21), 2179–2186.CrossRefGoogle ScholarPubMed
Lewington, S, Clarke, R, Qizilbash, N, Peto, R, Collins, R. Age-specific relevance of usual blood pressure to vascular mortality: a meta-analysis of individual data for one million adults in 61 prospective studies. Lancet. 2002; 360(9349), 1903–1913.Google ScholarPubMed
Chen, X, Wang, Y. Tracking of blood pressure from childhood to adulthood: a systematic review and meta-regression analysis. Circulation. 2008; 117(25), 3171–3180.CrossRefGoogle ScholarPubMed
Li, S, Xi, B. Preterm birth is associated with risk of essential hypertension in later life. Int J Cardiol. 2014; 172(2), e361–363.CrossRefGoogle ScholarPubMed
de Jong, F, Monuteaux, MC, van Elburg, RM, Gillman, MW, Belfort, MB. Systematic review and meta-analysis of preterm birth and later systolic blood pressure. Hypertension. 2012; 59(2), 226–234.CrossRefGoogle ScholarPubMed
Murphy, MO, Cohn, DM, Loria, AS. Developmental origins of cardiovascular disease: impact of early life stress in humans and rodents. Neurosci Biobehav Rev. 2017; 74(Pt B), 453–465.CrossRefGoogle ScholarPubMed
Andraweera, PH, Lassi, ZS. Cardiovascular risk factors in offspring of preeclamptic pregnancies-systematic review and meta-analysis. J Pediatr. 2019; 208, 104–113, e106.CrossRefGoogle ScholarPubMed
Pathirana, MM, Lassi, ZS, Roberts, CT, Andraweera, PH. Cardiovascular risk factors in offspring exposed to gestational diabetes mellitus in utero: systematic review and meta-analysis. J Dev Orig Health Dis. 2020, 1–18. doi: 10.1017/S2040174419000850. Epub ahead of print.CrossRefGoogle Scholar
Luyckx, VA, Bertram, JF, Brenner, BM, et al. Effect of fetal and child health on kidney development and long-term risk of hypertension and kidney disease. Lancet. 2013; 382(9888), 273–283.CrossRefGoogle ScholarPubMed
Clark, RH, Thomas, P, Peabody, J. Extrauterine growth restriction remains a serious problem in prematurely born neonates. Pediatrics. 2003; 111(5 Pt 1), 986–990.CrossRefGoogle ScholarPubMed
Singhal, A, Cole, TJ, Lucas, A. Early nutrition in preterm infants and later blood pressure: two cohorts after randomised trials. Lancet. 2001; 357(9254), 413–419.CrossRefGoogle ScholarPubMed
Crump, C, Howell, EA, Stroustrup, A, McLaughlin, MA, Sundquist, J, Sundquist, K. Association of preterm birth with risk of ischemic heart disease in adulthood. JAMA Pediatr. 2019; 173(8), 736–743.CrossRefGoogle ScholarPubMed
Cohen, G, Lagercrantz, H, Katz-Salamon, M. Abnormal circulatory stress responses of preterm graduates. Pediatric research. 2007; 61(3), 329–334.CrossRefGoogle ScholarPubMed
Dalziel, SR, Parag, V, Rodgers, A, Harding, JE. Cardiovascular risk factors at age 30 following pre-term birth. Int J Epidemiol. 2007; 36(4), 907–915.CrossRefGoogle ScholarPubMed
Farooqi, A, Hagglof, B, Sedin, G, Gothefors, L, Serenius, F. Growth in 10- to 12-year-old children born at 23 to 25 weeks’ gestation in the 1990s: a Swedish national prospective follow-up study. Pediatrics. 2006; 118(5), e1452–1465.CrossRefGoogle ScholarPubMed
Fewtrell, MS, Lucas, A, Cole, TJ, Wells, JC. Prematurity and reduced body fatness at 8–12 y of age. Am J Clin Nutr. 2004; 80(2), 436–440.CrossRefGoogle ScholarPubMed
Lewandowski, AJ, Lazdam, M, Davis, E, et al. Short-term exposure to exogenous lipids in premature infants and long-term changes in aortic and cardiac function. Arterioscler Thromb Vasc Biol. 2011; 31(9), 2125–2135.CrossRefGoogle ScholarPubMed
Singhal, A, Fewtrell, M, Cole, TJ, Lucas, A. Low nutrient intake and early growth for later insulin resistance in adolescents born preterm. Lancet. 2003; 361(9363), 1089–1097.CrossRefGoogle ScholarPubMed
Goldani, MZ, Haeffner, LS, Agranonik, M, Barbieri, MA, Bettiol, H, Silva, AA. Do early life factors influence body mass index in adolescents? Braz J Med Biol Res. 2007; 40(9), 1231–1236.CrossRefGoogle ScholarPubMed
Gunay, F, Alpay, H, Gokce, I, Bilgen, H. Is late-preterm birth a risk factor for hypertension in childhood? Eur J Pediatr. 2014; 173(6), 751–756.CrossRefGoogle ScholarPubMed
Hovi, P, Andersson, S, Eriksson, JG, et al. Glucose regulation in young adults with very low birth weight. N Eng J Med. 2007; 356(20), 2053–2063.CrossRefGoogle ScholarPubMed
Kaijser, M, Bonamy, AK, Akre, O, et al. Perinatal risk factors for diabetes in later life. Diabetes. 2009; 58(3), 523–526.CrossRefGoogle ScholarPubMed
Rotteveel, J, van Weissenbruch, MM, Twisk, JW, Delemarre-Van de Waal, HA. Infant and childhood growth patterns, insulin sensitivity, and blood pressure in prematurely born young adults. Pediatrics. 2008; 122(2), 313–321.CrossRefGoogle ScholarPubMed
Rotteveel, J, van Weissenbruch, MM, Twisk, JW, Delemarre-Van de Waal, HA. Insulin sensitivity in prematurely born adults: relation to preterm growth restraint. Horm Res Paediatr. 2011; 75(4), 252–257.CrossRefGoogle ScholarPubMed
Kistner, A, Jacobson, SH, Celsi, G, Vanpee, M, Brismar, K. IGFBP-1 levels in adult women born small for gestational age suggest insulin resistance in spite of normal BMI. J Int Med. 2004; 255(1), 82–88.CrossRefGoogle ScholarPubMed
Kwinta, P, Klimek, M, Drozdz, D, et al. Assessment of long-term renal complications in extremely low birth weight children. Pediatr Nephrol (Berlin, Germany). 2011; 26(7), 1095–1103.CrossRefGoogle ScholarPubMed
Lazdam, M, de la Horra, A, Pitcher, A, et al. Elevated blood pressure in offspring born premature to hypertensive pregnancy: is endothelial dysfunction the underlying vascular mechanism? Hypertension. 2010; 56(1), 159–165.CrossRefGoogle ScholarPubMed
Bolton, CE, Stocks, J, Hennessy, E, et al. The EPICure study: association between hemodynamics and lung function at 11 years after extremely preterm birth. J Pediatr. 2012; 161(4), 595–601, e592.CrossRefGoogle ScholarPubMed
Bracewell, MA, Hennessy, EM, Wolke, D, Marlow, N. The EPICure study: growth and blood pressure at 6 years of age following extremely preterm birth. Arch Dis Child Fetal Neonatal Ed. 2008; 93(2), F108–114.CrossRefGoogle ScholarPubMed
Mikkola, K, Leipala, J, Boldt, T, Fellman, V. Fetal growth restriction in preterm infants and cardiovascular function at five years of age. J Pediatr. 2007; 151(5), 494–499,, e491–492.CrossRefGoogle ScholarPubMed
Bonamy, AK, Kallen, K, Norman, M. High blood pressure in 2.5-year-old children born extremely preterm. Pediatrics. 2012; 129(5), e1199–1204.CrossRefGoogle ScholarPubMed
Pilgaard, K, Faerch, K, Carstensen, B, et al. Low birthweight and premature birth are both associated with type 2 diabetes in a random sample of middle-aged Danes. Diabetologia. 2010; 53(12), 2526–2530.CrossRefGoogle Scholar
Rossi, P, Tauzin, L, Marchand, E, Boussuges, A, Gaudart, J, Frances, Y. Respective roles of preterm birth and fetal growth restriction in blood pressure and arterial stiffness in adolescence. J Adolesc Health. 2011; 48(5), 520–522.CrossRefGoogle ScholarPubMed
Sipola-Leppanen, M, Vaarasmaki, M, Tikanmaki, M, et al. Cardiovascular risk factors in adolescents born preterm. Pediatrics. 2014; 134(4), e1072–1081.CrossRefGoogle ScholarPubMed
Sipola-Leppanen, M, Vaarasmaki, M, Tikanmaki, M, et al. Cardiometabolic risk factors in young adults who were born preterm. Am J Epidemiol. 2015; 181(11), 861–873.CrossRefGoogle ScholarPubMed
Hussain, SM, Kahonen, M, Raitakari, OT, et al. Impact of fetal growth and preterm birth on the retinal microvasculature in mid-adulthood. Microcirculation (New York, NY: 1994). 2015; 22(4), 285–293.CrossRefGoogle ScholarPubMed
Juonala, M, Cheung, MM, Sabin, MA, et al. Effect of birth weight on life-course blood pressure levels among children born premature: the Cardiovascular Risk in Young Finns Study. J Hyperten. 2015; 33(8), 1542–1548.CrossRefGoogle ScholarPubMed
Toumba, M, Hadjidemetriou, A, Topouzi, M, et al. Evaluation of the auxological and metabolic status in prepubertal children born small for gestational age. J Pediatr Endocrinol Metab. 2005; 18(7), 677–688.CrossRefGoogle ScholarPubMed
Supplementary material: File

Andraweera et al. Supplementary Materials

Andraweera et al. Supplementary Materials 1

Download Andraweera et al. Supplementary Materials(File)
File 247.4 KB
Supplementary material: File

Andraweera et al. Supplementary Materials

Andraweera et al. Supplementary Materials 2

Download Andraweera et al. Supplementary Materials(File)
File 65 KB