Hostname: page-component-cc8bf7c57-qfg88 Total loading time: 0 Render date: 2024-12-12T05:10:01.440Z Has data issue: false hasContentIssue false

Hypertensive disorders during pregnancy and health outcomes in the offspring: a systematic review

Published online by Cambridge University Press:  11 May 2016

T. V. Pinheiro*
Affiliation:
Saúde da Criança e do Adolescente, Universidade Federal do Rio Grande do Sul, Brazil
S. Brunetto
Affiliation:
Saúde da Criança e do Adolescente, Universidade Federal do Rio Grande do Sul, Brazil
J. G. L. Ramos
Affiliation:
Department of Gynecology and Obstetrics, Universidade Federal do Rio Grande do Sul, Brazil
J. R. Bernardi
Affiliation:
Saúde da Criança e do Adolescente, Universidade Federal do Rio Grande do Sul, Brazil
M. Z. Goldani
Affiliation:
Saúde da Criança e do Adolescente, Universidade Federal do Rio Grande do Sul, Brazil Department of Pediatrics, Universidade Federal do Rio Grande do Sul, Brazil
*
*Address for correspondence: T. V. Pinheiro, Department of Paediatrics, Universidade Federal do Rio Grande do Sul, R. Ramiro Barcelos, 2350 – Santa Cecilia, Porto Alegre, Rio Grande do Sul 90035-903, Brazil. (Email tanaravogel@gmail.com)

Abstract

The hypertensive disorders of pregnancy complicate up to 10% of pregnancies worldwide and are a leading cause of maternal, foetal, and neonatal morbidity and mortality. The aim of this study was to present an overview of recent studies addressing offspring’s medium and long-term health outcomes after intrauterine exposure to maternal hypertension. A search on PubMed/MEDLINE and Bireme databases was conducted to identify observational studies that reported any offspring outcome measured after the 6th month of life. The search was limited to studies published after May 2008. Forty-five articles were included and categorized into four groups of outcomes: cardiovascular, immune, metabolic and behavioural/neurological effects. According to our findings, hypertensive disorders of pregnancy had an overall negative impact on offspring’s cardiovascular, immune and neurological health, although not all parameters analysed in each group had consistent results among studies. The most prominent and reliable associations were verified between gestational hypertension and higher offspring’s blood pressure and between preeclampsia and offspring’s lower cognitive functioning. In the metabolic outcomes, body composition had conflicting results among papers, while all studies that examined blood biomarkers showed no evidence that preeclampsia or gestational hypertension could be associated with an alteration of this metabolic outcomes. Most included studies were highly heterogeneous regarding the measure of outcomes and covariables used for adjustments. Future studies should consider using the same protocols and cut-off points already published so that results can be better compared and summarized.

This review was registered in PROSPERO. Registration number: CRD42015020838

Type
Review
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2016 

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

1. Barker, DJ, Winter, PD, Osmond, C, Margetts, B, Simmonds, SJ. Weight in infancy and death from ischaemic heart disease. Lancet. 1989; 2, 577580.Google Scholar
2. Barker, DJ, Osmond, C, Forsen, TJ, Kajantie, E, Eriksson, JG. Trajectories of growth among children who have coronary events as adults. N Engl J Med. 2005; 353, 18021809.CrossRefGoogle ScholarPubMed
3. Roberts, JM, August, PA, Bakris, G, et al. Hypertension in pregnancy. Report of the American College of Obstetricians and Gynecologists’ task force on hypertension in pregnancy. Obstet Gynecol. 2013; 122, 11221131.Google Scholar
4. Rugolo, LMSdS, Bentlin, MR, Trindade, CEP, et al. Effect on the fetus and newborn. NeoReviews. 2011; 12, 198206.CrossRefGoogle Scholar
5. Brown, MA, Lindheimer, MD, de Swiet, M, Van Assche, A, Moutquin, JM. The classification and diagnosis of the hypertensive disorders of pregnancy: statement from the International Society for the Study of Hypertension in Pregnancy (ISSHP). Hypertens Pregnancy. 2001; 20, 914.CrossRefGoogle Scholar
6. Ip, S, Chung, M, Raman, G, et al. Breastfeeding and maternal and infant health outcomes in developed countries. Evid Rep Technol Assess (Full Rep). 2007; 153, 1186.Google Scholar
7. Ehrenstein, V, Rothman, KJ, Pedersen, L, Hatch, EE, Sorensen, HT. Pregnancy-associated hypertensive disorders and adult cognitive function among Danish conscripts. Am J Epidemiol. 2009; 170, 10251031.CrossRefGoogle ScholarPubMed
8. Kajantie, E, Eriksson, JG, Osmond, C, Thornburg, K, Barker, DJ. Pre-eclampsia is associated with increased risk of stroke in the adult offspring: the Helsinki birth cohort study. Stroke. 2009; 40, 11761180.Google Scholar
9. Geelhoed, JJ, Fraser, A, Tilling, K, et al. Preeclampsia and gestational hypertension are associated with childhood blood pressure independently of family adiposity measures: the Avon Longitudinal Study of Parents and Children. Circulation. 2010; 122, 11921199.CrossRefGoogle ScholarPubMed
10. Lawlor, DA, Macdonald-Wallis, C, Fraser, A, et al. Cardiovascular biomarkers and vascular function during childhood in the offspring of mothers with hypertensive disorders of pregnancy: findings from the Avon Longitudinal Study of Parents and Children. Eur Heart J. 2012; 33, 335345.Google Scholar
11. Fraser, A, Nelson, SM, Macdonald-Wallis, C, Sattar, N, Lawlor, DA. Hypertensive disorders of pregnancy and cardiometabolic health in adolescent offspring. Hypertension. 2013; 62, 614620.CrossRefGoogle ScholarPubMed
12. Miettola, S, Hartikainen, AL, Vaarasmaki, M, et al. Offspring’s blood pressure and metabolic phenotype after exposure to gestational hypertension in utero. Eur J Epidemiol. 2013; 28, 8798.CrossRefGoogle ScholarPubMed
13. 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, 159165.Google Scholar
14. Palmsten, K, Buka, SL, Michels, KB. Maternal pregnancy-related hypertension and risk for hypertension in offspring later in life. Obstet Gynecol. 2010; 116, 858864.Google Scholar
15. Mamun, AA, Kinarivala, MK, O’Callaghan, M, et al. Does hypertensive disorder of pregnancy predict offspring blood pressure at 21 years? Evidence from a birth cohort study. J Hum Hypertens. 2012; 26, 288294.Google Scholar
16. Oglaend, B, Forman, MR, Romundstad, PR, Nilsen, ST, Vatten, LJ. Blood pressure in early adolescence in the offspring of preeclamptic and normotensive pregnancies. J Hypertens. 2009; 27, 20512054.CrossRefGoogle ScholarPubMed
17. Lazdam, M, de la Horra, A, Diesch, J, et al. Unique blood pressure characteristics in mother and offspring after early onset preeclampsia. Hypertension. 2012; 60, 13381345.Google Scholar
18. Fugelseth, D, Ramstad, HB, Kvehaugen, AS, et al. Myocardial function in offspring 5-8 years after pregnancy complicated by preeclampsia. Early Hum Dev. 2011; 87, 531535.CrossRefGoogle ScholarPubMed
19. Jayet, PY, Rimoldi, SF, Stuber, T, et al. Pulmonary and systemic vascular dysfunction in young offspring of mothers with preeclampsia. Circulation. 2010; 122, 488494.Google Scholar
20. Keski-Nisula, L, Heinonen, S, Remes, S, Pekkanen, J. Pre-eclampsia, placental abruption and increased risk of atopic sensitization in male adolescent offspring. Am J Reprod Immunol. 2009; 62, 293300.CrossRefGoogle ScholarPubMed
21. Byberg, KK, Ogland, B, Eide, GE, Oymar, K. Birth after preeclamptic pregnancies: association with allergic sensitization and allergic rhinoconjunctivitis in late childhood; a historically matched cohort study. BMC Pediatr. 2014; 14, 101.Google Scholar
22. Wu, CS, Nohr, EA, Bech, BH, et al. Health of children born to mothers who had preeclampsia: a population-based cohort study. Am J Obstet Gynecol. 2009; 201, 269 e1269 e10.Google Scholar
23. Liu, X, Olsen, J, Agerbo, E, et al. Maternal preeclampsia and childhood asthma in the offspring. Pediatr Allergy Immunol. 2015; 26, 181185.Google Scholar
24. Kulak, W, Sobaniec, W, Okurowska-Zawada, B, Sienkiewicz, D, Paszko-Patej, G. Antenatal, intrapartum and neonatal risk factors for cerebral palsy in children in Podlaskie Province. Neurologia Dziecięca. 2009; 18, 1924.Google Scholar
25. Kulak, W, Okurowska-Zawada, B, Sienkiewicz, D, Paszko-Patej, G, Krajewska-Kulak, E. Risk factors for cerebral palsy in term birth infants. Adv Med Sci. 2010; 55, 216221.Google Scholar
26. Strand, KM, Heimstad, R, Iversen, AC, et al. Mediators of the association between pre-eclampsia and cerebral palsy: population based cohort study. BMJ. 2013; 347, f4089.CrossRefGoogle ScholarPubMed
27. Mann, JR, McDermott, S, Griffith, MI, Hardin, J, Gregg, A. Uncovering the complex relationship between pre-eclampsia, preterm birth and cerebral palsy. Paediatr Perinat Epidemiol. 2011; 25, 100110.Google Scholar
28. Tronnes, H, Wilcox, AJ, Lie, RT, Markestad, T, Moster, D. Risk of cerebral palsy in relation to pregnancy disorders and preterm birth: a national cohort study. Dev Med Child Neurol. 2014; 56, 779785.Google Scholar
29. Beaino, G, Khoshnood, B, Kaminski, M, et al. Predictors of cerebral palsy in very preterm infants: the EPIPAGE prospective population-based cohort study. Dev Med Child Neurol. 2010; 52, e119e125.Google Scholar
30. Tuovinen, S, Raikkonen, K, Kajantie, E, et al. Hypertensive disorders in pregnancy and intellectual abilities in the offspring in young adulthood: the Helsinki Birth Cohort Study. Ann Med. 2012; 44, 394403.CrossRefGoogle ScholarPubMed
31. Tuovinen, S, Raikkonen, K, Kajantie, E, et al. Hypertensive disorders in pregnancy and cognitive decline in the offspring up to old age. Neurology. 2012; 79, 15781582.Google Scholar
32. Tuovinen, S, Eriksson, JG, Kajantie, E, et al. Maternal hypertensive disorders in pregnancy and self-reported cognitive impairment of the offspring 70 years later: the Helsinki Birth Cohort Study. Am J Obstet Gynecol. 2013; 208, 200.e1200.e9.Google Scholar
33. Morsing, E, Marsal, K. Pre-eclampsia- an additional risk factor for cognitive impairment at school age after intrauterine growth restriction and very preterm birth. Early Hum Dev. 2014; 90, 99101.CrossRefGoogle ScholarPubMed
34. van Wassenaer, AG, Westera, J, van Schie, PE, et al. Outcome at 4.5 years of children born after expectant management of early-onset hypertensive disorders of pregnancy. Am J Obstet Gynecol. 2011; 204, 510.e1510.e9.Google Scholar
35. Whitehouse, AJ, Robinson, M, Newnham, JP, Pennell, CE. Do hypertensive diseases of pregnancy disrupt neurocognitive development in offspring? Paediatr Perinat Epidemiol. 2012; 26, 101108.Google Scholar
36. Heikura, U, Hartikainen, AL, Nordstrom, T, et al. Maternal hypertensive disorders during pregnancy and mild cognitive limitations in the offspring. Paediatr Perinat Epidemiol. 2013; 27, 188198.Google Scholar
37. Tuovinen, S, Raikkonen, K, Kajantie, E, et al. Depressive symptoms in adulthood and intrauterine exposure to pre-eclampsia: the Helsinki Birth Cohort Study. BJOG. 2010; 117, 12361242.Google Scholar
38. Tuovinen, S, Raikkonen, K, Pesonen, AK, et al. Hypertensive disorders in pregnancy and risk of severe mental disorders in the offspring in adulthood: the Helsinki Birth Cohort Study. J Psychiatr Res. 2012; 46, 303310.Google Scholar
39. Tuovinen, S, Aalto-Viljakainen, T, Eriksson, JG, et al. Maternal hypertensive disorders during pregnancy: adaptive functioning and psychiatric and psychological problems of the older offspring. BJOG. 2014; 121, 14821491.CrossRefGoogle ScholarPubMed
40. Wade, M, Jenkins, JM. Pregnancy hypertension and the risk for neuropsychological difficulties across early development: a brief report. Child Neuropsychol. 2014; 22, 18.Google ScholarPubMed
41. Robinson, M, Mattes, E, Oddy, WH, et al. Hypertensive diseases of pregnancy and the development of behavioral problems in childhood and adolescence: the Western Australian Pregnancy Cohort Study. J Pediatr. 2009; 154, 218224.Google Scholar
42. Robinson, M, Oddy, WH, Whitehouse, AJ, et al. Hypertensive diseases of pregnancy predict parent-reported difficult temperament in infancy. J Dev Behav Pediatr. 2013; 34, 174180.CrossRefGoogle ScholarPubMed
43. Mann, JR, McDermott, S. Maternal pre-eclampsia is associated with childhood epilepsy in South Carolina children insured by Medicaid. Epilepsy Behav. 2011; 20, 506511.Google Scholar
44. Grace, T, Bulsara, M, Pennell, C, Hands, B. Maternal hypertensive diseases negatively affect offspring motor development. Pregnancy Hypertens. 2014; 4, 209214.Google Scholar
45. Miettola, S, Hovi, P, Andersson, S, et al. Maternal preeclampsia and bone mineral density of the adult offspring. Am J Obstet Gynecol. 2013; 209, 443 e1443 e10.Google Scholar
46. Kvehaugen, AS, Andersen, LF, Staff, AC. Anthropometry and cardiovascular risk factors in women and offspring after pregnancies complicated by preeclampsia or diabetes mellitus. Acta Obstet Gynecol Scand. 2010; 89, 14781485.Google Scholar
47. Washburn, L, Nixon, P, Russell, G, Snively, BM, O’Shea, TM. Adiposity in adolescent offspring born prematurely to mothers with preeclampsia. J Pediatr. 2013; 162, 912.e1917.e1.Google Scholar
48. Hannam, K, Lawlor, DA, Tobias, JH. Maternal preeclampsia is associated with reduced adolescent off-spring hip bone mineral density in a UK population based birth cohort. J Bone Miner Res. 2015; 30, 16841691.Google Scholar
49. Tuovinen, S, Eriksson, JG, Kajantie, E, Raikkonen, K. Maternal hypertensive pregnancy disorders and cognitive functioning of the offspring: a systematic review. J Am Soc Hypertens. 2014; 8, 832.e1847.e1.Google Scholar
50. Davis, E, Lazdam, M, Lewandowski, A, et al. Cardiovascular risk factors in children and young adults born to preeclamptic pregnancies: a systematic review. Pediatrics. 2012; 129, 15521561.Google Scholar
51. Roberts, JM, Redman, CW. Pre-eclampsia: more than pregnancy-induced hypertension. Lancet. 1993; 341, 14471451.Google Scholar
52. Burton, GJ, Jauniaux, E. Placental oxidative stress: from miscarriage to preeclampsia. J Soc Gynecol Investig. 2004; 11, 342352.Google Scholar
53. Rees, S, Harding, R. Brain development during fetal life: influences of the intra-uterine environment. Neurosci Lett. 2004; 361, 111114.CrossRefGoogle ScholarPubMed
54. Zucchi, FC, Yao, Y, Ward, ID, et al. Maternal stress induces epigenetic signatures of psychiatric and neurological diseases in the offspring. PLoS One. 2013; 8, e56967.CrossRefGoogle ScholarPubMed
55. Jaenisch, R, Bird, A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nature Genetics. 2003; 33, 245254.CrossRefGoogle ScholarPubMed
56. Challis, JR, Sloboda, D, Matthews, SG, et al. The fetal placental hypothalamic-pituitary-adrenal (HPA) axis, parturition and post natal health. Mol Cell Endocrinol. 2001; 185, 135144.Google Scholar
57. McCalla, CO, Nacharaju, VL, Muneyyirci-Delale, O, Glasgow, S, Feldman, JG. Placental 11 beta-hydroxysteroid dehydrogenase activity in normotensive and pre-eclamptic pregnancies. Steroids. 1998; 63, 511515.Google Scholar
58. Seckl, JR, Meaney, MJ. Glucocorticoid programming. Ann N Y Acad Sci. 2004; 1032, 6384.Google Scholar
59. Cottrell, EC, Holmes, MC, Livingstone, DE, Kenyon, CJ, Seckl, JR. Reconciling the nutritional and glucocorticoid hypotheses of fetal programming. FASEB J. 2012; 26, 18661874.CrossRefGoogle ScholarPubMed
60. Doridot, L, Houry, D, Gaillard, H, et al. miR-34a expression, epigenetic regulation, and function in human placental diseases. Epigenetics. 2014; 9, 142151.CrossRefGoogle ScholarPubMed
61. Huang, Q, Chen, H, Li, J, et al. Epigenetic and non-epigenetic regulation of syncytin-1 expression in human placenta and cancer tissues. Cell Signal. 2014; 26, 648656.CrossRefGoogle ScholarPubMed
62. Tsankova, N, Renthal, W, Kumar, A, Nestler, EJ. Epigenetic regulation in psychiatric disorders. Nat Rev Neurosci. 2007; 8, 355367.Google Scholar
63. Vatten, L, Skjaerven, R. Is pre-eclampsia more than one disease? BJOG. 2016; 111, 298302.Google Scholar
64. Lewandowski, A, Leeson, P. Preeclampsia, prematurity and cardiovascular health in adult life. Early Hum Dev. 2014; 90, 725729.Google Scholar
65. Seckl, JR. Glucocorticoid programming of the fetus; adult phenotypes and molecular mechanisms. Mol Cell Endocrinol. 2001; 185, 6171.CrossRefGoogle ScholarPubMed
66. Bell, MJ. A historical overview of preeclampsia-eclampsia. J Obstet Gynecol Neonatal Nurs. 2010; 39, 510518.CrossRefGoogle ScholarPubMed
Supplementary material: PDF

Pinheiro supplementary material

Pinheiro supplementary material 1

Download Pinheiro supplementary material(PDF)
PDF 141.1 KB