Gender differences in developmental programming of cardiovascular diseases

Clinical Science

Volumn 130, Issue 5, 2016, Pages 337-348

  Dasinger, John Henry ^a   Alexander, Barbara T ^a  

^a UNIVERSITY OF MISSISSIPPI SCHOOL OF MEDICINE   (United States)

Author keywords

Ageing; Blood pressure; Developmental programming; Low birth weight; Sex differences

Indexed keywords

AGING; ARTICLE; BLOOD PRESSURE; CARDIOVASCULAR DISEASE; CARDIOVASCULAR RISK; CAUSE OF DEATH; CHILD GROWTH; CHILDHOOD; CHRONIC DISEASE; DISEASE SEVERITY; HUMAN; HYPERTENSION; LOW BIRTH WEIGHT; PRENATAL EXPOSURE; PRIORITY JOURNAL; RISK FACTOR; SEX DIFFERENCE; BIRTH WEIGHT; EMBRYOLOGY; FEMALE; FETUS DEVELOPMENT; MALE; NEWBORN; PATHOPHYSIOLOGY; PHYSIOLOGY; PREGNANCY; SEXUAL DEVELOPMENT;

BIRTH WEIGHT; BLOOD PRESSURE; FEMALE; FETAL DEVELOPMENT; HUMANS; HYPERTENSION; INFANT, LOW BIRTH WEIGHT; INFANT, NEWBORN; MALE; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RISK FACTORS; SEX CHARACTERISTICS;

EID: 84958063229     PISSN: 01435221     EISSN: 14708736     Source Type: Journal    
DOI: 10.1042/CS20150611     Document Type: Article

References (109)

1. Barker, D.J. and Osmond, C. (1986) Infant mortality, childhood nutrition, and ischaemic heart disease in England and Wales. Lancet i, 1077-1081
2. Forsdahl, A. (2002) Observations throwing light on the high mortality in the county of Finnmark. Is the high mortality today a late effect of very poor living conditions in childhood and adolescence? Int. J. Epidemiol. 31, 302-308
3. Barker, D.J. and Osmond, C. (1988) Low birth weight and hypertension. BMJ 297, 134-135
4. Kotsis, V., Stabouli, S., Pitiriga, V., Toumanidis, S., Papmichael, C. and Zakopoulos, N. (2006) Ambulatory blood pressure monitoring and target organ damage: effects of age and sex. Blood Press. Monit. 11, 9-15
5. Alexander, B.T. (2003) Placental insufficiency leads to development of hypertension in growth-restricted offspring. Hypertension 41, 457-462
6. Woods, L.L., Ingelfinger, J.R., Nyengaard, J.R. and Rasch, R. (2001) Maternal protein restriction suppresses the newborn renin-angiotensin system and programs adult hypertension in rats. Pediatr. Res. 49, 460-467
7. Woods, L.L., Ingelfinger, J.R. and Rasch, R. (2005) Modest maternal protein restriction fails to program adult hypertension in female rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 289, R1131-R1136
8. Ortiz, L.A., Quan, A., Zarzar, F., Weinberg, A. and Baum, M. (2003) Prenatal dexamethasone programs hypertension and renal injury in the rat. Hypertension 41, 328-334
9. Intapad, S., Tull, F.L., Brown, A.D., Dasinger, J.H., Ojeda, N.B., Fahling, J.M. and Alexander, B.T. (2013) Renal denervation abolishes the age-dependent increase in blood pressure in female intrauterine growth-restricted rats at 12 months of age. Hypertension 61, 828-834
10. Primatesta, P., Falaschetti, E. and Poulter, N.R. (2005) Birth weight and blood pressure in childhood: results from the Health Survey for England. Hypertension 45, 75-79
11. Singhal, A., Cole, T.J., Fewtrell, M., Kennedy, K., Stephenson, T. and Elias-Jones, A. (2007) Promotion of faster weight gain in infants born small for gestational age. Hypertension 115, 213-220
12. Belfort, M.B., Rifas-Shiman, S.L., Rich-Edwards, J., Kleinman, K.P. and Gillman, M.W. (2007) Size at birth, infant growth, and blood pressure at three years of age. J Pediatr. 151, 670-674
13. Hindmarsh, P.C., Bryan, S., Geary, M.P. and Cole, T.J. (2010) Effects of current size, postnatal growth, and birth size on blood pressure in early childhood. Pediatrics 126, e1507-e1513
14. Law, C.M., Shiell, A.W., Newsome, C.A., Syddall, H.E., Shinebourne, E.A., Fayers, P.M., Martyn, C.N. and de Swiet, M. (2002) Fetal, infant, and childhood growth and adult blood pressure: a longitudinal study from birth to 22 years of age. Circulation 105, 1088-1092
15. Barker, D.J., Osmond, C., Golding, J., Kuh, D. and Wadsworth, M.E. (1989) Growth in utero, blood pressure in childhood and adult life, and mortality from cardiovascular disease. BMJ 298, 564-567
16. Chen, W., Srinivasan, S.R., Ruan, L., Mei, H. and Berenson, G.S. (2011) Adult hypertension is associated with blood pressure variability in childhood in blacks and whites: the Bogalusa Heart Study. Am. J. Hypertens. 24, 77-82
17. Moore, V.M., Miller, A.G., Boulton, T.J.C., Cockington, R.A., Craig, I.H., Magarey, A.M. and Robinson, J.S. (1996) Placental weight, birth measurements and blood pressure at age 8 years. Arch. Dis. Child. 74, 538-541
18. Moore, V.M., Cockington, R.A., Ryan, P. and Robinson, J.S. (1999) The relationship between birth weight and blood pressure amplifies from childhood to adulthood. J. Hypertens. 17, 883-888
19. Law, C.M., de Swiet, M., Osmond, C., Fayers, P.M., Barker, D.J., Cruddas, A.M. and Fall, C.H. (1993) Initiation of hypertension in utero and its amplification throughout life. BMJ 306, 24-27
20. Ulterwaal, C.S., Anthony, S., Launer, L.J., Witteman, J.C., Trouwborst, A.M., Hofman, A. and Grobbee, D.E. (1997) Birth weight, growth, and blood pressure: an annual follow-up of children aged 5 through 21 years. Hypertension 30, 267-271
21. Head, R.F., Tu, Y.K., Gilthorpe, M.S., Mishra, G.D., Williams, S. and Ellison, G.T. (2007) What evidence is there that adjustment for adult height influences the relationship between birth weight and blood pressure? Ann. Hum. Biol. +34, 252-264
22. Bowers, K., Liu, G., Wang, P., Ye, T., Tian, Z., Liu, E., Yu, Z., Yang, X., Klebanoff, M., Yeung, E. et al. (2011) Birth weight, postnatal weight change, and risk for high blood pressure among Chinese children. Pediatrics 127, e1272-e1279
23. Huang, R.C., Burke, V., Newnham, J.P., Stanley, F.J., Kendall, G.E., Landau, L.I., Oddy, W.H., Blake, K.V., Palmer, L.J. and Beilin, L.J. (2007) Perinatal and childhood origins of cardiovascular disease. Int. J. Obes. 31, 236-44
24. Zhang, Y., Li, H., Liu, S.J., Fu, G.J., Zhao, Y., Xie, Y.J., Zhang, Y. and Wang, Y.X. (2013) The associations of high birth weight and blood pressure with hypertension in later life: a systematic review and meta-analysis. Hypertens. Res. 36, 725-733
25. Huxley, R., Neil, A. and Collins, R. (2002) Unravelling the fetal origins hypothesis: is there really an inverse association between birth weight and subsequent blood pressure? Lancet 360, 659-665
26. Falkner, B., Hulman, S. and Kushner, H. (2004) Effect of birth weight on blood pressure and body size in early adolescence. Hypertension 43, 203-207
27. Salvi, P., Meriem, C., Temmar, M., Marino, F., Sari-Ahmed, M., Labat, C., Alla, F., Joly, L., Safar, M.E. and Benetos, A. (2010) Association of current weight and birth weight with blood pressure levels in Saharan and European teenager populations. Am. J. Hypertens. 23, 379-386
28. Lurbe, E., Torro, I., Rodriguez, C., Alvarez, V. and Redon, J. (2001) Birth weight influences blood pressure values and variability in children and adolescents. Hypertension 38, 389-393
29. Hemachandra, A.H., Howards, P.P., Furth, S.L. and Klebanoff, M.A. (2007) Birth weight, postnatal growth, and risk for high blood pressure at 7 years of age: results from the collaborative perinatal project. Pediatrics 119, 1264-1270
30. Järvelin, M.R., Sovio, U., King, V., Lauren, L., Xu, B., McCarthy, M.I., Hartikainen, A.L., Laitinen, J., Zitting, P., Rantakallio, P. et al. (2004) Early life factors and blood pressure at age 31 years in the 1966 northern Finland birth cohort. Hypertension 44, 838-846
31. Chen, H., Nembhard, W.N. and Stockwell, G.H. (2014) Sex-specific effects of fetal exposure to the 1959-1961 Chinese famine on risk of adult hypertension. Matern. Child Health J. 18, 527-533
32. Gamborg, M., Byberg, L., Rasmussen, F., Andersen, P.K., Baker, J.L., Bengtsson, C., Canoy, D., Drøyvold, W., Eriksson, J.G., Forsén, T. et al., NordNet Study Group (2007) Birth weight and systolic blood pressure in adolescence and adulthood: meta-regression analysis of sex-and age-specific results from 20 Nordic studies. Am. J. Epidemiol. 166, 634-645
33. Lawlor, D.A., Ebrahim, S. and Davey, S.G. (2002) Is there a sex difference in the association between birth weight and systolic blood pressure in later life? Findings from a meta-regression analysis. Am. J. Epidemiol. 156, 1100-1104
34. Vos, L.E., Oren, A., Bots, M.L., Gorissen, W.H., Grobbee, D.E. and Uiterwaal, C.S. (2006) Birth size and coronary heart disease risk score in young adulthood. The Atherosclerosis Risk in Young Adults (ARYA) study. Eur. J. Epidemiol. 21, 33-38
35. Lawlor, D.A., Ronalds, G., Clark, H., Smith, G.D. and Leon, D.A. (2005) Birth weight is inversely associated with incident coronary heart disease and stroke among individuals born in the 1950s: findings from the Aberdeen Children of the 1950s prospective cohort study. Circulation 112, 1414-1418
36. Wellons, M., Ouyang, P., Schreiner, P.J., Herrington, D.M. and Vaidya, D. (2012) Early menopause predicts future coronary heart disease and stroke: the Multi-Ethnic Study of Atherosclerosis. Menopause 19, 1081-1087
37. Stein, A.D., Zybert, P.A., van der Pal-de Bruin, K. and Lumey, L.H. (2006) Exposure to famine during gestation, size at birth, and blood pressure at age 59 y: evidence from the Dutch Famine. Eur. J. Epidemiol. 21, 759-765
38. Tom, S.E., Cooper, R., Kuh, D., Guralnik, J.M., Hardy, R. and Power, C. (2010) Fetal environment and early age at natural menopause in a British birth cohort study. Hum. Reprod. 25, 791-798
39. Ojeda, N.B., Grigore, D., Yanes, L.L., Iliescu, R., Robertson, E.B., Zhang, H. and Alexander, B.T. (2007) Testosterone contributes to marked elevations in mean arterial pressure in adult male intrauterine growth restricted offspring. Am. J. Physiol. Regul. Integr. Comp. Physiol. 292, R758-R763
40. Ojeda, N.B., Grigore, D., Robertson, E.B. and Alexander, B.T. (2007) Estrogen protects against increased blood pressure in postpubertal female growth restricted offspring. Hypertension 50, 679-685
41. Schreuder, M.F., Fodor, M., van Wijk, J.A. and Delemarre-van de Waal, H.A. (2006) Association of birth weight with cardiovascular parameters in adult rats during baseline and stressed conditions. Pediatr. Res. 59, 126-130
42. Wlodek, M.E., Westcott, K., Siebel, A.L., Owens, J.A. and Moritz, K.M. (2008) Growth restriction before or after birth reduces nephron number and increases blood pressure in male rats. Kidney Int. 74, 187-195
43. Moritz, K.M., Mazzuca, M.Q., Siebel, A.L., Mibus, A., Arena, D., Tare, M., Owens, J.A. and Wlodek, M.E. (2009) Uteroplacental insufficiency causes a nephron deficit, modest renal insufficiency but no hypertension with ageing in female rats. J. Physiol. 587, 2635-2646
44. Bourque, S.L., Gragasin, F.S., Quon, A.L., Mansour, Y., Morton, J.S. and Davidge, S.T. (2013) Prenatal hypoxia causes long-term alterations in vascular endothelin-1 function in aged male, but not female, offspring. Hypertension 62, 753-758
45. Pijacka, W., Clifford, B., Tilburgs, C., Joles, J.A., Langley-Evans, S. and McMullen, S. (2015) Protective role of female gender in programmed accelerated renal aging in the rat. Physiol. Rep. 3, e12342
46. Vehaskari, V.M., Aviles, D.H. and Manning, J. (2001) Prenatal programming of adult hypertension in the rat. Kidney Int. 59, 238-245
47. Tao, H., Rui, C., Zheng, J., Tang, J., Wu, L., Shi, A., Chen, N., He, R., Wu, C., Li, J. et al. (2013) Angiotensin II-mediated vascular changes in aged offspring rats exposed to perinatal nicotine. Peptides 44, 111-119
48. Villar, J., Carroli, G., Wojdyla, D., Abalos, E., Giordano, D., Ba'aqeel, H., Farno, U., Bergsjø, P., Bakketeig, L., Lumbiganon, P. et al., World Health Organization Antenatal Care Trial Research Group (2006) Preeclampsia, gestational hypertension and intrauterine growth restriction, related or independent conditions? Am. J. Obstet. Gynecol. 194, 921-931
49. Davis, E.F., Lewandowski, A.J., Aye, C., Williamson, W., Boardman, H., Huang, R.C., Mori, T.A., Newnham, J., Beilin, L.J. and Leeson, P. (2015) Clinical cardiovascular risk during young adulthood in offspring of hypertensive pregnancies: insights from a 20-year prospective follow-up birth cohort. BMJ Open 5, e008136
50. Fisher, M., Baessler, A. and Schunkert, H. (2002) Renin angiotensin system and gender differences in the cardiovascular system. Cardiovasc. Res. 15, 672-677
51. Chen, Y.F., Naftilan, A.J. and Oparil, S. (1992) An4drogen-dependent angiotensinogen and renin messenger RNA expression in hypertensive rats. Hypertension 19, 456-463
52. Grigore, D., Ojeda, N.B., Robertson, E.B., Dawson, A.S., Huffman, C.A., Bourassa, E.A., Speth, R.C., Brosnihan, K.B. and Alexander, B.T. (2007) Placental insufficiency results in temporal alterations in the renin angiotensin system in male hypertensive growth restricted offspring. Am. J. Physiol. Regul. Integr. Comp. Physiol. 293, R804-R8011
53. Ojeda, N.B., Royals, T.P., Black, J.T., Dasinger, J.H., Johnson, J.M. and Alexander, B.T. (2010) Enhanced sensitivity to acute angiotensin II is testosterone dependent in adult male growth-restricted offspring. Am. J. Physiol. Regul. Integr. Comp. Physiol. 298, R1421-R1427
54. Iliescu, R., Cucchiarelli, V.E., Yanes, L.L., Iles, J.W. and Reckelhoff, J.F. (2007) Impact of androgen-induced oxidative stress on hypertension in male SHR. Am. J. Physiol. Regul. Integr. Comp. Physiol. 292, R731-R735
55. Alonso-Alvarez, C., Bertrand, S., Faivre, B., Chastel, O. and Sorci, G. (2007) Testosterone and oxidative stress: the oxidation handicap hypothesis. Proc. R. Soc. Lond. 274, 819-825
56. Ojeda, N.B., Hennington, B.S., Williamson, D.T., Hill, M.L., Betson, N.E., Sartori-Valinotti, J.C., Reckelhoff, J.F., Royals, T.P. and Alexander, B.T. (2012) Oxidative stress contributes to sex differences in blood pressure in adult growth-restricted offspring. Hypertension 60, 114-122
57. Rosamond, W., Flegal, K., Friday, G., Furie, K., Go, A., Greenlund, K., Haase, N., Ho, M., Howard, V., Kissela, B., Committee, American Heart Association Statistics, Subcommittee, Stroke Statistics et al. (2007) Heart disease and stroke statistics - 2007 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation 115, e69-e171
58. Preston, R.A. (2007) Effects of blood pressure reduction on cardiovascular risk estimates in hypertensive postmenopausal women. Climacteric 10 (Suppl), 132-141
59. Moritz, K.M., Cuffe, J.S., Wilson, L.B., Dickinson, H., Wlodek, M.E., Simmons, D.G. and Denton, K.M. (2010) Review: sex specific programming: a critical role for the renal renin-angiotensin system. Placenta 31, S40-S46
60. Baumer, A.T., Nickenig, G. and Bohm, M. (2000) Protection of the cardiovascular system by estrogens. Role of the renin-angiotensin system. Dtsch. Med. Wochenschr. +125, 1444-1449
61. Wassmann, K., Ghiassi, A., Wassmann, S., Bohm, M. and Nickenig, G. (2006) AT1 receptor antagonism improves endothelial dysfunction in postmenopausal women. Maturitas 53, 176-183
62. Bureau, I., Gueux, E., Mazur, A., Rock, E., Roussel, A.M. and Rayssiguier, Y. (2003) Female rats are protected against oxidative stress during copper deficiency. J. Am. Coll. Nutr. 22, 239-246
63. Wiinberg, N., Høegholm, A., Christensen, H.R., Bang, L.E., Mikkelsen, K.L., Nielsen, P.E., Svendsen, T.L., Kampmann, J.P., Madsen, N.H. and Bentzon, M.W. (1995) 24-h ambulatory blood pressure in 352 normal Danish subjects, related to age and gender. Am. J. Hypertens. 8, 978-986
64. Davies, A.A., Smith, G.D., May, M.T. and Ben-Shlomo, Y. (2006) Association between birth weight and blood pressure is robust, amplifies with age, and may be underestimated. Hypertension 48, 431-436
65. Sokol, R.Z., Okuda, H., Stanczyk, F.Z., Wolfe, G.W., Delaney, J.C. and Chapin, R.E. (1999) Normative reproductive indices for male and female adult Sprague-Dawley rats. Contraception 59, 203-207
66. Shah, N.R. and Braverman, E.R. (2012) Measuring adiposity in patients: the utility of body mass index (BMI), percent body fat, and leptin. PLoS One 7, e33308
67. Hall, J.E., da Silva, A.A., do Carmo, J.M., Dubinion, J., Hamza, S., Munusamy, S., Smith, G. and Stec, D.E. (2010) Obesity-induced hypertension: role of sympathetic nervous system, leptin, and melanocortins. J. Biol. Chem. 285, 17271-17276
68. Mark, A.L., Agassandian, K., Morgan, D.A., Liu, X., Cassell, M.D. and Rahmouni, K. (2009) Leptin signaling in the nucleus tractus solitarii increases sympathetic nerve activity to the kidney. Hypertension 53, 375-380
69. Alexander, B.T., Hendon, A.E., Ferril, G. and Dwyer, TM. (2005) Renal denervation abolishes hypertension in low birth weight offspring from regnant rats with reduced uterine perfusion. Hypertension 45, 754-758
70. Lane, R.H., Chandorkar, A.K., Flozak, A.S. and Simmons, R.A. (1998) Intrauterine growth retardation alters mitochondrial gene expression and function in fetal and juvenile rat skeletal muscle. Pediatr. Res. 43, 563-570
71. Schreuder, M.F., Nyengaard, J.R., Fodor, M., van Wijk, J.A. and Delemarre-van de Waal, H.A. (2005) Glomerular number and function are influenced by spontaneous and induced low birth weight in rats. J. Am. Soc. Nephrol. 16, 2913-2919
72. Hughson, M., Farris, 3rd, A.B., Douglas-Denton, R., Hoy, W.E. and Bertram, J.F. (2003) Glomerular number and size in autopsy kidneys: the relationship to birth weight. Kidney Int 63, 2113-212
73. Williams, S.J., Campbell, M.E., McMillen, I.C. and Davidge, S.T. (2005) Differential effects of maternal hypoxia or nutrient restriction on carotid and femoral vascular function in neonatal rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 288, R360-R367
74. Morton, J.S., Rueda-Clausen, C.F. and Davidge, S.T. (2010) Mechanisms of endothelium-dependent vasodilation in male and female, young and aged offspring born growth restricted. Am. J. Physiol. Regul. Integr. Comp. Physiol. 298, R930-R938
75. Williams, S.J., Hemmings, D.G., Mitchell, J.M., McMillen, I.C. and Davidge, S.T. (2005) Effects of maternal hypoxia or nutrient restriction during pregnancy on endothelial function in adult male rat offspring. J. Physiol. 565, 125-135
76. Van Geijn, H.P., Kaylor, Jr, W.M., Nicola, K.R. and Zuspan, F.P. (1980) Induction of severe intrauterine growth retardation in the Sprague-Dawley rat. Am. J. Obstet. Gynecol. 137, 43-47
77. Martin, H., Hu, J., Gennser, G. and Norman, M. (2000) Impaired endothelial function and increased carotid stiffness in 9-year-old children with low birth weight. Circulation 102, 2739-2744
78. Martin, H., Gazelius, B. and Norman, M. (2000) Impaired acetylcholine-induced vascular relaxation in low birth weight infants: implications for adult hypertension? Pediatr. Res. 47, 457-462
79. Goodfellow, J., Bellamy, M.F., Gorman, S.T., Brownlee, M., Ramsey, M.W., Lewis, M.J., Davies, D.P. and Henderson, A.H. (1998) Endothelial function is impaired in fit young adults of low birth weight. Cardiovasc. Res. 40, 600-606
80. Langley, S.C. and Jackson, A.A. (1994) Increased systolic blood pressure in adult rats induced by fetal exposure to maternal low protein diets. Clin. Sci. (Lond.) 86, 217-222
81. Langley-Evans, SC. (2000) Critical differences between two low protein diet protocols in th programming of hypertension in the rat. Int. J. Food Sci. Nutr. 51, 11-1
82. Joles, J.A., Sculley, D.V. and Langley-Evans, S.C. (2010) Proteinuria in aging rats due to low-protein diet during mid-gestation. J. Dev. Orig. Health Dis. 1, 75-83
83. Woods, L.L., Morgan, T.K. and Resko, J.A. (2010) Castration fails to prevent prenatally programmed hypertension in male rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 298, R1111-R1116
84. Manning, J. and ,V.M., Vehaskari (2001) Low birth weight-associated adult hypertension in the rat. Pediatr. Nephrol. 16, 417-422
85. Zhang, D.Y., Lumbers, E.R., Simonetta, G., Wu, JJ, Owens, J.A., Robinson, J.S. and McMillen, I.C. (2000) Effects of placental insufficiency on the ovine fetal renin-angiotensin system. Exp. Physiol. 85, 79-84
86. Grigore, D., Ojeda, N.B. and Alexander, B.T. (2008) Sex differences in the fetal programming of hypertension. Gend. Med. 5, S121-S132
87. Lozano, G., Elmaghrabi, A., Salley, J., Siddique, K., Gattineni, J. and Baum, M. (2015) Effect of prenatal programming and postnatal rearing on glomerular filtration rate in adult rats. Am. J. Physiol. Renal Physiol. 308, F411-F419
88. Kind, K.L., Simonetta, G., Clifton, P.M., Robinson, J.S. and Owens, J.A. (2002) Effect of maternal feed restriction on blood pressure in the adult guinea pig. Exp. Physiol. 87, 469-477
89. Ponzio, B.F., Carvalho, M.H., Fortes, Z.B. and do Carmo Franco, M. (2012) Implications of maternal nutrient restriction in transgenerational programming of hypertension and endothelial dysfunction across F1-F3 offspring. Life Sci. 90, 571-577
90. Araminaite, V., Zalgeviciene, V., Simkunaite-Rizgeliene, R., Stukas, R., Kaminskas, A. and Tutkuviene, J. (2014) Maternal caloric restriction prior to pregnancy increases the body weight of the second-generation male offspring and shortens their longevity in rats. Tohoku J. Exp. Med. 234, 41-50
91. Camelo, L.V., Giatti, L., Chor, D., Griep, R.H., Benseñor, I.M., Santos, I.S., Kawachi, I. and Barreto, S.M. (2015) Associations of life course socioeconomic position and job stress with carotid intima-media thickness. The Brazilian Longitudinal Study of Adult Health (ELSA-Brasil). Soc. Sci. Med. 141, 91-99
92. Plana-Ripoll, O., Liu, X., Momen, N.C., Parner, E., Olsen, J. and Li, J. (2015) Prenatal exposure to maternal stress following bereavement and cardiovascular disease: A nationwide population-based and sibling-matched cohort study. Eur. J. Prev. Cardiol. pii: 2047487315585294
93. Loria, A.S., Pollock, D.M. and Pollock, J.S. (2010) Early life stress sensitizes rats to angiotensin II-induced hypertension and vascular inflammation in adult life. Hypertension 55, 494-499
94. Loria, A.S., Yamamoto, T., Pollock, D.M. and Pollock, J.S. (2013) Early life stress induces renal dysfunction in adult male rats but not female rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 304, R121-R129
95. Crowley, P., Chalmers, I. and Keirse, M.J. (1990) The effects of corticosteroid administration before preterm delivery: an overview of the evidence from controlled trials. Br. J. Obstet. Gynaecol. 97, 11-25
96. Reinisch, J.M., Simon, N.G., Karow, W.G. and Gandelman, R. (1978) Prenatal exposure to prednisone in humans and animals retards intrauterine growth. Science 202, 436-438
97. Celsi, G., Kistner, A., Aizman, R., Eklof, A.C., Ceccatelli, S., de Santiago, A. and Jacobson, S.H. (1998) Prenatal dexamethasone causes oligonephronia, sodium retention, and higher blood pressure in the offspring. Pediatr. Res. 44, 317-322
98. Tang, L., Carey, L.C., Bi, J., Valego, N., Sun, X., Deibel, P., Perrott, J., Figueroa, J.P., Chappell, M.C. and Rose, J.C. (2009) Gender differences in the effects of antenatal betamethasone exposure on renal function in adult sheep. Am. J. Physiol. Regul. Integr. Comp. Physiol. 296, R309-R317
99. Singh, R.R., Cullen-McEwen, L.A., Kett, M.M., Boon, W.M., Dowling, J., Bertram, J.F. and Moritz, K.M. (2007) Prenatal corticosterone exposure results in altered AT1/AT2, nephron deficit and hypertension in the rat offspring. J. Physiol. 579, 503-513
100. Dagan, A., Kwon, H.M., Dwarakanath, V. and Baum, M. (2008) Effect of renal denervation on prenatal programming of hypertension and renal tubular transporter abundance. Am. J. Physiol. Renal. Physiol. 295, F29-F34
101. Blake, K.V., Gurrin, L.C., Evans, S.F., Beilin, L.J., Landau, L.I., Stanley, F.J. and Newnham, J.P. (2000) Maternal cigarette smoking during pregnancy, low birth weight and subsequent blood pressure in early childhood. Early Hum. Dev. 57, 137-147
102. Lambers, D.S. and Clark, K.E. (1996) The maternal and fetal physiologic effects of nicotine. Semin. Perinatol. 20, 115-126
103. Slotkin, T.A. (1998) Fetal nicotine or cocaine exposure: which one is worse? J. Pharmacol. Exp. Ther. 285, 931-945 PubMed
104. Xiao, D., Huang, X., Lawrence, J., Yang, S. and Zhang, L. (2007) Fetal and neonatal nicotine exposure differentially regulates vascular contractility in adult male and female offspring. J. Pharmacol. Exp. Ther. 320, 654-461
105. Xiao, D., Xu, Z., Huang, X., Longo, L.D., Yang, S. and Zhang, L. (2008) Prenatal gender-related nicotine exposure increases blood pressure response to angiotensin II in adult offspring. Hypertension 51, 1239-1247
106. Xiao, D., Huang, X., Yang, S. and Zhang, L. (2013) Estrogen normalizes perinatal nicotine-induced hypertensive responses in adult female rat offspring. Hypertension 61, 1246-54
107. Mao, C., Wu, J., Xiao, D., Lv, J., Ding, Y., Xu, Z. and Zhang, L. (2009) The effect of fetal and neonatal nicotine exposure on renal development of AT(1) and AT(2) receptors. Reprod. Toxicol. 27, 149-154
108. Khorram, O., Keen-Rinehart, E., Chuang, T.D., Ross, M.G. and Desai, M. (2015) Maternal undernutrition induces premature reproductive senescence in adult female rat offspring. Fertil. Steril. 103, 291-298.e2
109. Bernal, A.B., Vickers, M.H., Hampton, M.B., Poynton, R.A. and Sloboda, D.M. (2010) Maternal undernutrition significantly impacts ovarian follicle number and increases ovarian oxidative stress in adult rat offspring. Plos One 5, e15558