Maternal body composition, offspring blood pressure and the hypothalamic-pituitary-adrenal axis
Corresponding Author
David I. W. Phillips
MRC Environmental Epidemiology Unit, University of Southampton, Southampton General Hospital, Southampton, UK, and
Professor D.I.W. Phillips PhD FRCP, MRC Unit, Southampton General Hospital, Tremona Road, Southampton SO16 6YD, UK. E-mail: [email protected]Search for more papers by this authorFranklyn I. Bennett
The Tropical Metabolism Research Unit, University of the West Indies, Mona, Kingston 7, Jamaica
Search for more papers by this authorRainford Wilks
The Tropical Metabolism Research Unit, University of the West Indies, Mona, Kingston 7, Jamaica
Search for more papers by this authorMinerva Thame
The Tropical Metabolism Research Unit, University of the West Indies, Mona, Kingston 7, Jamaica
Search for more papers by this authorMichael Boyne
The Tropical Metabolism Research Unit, University of the West Indies, Mona, Kingston 7, Jamaica
Search for more papers by this authorClive Osmond
MRC Environmental Epidemiology Unit, University of Southampton, Southampton General Hospital, Southampton, UK, and
Search for more papers by this authorTerrence E. Forrester
The Tropical Metabolism Research Unit, University of the West Indies, Mona, Kingston 7, Jamaica
Search for more papers by this authorCorresponding Author
David I. W. Phillips
MRC Environmental Epidemiology Unit, University of Southampton, Southampton General Hospital, Southampton, UK, and
Professor D.I.W. Phillips PhD FRCP, MRC Unit, Southampton General Hospital, Tremona Road, Southampton SO16 6YD, UK. E-mail: [email protected]Search for more papers by this authorFranklyn I. Bennett
The Tropical Metabolism Research Unit, University of the West Indies, Mona, Kingston 7, Jamaica
Search for more papers by this authorRainford Wilks
The Tropical Metabolism Research Unit, University of the West Indies, Mona, Kingston 7, Jamaica
Search for more papers by this authorMinerva Thame
The Tropical Metabolism Research Unit, University of the West Indies, Mona, Kingston 7, Jamaica
Search for more papers by this authorMichael Boyne
The Tropical Metabolism Research Unit, University of the West Indies, Mona, Kingston 7, Jamaica
Search for more papers by this authorClive Osmond
MRC Environmental Epidemiology Unit, University of Southampton, Southampton General Hospital, Southampton, UK, and
Search for more papers by this authorTerrence E. Forrester
The Tropical Metabolism Research Unit, University of the West Indies, Mona, Kingston 7, Jamaica
Search for more papers by this authorSummary
We tested the hypothesis that women who are thin or have poor pregnancy weight gain have offspring with higher blood pressure and examined whether this link is mediated by increased secretion of cortisol. We studied a cohort of 388 children born in Kingston, Jamaica. From hospital records we obtained information about their mother's body mass index (BMI) and weight gain during pregnancy. At age 8.5 years we measured the children's fasting plasma cortisol concentrations and blood pressure and assessed their mother's anthropometry. There were no relationships between the mother's BMI or weight gain during pregnancy and offspring blood pressure. However, mothers with a greater subscapular to triceps skinfold thickness ratio (SSTR) had offspring with higher blood pressure (5.6 mmHg systolic and 3.7 mmHg diastolic increase per unit change in SSTR, P = 0.002 and P = 0.008 respectively). Fasting plasma cortisol concentrations correlated with the children's systolic (r = 0.33, P < 0.0001) and diastolic pressures (r = 0.12, P = 0.02) independently of age, gender, weight or socio-economic status and were also predicted by the mother's SSTR. These findings suggest that maternal truncal obesity rather than thinness is associated with raised blood pressure in the offspring, and that this link may be mediated by increased cortisol secretion.
References
- 1 Godfrey KM. The ‘gold standard’ for optimal fetal growth and development. Journal of Pediatric Endocrinology and Metabolism 2001; 14: 1507–1513.
- 2 Stein CE, Fall CHD, Kumaran K, Osmond C, Cox V, Barker DJP. Fetal growth and coronary artery disease in South India. Lancet 1996; 348: 1269–1273.
- 3 Ravelli ACJ, Van Der Meulen JHP, Michels RPJ, Osmond C, Barker DJP, Hales CN, et al. Glucose tolerance in adults after prenatal exposure to famine. Lancet 1998; 351: 173–177.
- 4 Forsen T, Eriksson JG, Tuomilehto J, Teramo K, Osmond C, Barker DJP. Mother's weight in pregnancy and coronary heart disease in a cohort of Finnish men: follow up study. British Medical Journal 1997; 315: 837–840.
- 5 Laor A, Stevenson DK, Shemer J, Gale R, Seidman DS. Size at birth, maternal nutritional status in pregnancy, and blood pressure at age 17: population based analysis. British Medical Journal 1997; 315: 449–453.
- 6 Whincup PH, Cook DG, Papacosta O. Do maternal and intrauterine factors influence blood pressure in childhood? Archives of Disease in Childhood 1992; 67: 1423–1429.
- 7 Adair LS, Kuzawa CW, Borja J. Maternal energy stores and diet composition during pregnancy program adolescent blood pressure. Circulation 2001; 104: 1034–1439.
- 8 Godfrey KM, Forrester TE, Barker DJP, Jackson AA, Landman JP, Hall J St E, et al. Maternal nutritional status in pregnancy and blood pressure in childhood. British Journal of Obstetrics and Gynaecology 1994; 101: 398–403.
- 9 Clark PM, Atton C, Law CM, Sheill A, Godfrey K, Barker DJP. Weight in pregnancy, triceps skinfold thickness and blood pressure in the offspring. Obstetrics and Gynecology 1998; 91: 103–107.
- 10 Margetts B, Rowland MG, Foord FA, Cruddas AM, Cole TJ, Barker DJP. The relation of maternal weight to the blood pressures of Gambian children. International Journal of Epidemiology 1991; 20: 938–943.
- 11 Kramer MS. Determinants of low birthweight: methodological assessment and meta-analysis. Bulletin of the World Health Organisation 1987; 65: 663–737.
- 12 Owens JA, Owens PC, Robinson JS. Experimental fetal growth retardation: metabolic and endocrine aspects. In: Advances in Fetal Physiology. Editors: PD Gluckman, BM Johnston, PW Nathanielsz. New York: Ithaca, 1989; pp. 263–286.
- 13 Mellor D. Nutritional and placental determinants of foetal growth rate in sheep and consequences for the newborn lamb. British Veterinary Journal 1983; 139: 307–324.
- 14 Martyn CN, Barker DJP, Jespersen S, Greenwald S, Osmond C, Berry CL. Growth in utero, adult blood pressure, and arterial compliance. British Heart Journal 1995; 73: 116–121.
- 15 Phillips ID, Simonetta G, Owens JA, Robinson JS, Clarke IJ, McMillen IC. Placental restriction alters the functional development of the pituitary-adrenal axis in the sheep fetus during late gestation. Pediatric Research 1996; 40: 1–6.
- 16 Langley-Evans SC, Phillips GJ, Benediktsson R, Gardner DS, Edwards CRW, Jackson AA, et al. Protein intake in pregnancy, placental glucocorticoid metabolism and the programming of hypertension in the rat. Placenta 1996; 17: 169–172.
- 17 Welberg LAM, Seckl JR. Prenatal stress, glucocorticoids and the programming of the brain. Journal of Neuroendocrinology 2001; 13: 113–128.
- 18 Economides DL, Nicholaides KH, Linton EA, Perry LA, Chard T. Plasma cortisol and adrenocorticotrophin in appropriate and small for gestational age fetuses. Fetal Therapy 1988; 3: 158–164.
- 19 Clark PM, Hindmarsh PC, Sheill AW, Law CM, Honour JW, Barker DJP. Size at birth and adrenocortical function in childhood. Clinical Endocrinology 1996; 45: 721–726.
- 20 Harland PSEG, Watson MJ, Ashworth L. The effect of metabolic programming on atherosclerosis and obesity risk factors in UK adolescents living in poor socioeconomic areas. Annals of the New York Academy of Sciences 1997; 817: 361–364.
- 21 Phillips DIW, Walker BR, Reynolds RM, Flanagan DEH, Wood PJ, Osmond C, et al. Low birthweight predicts elevated plasma cortisol concentrations in adults from three populations. Hypertension 2000; 35: 1301–1306.
- 22 Reynolds RM, Walker BR, Syddall HE, Wood PJ, Phillips DIW, Whorwood CB. Altered control of cortisol secretion in adult men with low birthweight and cardiovascular risk factors. Journal of Clinical Endocrinology and Metabolism 2001; 86: 245–250.
- 23 Levitt NS, Lambert E, Woods D, Hales CN, Andrew R, Seckl JR. Impaired glucose tolerance and elevated blood pressure in low birthweight, non-obese, young South African adults: early programming of cortisol axis. Journal of Clinical Endocrinology and Metabolism 2000; 85: 4611–4618.
- 24 Watt GCM, Harrap SB, Foy CJW. Abnormalities of glucocorticoid metabolism and the renin-angiotensin system: a four corners approach to the identification of genetic determinants of blood pressure. Journal of Hypertension 1992; 10: 473–482.
- 25 Rosmond R, Dallman MF, Björntorp P. Stress-related cortisol secretion in men: relationships with abdominal obesity and endocrine, metabolic and hemodynamic abnormalities. Journal of Clinical Endocrinology and Metabolism 1998; 83: 1853–1859.
- 26 Stolk RP, Lamberts SWJ, De Jong FH, Pols HAP, Grobbee DE. Gender differences in the associations between cortisol and insulin in healthy subjects. Journal of Endocrinology 1996; 149: 313–318.
- 27 Filipovsky J, Ducimetiere P, Eschwege E, Richard JL, Rosselin G, Claude JR. The relationship of blood pressure with glucose, insulin, heart rate, free fatty acids and plasma cortisol levels according to degree of obesity in middle-aged men. Journal of Hypertension 1996; 14: 229–235.
- 28 Bennett F, Watson-Brown C, Thame M, Wilks R, Osmond C, Hales CN, et al. Shortness at birth is associated with insulin resistance in pre-pubertal Jamaican children. European Journal of Clinical Nutrition 2002; 56: 506–511.
- 29 Forrester TE, Wilks RJ, Bennett FI, Simeon D, Osmond C, Allen M, et al. Fetal growth and cardiovascular risk factors in Jamaican schoolchildren. British Medical Journal 1996; 312: 156–160.
- 30 Lohman TG, Roche AF, Martorell R. Anthropometric Standardization Reference Manual. Champaign, IL: Human Kinetics Books, 1987.
- 31 Slaughter MH, Lohman TG, Boileau RA, Horswill CA, Stillman RJ, Van Loan MD, et al. Skinfold equations for estimations of body fatness in children and youth. Human Biology 1988; 60: 709–723.
- 32 Wood PJ, Donovan SJ, Glenn C, Kilpatrick K. New immunoassays for cortisone in serum, urine and saliva. Proceedings of the 10th International Conference on Hormonal Steroids 1998; pp. 222.
- 33 Falkner B, Hulman S, Kushner H. Birth weight versus childhood growth as determinants of adult blood pressure. Hypertension 1998; 31: 145–150.
- 34 Fraser R, Ingram MC, Anderson NH, Morrison C, Davies E, Connell JMC. Cortisol effects on body mass, blood pressure, and cholesterol in the general population. Hypertension 1999; 3: 1374–1378.
- 35 Haffner SM, Stern MP, Hazuda HP, Pugh J, Patterson JK. Do upper-body and centralized adiposity measure different aspects of regional body-fat distribution? Relationship to non-insulin-dependent diabetes mellitus, lipids and lipoproteins. Diabetes 1987; 36: 43–51.
- 36 Malina RM, Katzmarzyk PT, Beunen G. Birth weight and its relationship to size attained and relative fat distribution at 7–12 years of age. Obesity Research 1996; 4: 385–390.
- 37 Barker M, Robinson S, Osmond C, Barker DJP. Birth weight and body fat distribution in adolescent girls. Archives of Disease in Childhood 1997; 77: 381–383.
- 38 Byberg L, McKeigue PM, Zethelius B, Lithell HO. Birth weight and the insulin resistance syndrome; association of low birthweight with truncal obesity and raised plasminogen activator inhibitor -1 but not with abdominal obesity or plasma lipid disturbances. Diabetologia 2000; 43: 54–60.
- 39 Conway JM, Yanovski SZ, Avila NA, Hubbard VS. Visceral adipose tissue differences in black and white women. American Journal of Clinical Nutrition 1995; 61: 765–771.
- 40 Hattersley AT, Took JE. The fetal insulin hypothesis: an alternative explanation of the association of low birthweight with diabetes and vascular disease. Lancet 1999; 353: 1789–1792.