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Elevated Plasma Cortisol Concentrations: A Link between Low Birth Weight and the Insulin Resistance Syndrome?¹

Medical Research Council Environmental Epidemiology Unit, University of Southampton (D.I.W.P., D.J.P.B., C.H.D.F, C.B.W.), and the Regional Endocrine Unit, Southampton General Hospital (P.W.), Southampton, United Kingdom; and the Department of Medicine, University of Edinburgh, Western General Hospital (J.R.S., B.R.W.), Edinburgh, Scotland

Address all correspondence and requests for reprints to: Dr. D. I. W. Phillips, Medical Research Council Unit, Southampton General Hospital, Tremona Road, Southampton, United Kingdom SO16 6YD. E-mail: diwp{at}mrc.soton.ac.uk

	Abstract

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Recent studies have shown that reduced fetal growth is associated with the development of the insulin resistance syndrome in adult life. The mechanisms are not known. However increased activity of the hypothalamic-pituitary-adrenal axis (HPAA) may underlie this association; the axis is known to be reset by fetal growth retardation in animals, and there is evidence in humans of an association between raised HPAA activity and the insulin resistance syndrome. We have, therefore, examined the relations among size at birth, plasma cortisol concentrations, and components of the insulin resistance syndrome in a sample of healthy men. We measured 0900 h fasting plasma cortisol and corticosteroid-binding globulin levels in 370 men who were born in Hertfordshire, UK, between 1920–1930 and whose birth weights were recorded. Fasting plasma cortisol concentrations varied from 112–702 nmol/L and were related to systolic blood pressure (P = 0.02), fasting and 2-h plasma glucose concentrations after an oral glucose tolerance test (P = 0.0002 and P = 0.04), plasma triglyceride levels (P = 0.009), and insulin resistance (P = 0.006). Plasma cortisol concentrations fell progressively (P = 0.007) from 408 nmol/L in men whose birth weights were 5.5 lb (2.50 kg) or less to 309 nmol/L among those who weighed 9.5 lb (4.31 kg) or more at birth, a trend independent of age and body mass index. These findings suggest that plasma concentrations of cortisol within the normal range could have an important effect on blood pressure and glucose tolerance. Moreover, this study provides the first evidence that intrauterine programming of the HPAA may be a mechanism underlying the association between low birth weight and the insulin resistance syndrome in adult life.

	Introduction

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STUDIES in both Europe and North America have shown that low birth weight is associated with increased rates of coronary heart disease in adult life (1, 2). Low birth weight is also associated with an increased prevalence of the insulin resistance syndrome, characterized by raised blood pressure, glucose intolerance, and dyslipidemia (3, 4, 5), which is known to predispose to coronary heart disease (6). Although the mechanisms are not known, it has been suggested that resetting of major hormonal axes controlling growth and development may explain these associations (7). Recent studies suggest that subtle abnormalities of the hypothalamic-pituitary-adrenal axis (HPAA) may be of particular importance in linking reduced prenatal growth with the insulin resistance syndrome in adult life. It is well established that environmental exposures in prenatal and early postnatal life may imprint the rodent HPAA, resulting in permanent modification of the neuroendocrine response to stress throughout life (8, 9). Glucocorticoids have potent biological effects, and when present in excess, for example in patients with Cushing’s disease, cause several features of the insulin resistance syndrome, including raised blood pressure, glucose intolerance, and insulin resistance (10, 11, 12). These similarities have led to the suggestion that increased HPAA activity may underlie the development of the insulin resistance syndrome (13). However, the extent to which early growth retardation may affect the HPAA in humans and whether the alterations in HPAA activity could explain the link between reduced fetal growth and the insulin resistance syndrome are not known.

We have studied a sample of men to determine whether low birth weight is associated with increased HPAA activity, as measured by accurately timed, fasting plasma cortisol concentrations, and whether variations in cortisol concentrations within the normal range are linked to insulin resistance, blood pressure, and glucose tolerance.

	Subjects and Methods

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In the county of Hertfordshire, from 1911 onward, midwives who attended the birth of a child recorded the birth weight. Weights were measured in pounds and were often rounded to the nearest half-pound or pound. As previously described (14), we traced 1157 singleton boys born in East Hertfordshire between 1920–1930 who still lived there. Of these, 845 men agreed to be interviewed at home, where their blood pressure was measured with an automated recorder (Dinamap, Critikon, Tampa, FL). Their heights were measured with a portable stadiometer, and their weights were measured with a portable (SECA Ltd, Birmingham, UK) scale. The ratio of waist to hip circumference was recorded as a marker of central obesity. The father’s occupation was used to define social class at birth, and current social class was derived from the subject’s own occupation. Smoking habits and alcohol consumption were recorded. After the home visit, the men were asked if they would be willing to attend a local clinic between 0900–0930 h in the morning after an overnight fast for a standard 75-g oral glucose tolerance test. Among the 370 men who had complete measurements for all blood samples, 66 had impaired glucose tolerance, and 27 had diabetes (14). In addition, 95 were receiving treatment with antihypertensive drugs.

We assayed cortisol in the 0900 h fasting plasma samples by RIA (15), which had an interassay coefficient of variation of between 7.4–10.3%. We measured corticosteroid-binding globulin (CBG) with a commercial assay (Medgenics Diagnostics, Fleurus, Belgium). Plasma free cortisol concentrations were estimated by the ratio of cortisol to CBG. Plasma glucose, insulin, proinsulin, 32–33 split proinsulin, high density lipoprotein cholesterol, and triglyceride concentrations were measured as we have previously described (14, 16). Homeostasis model assessment was used as an index of insulin resistance (17). The sum of the fasting insulin, proinsulin, and 32–33 split proinsulin concentrations was used to estimate the total immunoreactive insulin concentrations required in this model (18). The measurements of glucose, insulin, and triglycerides were transformed to normality using logarithms. Linear regression was used to examine the association between cortisol, birth weight, blood pressure, plasma glucose, insulin, and lipids. P refer to analyses using continuously distributed variables.

	Results

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In this sample of men, aged 59–70 yr (mean, 64 yr), the 0900 h fasting plasma cortisol concentration ranged from 112–702 nmol/L (mean, 344; SD = 112), whereas plasma CBG concentrations ranged from 23.5–86.3 mg/L (mean, 36.6; SD = 5.5). Table 1 shows that higher plasma cortisol concentrations were associated with older age and lower body mass index, but not with the waist to hip ratio. Cortisol concentrations were not associated with smoking, alcohol consumption, or social class, whether defined currently or at birth. Higher plasma cortisol concentrations were associated with higher systolic blood pressure, higher plasma glucose concentrations (fasting and 120 min after oral glucose), insulin resistance, and higher plasma triglyceride concentrations (Table 1). High density lipoprotein cholesterol concentrations fell with increasing cortisol concentrations, although this was not statistically significant (P = 0.06). These associations persisted after adjustment for age and body mass index. The trends with free plasma cortisol concentrations were similar to those with cortisol. There was no trend in low density lipoprotein concentrations with cortisol.

	Discussion

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Our data are in accord with the results of animal experiments that suggest that the HPAA can be reset by transient environment stimuli occurring during prenatal life. Thus, for example, studies of pregnant rats exposed to a variety of stressors, including low protein diets, restraint, alcohol, or nonabortive maternal infections, have shown that the offspring have increased HPAA activity with increased stress-induced corticosteroid secretion in adult life (9, 19, 20, 21). It is thought that these effects are mediated by excessive fetal glucocorticoid exposure, which results in persisting alterations in the activity of the HPAA. In rats, fetal growth retardation induced by dexamethasone leads to permanently increased activity of the HPAA with increased circulating concentrations of corticosterone (22). These changes in the axis are probably effected by a reduced number of glucocorticoid receptors in the hippocampus, which is an important site of negative feedback control (9, 23). The human evidence for this phenomenon, however, is limited to the observations that low birth weight babies have elevated cortisol concentrations in umbilical cord blood and elevated excretion of glucocorticoid metabolites in childhood (24, 25).

Although Cushing’s syndrome and glucocorticoid treatment are known to increase blood pressure and cause glucose intolerance (10, 11, 12), less is known about the effects of physiological variations in plasma cortisol concentrations. Certainly there is good evidence that cortisol concentrations similar to those observed during hypoglycemia, stress, or serious illness (>900 nmol) impair both insulin-mediated suppression of hepatic glucose output and stimulation of glucose uptake (11) as well as enhance lipolysis (26). Our findings suggest that higher cortisol concentrations within the normal range are associated with raised blood pressure, impaired glucose tolerance, insulin resistance, and raised serum triglyceride levels. Previous studies have shown positive correlations between morning plasma cortisol concentrations and fasting insulin concentrations in women (27) and blood pressure in men (28). In contrast, the insulin resistance and hyperinsulinemia of subjects with central obesity is associated with either normal or lower fasting morning plasma cortisol concentrations, albeit with increased urinary cortisol excretion (29, 30, 31, 32, 33). Our finding of an inverse relationship between plasma cortisol concentrations and current body mass index also agrees with these studies. It may be that the strength of the relationship between plasma cortisol concentrations and carbohydrate metabolism is dependent on a balance of the opposing effects of early programming vs. later obesity. Restricted fetal growth is associated with high cortisol levels, whereas adult obesity, which exacerbates insulin resistance, is associated with lower cortisol levels.

Other factors may also influence cortisol levels. By analogy with primate studies (34), which show that subordinate wild baboons have higher circulating glucocorticoid concentrations, it has been suggested that a low position in the social hierarchy, in particular a low level of control at work, and the resulting increased neuroendocrine reactivity and cortisol secretion may contribute to increased risks of cardiovascular disease (35). In the present study, however, we found no association between cortisol concentration and social class whether defined currently or at birth. This suggests that biological factors and, in particular, events in early life may be more potent modulators of the HPAA than the adult social environment.

A single fasting morning plasma cortisol concentration, even when accurately timed, is an imprecise measure of HPAA activity. Our findings are, therefore, all the more remarkable and may have underestimated the strength of the associations. However, we believe that the relationships were observed because of the large size of the study and the careful timing of samples. Our study comprised men who had complete health visitor records, who were traced and still lived in East Hertfordshire, and who were willing to take part in the study. We traced 75% of the men despite the lapse of more than 60 yr. There was no difference in the mean birth weight between men who were traced and not traced or between those who agreed to take part and those who did not. The analysis was based on internal comparisons, and bias would only be introduced if the relation between early growth and subsequent plasma cortisol concentrations differed between those who agreed to take part and those who did not; this is unlikely.

Although our observations are consistent with the hypothesis that the association between impaired fetal growth and the insulin resistance syndrome or coronary heart disease is mediated by programming of the HPAA with increased cortisol production (36), they do not establish the mechanism of the difference in plasma cortisol concentrations. Our data could be explained by alterations in the central drive to CRH secretion, altered feedback responsiveness to glucocorticoids, or alterations in cortisol metabolism. Moreover, the importance of an increased circulating level of cortisol depends on the sensitivity of peripheral tissues to cortisol. We have suggested previously that sensitivity to glucocorticoids is increased in patients with hypertension (37), and more recent data suggest that subjects with increased cortisol secretion in association with multiple cardiovascular risk factors have, if anything, increased tissue sensitivity to glucocorticoids (38). Further detailed studies of the HPAA and of glucocorticoid action in subjects of known birth measurements will determine the nature of the long term changes in glucocorticoid secretion associated with reduced fetal growth.

	Acknowledgments

 
We are grateful to C. Glenn for technical assistance.

	Footnotes

 
¹ This work was supported by the Medical Research Council, the British Heart Foundation, and Lilly Industries.

Received August 14, 1997.

Revised October 20, 1997.

Accepted December 2, 1997.

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				M. J. Holness, G. K. Greenwood, N. D. Smith, and M. C. Sugden Peroxisome Proliferator-Activated Receptor-{alpha} and Glucocorticoids Interactively Regulate Insulin Secretion During Pregnancy Diabetes, December 1, 2006; 55(12): 3501 - 3508. [Abstract] [Full Text] [PDF]

				D I. Phillips External influences on the fetus and their long-term consequences Lupus, November 1, 2006; 15(11): 794 - 800. [Abstract] [PDF]

				A. Rautanen, J. G. Eriksson, J. Kere, S. Andersson, C. Osmond, P. Tienari, H. Sairanen, D. J. P. Barker, D. I. W. Phillips, T. Forsen, et al. Associations of Body Size at Birth with Late-Life Cortisol Concentrations and Glucose Tolerance Are Modified by Haplotypes of the Glucocorticoid Receptor Gene J. Clin. Endocrinol. Metab., November 1, 2006; 91(11): 4544 - 4551. [Abstract] [Full Text] [PDF]

				C. Power, L. Li, and C. Hertzman Associations of Early Growth and Adult Adiposity with Patterns of Salivary Cortisol in Adulthood J. Clin. Endocrinol. Metab., November 1, 2006; 91(11): 4264 - 4270. [Abstract] [Full Text] [PDF]

				E. Kanitz, W. Otten, and M. Tuchscherer Changes in endocrine and neurochemical profiles in neonatal pigs prenatally exposed to increased maternal cortisol. J. Endocrinol., October 1, 2006; 191(1): 207 - 220. [Abstract] [Full Text] [PDF]

				D S Gardner, B W M Van Bon, J Dandrea, P J Goddard, S F May, V Wilson, T Stephenson, and M E Symonds Effect of periconceptional undernutrition and gender on hypothalamic-pituitary-adrenal axis function in young adult sheep. J. Endocrinol., August 1, 2006; 190(2): 203 - 212. [Abstract] [Full Text] [PDF]

				D. Qi, D. An, G. Kewalramani, Y. Qi, T. Pulinilkunnil, A. Abrahani, U. Al-Atar, S. Ghosh, R. B. Wambolt, M. F. Allard, et al. Altered cardiac fatty acid composition and utilization following dexamethasone-induced insulin resistance Am J Physiol Endocrinol Metab, August 1, 2006; 291(2): E420 - E427. [Abstract] [Full Text] [PDF]

				A. Jones, K. M. Godfrey, P. Wood, C. Osmond, P. Goulden, and D. I. W. Phillips Fetal Growth and the Adrenocortical Response to Psychological Stress J. Clin. Endocrinol. Metab., May 1, 2006; 91(5): 1868 - 1871. [Abstract] [Full Text] [PDF]

				D. I. W. Phillips and A. Jones Fetal programming of autonomic and HPA function: do people who were small babies have enhanced stress responses? J. Physiol., April 1, 2006; 572(1): 45 - 50. [Abstract] [Full Text] [PDF]

				T. Chandola, E. Brunner, and M. Marmot Chronic stress at work and the metabolic syndrome: prospective study BMJ, March 4, 2006; 332(7540): 521 - 525. [Abstract] [Full Text] [PDF]

				N van Montfoort, M J J Finken, S le Cessie, F W Dekker, and J M Wit Could cortisol explain the association between birth weight and cardiovascular disease in later life? A meta-analysis Eur. J. Endocrinol., December 1, 2005; 153(6): 811 - 817. [Abstract] [Full Text] [PDF]

				M. Baserga, M. A. Hale, R. A. McKnight, X. Yu, C. W. Callaway, and R. H. Lane Uteroplacental insufficiency alters hepatic expression, phosphorylation, and activity of the glucocorticoid receptor in fetal IUGR rats Am J Physiol Regulatory Integrative Comp Physiol, November 1, 2005; 289(5): R1348 - R1353. [Abstract] [Full Text] [PDF]

				J. R. Lindsay and L. K. Nieman The Hypothalamic-Pituitary-Adrenal Axis in Pregnancy: Challenges in Disease Detection and Treatment Endocr. Rev., October 1, 2005; 26(6): 775 - 799. [Abstract] [Full Text] [PDF]

				D. M. Sloboda, T. J. M. Moss, S. Li, D. A. Doherty, I. Nitsos, J. R. G. Challis, and J. P. Newnham Hepatic glucose regulation and metabolism in adult sheep: effects of prenatal betamethasone Am J Physiol Endocrinol Metab, October 1, 2005; 289(4): E721 - E728. [Abstract] [Full Text] [PDF]

				G. R. Small, P. W. F. Hadoke, I. Sharif, A. R. Dover, D. Armour, C. J. Kenyon, G. A. Gray, and B. R. Walker Preventing local regeneration of glucocorticoids by 11{beta}-hydroxysteroid dehydrogenase type 1 enhances angiogenesis PNAS, August 23, 2005; 102(34): 12165 - 12170. [Abstract] [Full Text] [PDF]

				M. Terzolo, S. Bovio, A. Pia, P. A. Conton, G. Reimondo, C. Dall'Asta, D. Bemporad, A. Angeli, G. Opocher, M. Mannelli, et al. Midnight serum cortisol as a marker of increased cardiovascular risk in patients with a clinically inapparent adrenal adenoma Eur. J. Endocrinol., August 1, 2005; 153(2): 307 - 315. [Abstract] [Full Text] [PDF]

				G. D. Smith, Y. Ben-Shlomo, A. Beswick, J. Yarnell, S. Lightman, and P. Elwood Cortisol, Testosterone, and Coronary Heart Disease: Prospective Evidence From the Caerphilly Study Circulation, July 19, 2005; 112(3): 332 - 340. [Abstract] [Full Text] [PDF]

				H. Hemingway, M. Shipley, E. Brunner, A. Britton, M. Malik, and M. Marmot Does Autonomic Function Link Social Position to Coronary Risk?: The Whitehall II Study Circulation, June 14, 2005; 111(23): 3071 - 3077. [Abstract] [Full Text] [PDF]

				X. Zhang, J. H. Sliwowska, and J. Weinberg Prenatal Alcohol Exposure and Fetal Programming: Effects on Neuroendocrine and Immune Function Experimental Biology and Medicine, June 1, 2005; 230(6): 376 - 388. [Abstract] [Full Text] [PDF]

				K. A. Lillycrop, E. S. Phillips, A. A. Jackson, M. A. Hanson, and G. C. Burdge Dietary Protein Restriction of Pregnant Rats Induces and Folic Acid Supplementation Prevents Epigenetic Modification of Hepatic Gene Expression in the Offspring J. Nutr., June 1, 2005; 135(6): 1382 - 1386. [Abstract] [Full Text] [PDF]

				T.-M. Hng, N. W. Cheung, and M. McLean Growth Hormone and Cortisol Dynamic Function in Relation to Birth Weight: A Study in Adult Twins J. Clin. Endocrinol. Metab., May 1, 2005; 90(5): 2781 - 2786. [Abstract] [Full Text] [PDF]

				I. C. Mcmillen and J. S. Robinson Developmental Origins of the Metabolic Syndrome: Prediction, Plasticity, and Programming Physiol Rev, April 1, 2005; 85(2): 571 - 633. [Abstract] [Full Text] [PDF]

				R. M Reynolds, B. R Walker, H. E Syddall, R. Andrew, P. J Wood, and D. I W Phillips Is there a gender difference in the associations of birthweight and adult hypothalamic-pituitary-adrenal axis activity? Eur. J. Endocrinol., February 1, 2005; 152(2): 249 - 253. [Abstract] [Full Text] [PDF]

				S. Boullu-Ciocca, A. Dutour, V. Guillaume, V. Achard, C. Oliver, and M. Grino Postnatal Diet-Induced Obesity in Rats Upregulates Systemic and Adipose Tissue Glucocorticoid Metabolism During Development and in Adulthood: Its Relationship With the Metabolic Syndrome Diabetes, January 1, 2005; 54(1): 197 - 203. [Abstract] [Full Text] [PDF]

				G. Radetti, L. Renzullo, E. Gottardi, G. D'Addato, and H. Messner Altered Thyroid and Adrenal Function in Children Born at Term and Preterm, Small for Gestational Age J. Clin. Endocrinol. Metab., December 1, 2004; 89(12): 6320 - 6324. [Abstract] [Full Text] [PDF]

				P C Souverein, A Berard, T P Van Staa, C Cooper, A C G Egberts, H G M Leufkens, and B R Walker Use of oral glucocorticoids and risk of cardiovascular and cerebrovascular disease in a population based case-control study Heart, August 1, 2004; 90(8): 859 - 865. [Abstract] [Full Text] [PDF]

				D. Qi, T. Pulinilkunnil, D. An, S. Ghosh, A. Abrahani, J. A. Pospisilik, R. Brownsey, R. Wambolt, M. Allard, and B. Rodrigues Single-Dose Dexamethasone Induces Whole-Body Insulin Resistance and Alters Both Cardiac Fatty Acid and Carbohydrate Metabolism Diabetes, July 1, 2004; 53(7): 1790 - 1797. [Abstract] [Full Text] [PDF]

				K. K. Ong, N. Potau, C. J. Petry, R. Jones, A. R. Ness, J. W. Honour, F. de Zegher, L. Ibanez, and D. B. Dunger Opposing Influences of Prenatal and Postnatal Weight Gain on Adrenarche in Normal Boys and Girls J. Clin. Endocrinol. Metab., June 1, 2004; 89(6): 2647 - 2651. [Abstract] [Full Text] [PDF]

				A L Fowden and A J Forhead Endocrine mechanisms of intrauterine programming Reproduction, May 1, 2004; 127(5): 515 - 526. [Abstract] [Full Text] [PDF]

				G. C. Patton, C. Coffey, J. B. Carlin, C. A. Olsson, and R. Morley Prematurity at birth and adolescent depressive disorder The British Journal of Psychiatry, May 1, 2004; 184(5): 446 - 447. [Abstract] [Full Text] [PDF]

				A. M. V. Ward, H. E. Syddall, P. J. Wood, G. P. Chrousos, and D. I. W. Phillips Fetal Programming of the Hypothalamic-Pituitary-Adrenal (HPA) Axis: Low Birth Weight and Central HPA Regulation J. Clin. Endocrinol. Metab., March 1, 2004; 89(3): 1227 - 1233. [Abstract] [Full Text] [PDF]

				S. Wust, E. F. C. van Rossum, I. S. Federenko, J. W. Koper, R. Kumsta, and D. H. Hellhammer Common Polymorphisms in the Glucocorticoid Receptor Gene Are Associated with Adrenocortical Responses to Psychosocial Stress J. Clin. Endocrinol. Metab., February 1, 2004; 89(2): 565 - 573. [Abstract] [Full Text] [PDF]

				M. Manikkam, E. J. Crespi, D. D. Doop, C. Herkimer, J. S. Lee, S. Yu, M. B. Brown, D. L. Foster, and V. Padmanabhan Fetal Programming: Prenatal Testosterone Excess Leads to Fetal Growth Retardation and Postnatal Catch-Up Growth in Sheep Endocrinology, February 1, 2004; 145(2): 790 - 798. [Abstract] [Full Text] [PDF]

				J. R. Seckl, N. M. Morton, K. E. Chapman, and B. R. Walker Glucocorticoids and 11beta-Hydroxysteroid Dehydrogenase in Adipose Tissue Recent Prog. Horm. Res., January 1, 2004; 59(1): 359 - 393. [Abstract] [Full Text]

				J A Jackson, M P Wailoo, J R Thompson, and S A Petersen Early physiological development of infants with intrauterine growth retardation Arch. Dis. Child. Fetal Neonatal Ed., January 1, 2004; 89(1): F46 - F50. [Abstract] [Full Text] [PDF]

				K. Herrick, D. I. W. Phillips, S. Haselden, A. W. Shiell, M. Campbell-Brown, and K. M. Godfrey Maternal Consumption of a High-Meat, Low-Carbohydrate Diet in Late Pregnancy: Relation to Adult Cortisol Concentrations in the Offspring J. Clin. Endocrinol. Metab., August 1, 2003; 88(8): 3554 - 3560. [Abstract] [Full Text] [PDF]

				N. Soto, R. A. Bazaes, V. Pena, T. Salazar, A. Avila, G. Iniguez, K. K. Ong, D. B. Dunger, and M. V. Mericq Insulin Sensitivity and Secretion Are Related to Catch-Up Growth in Small-for-Gestational-Age Infants at Age 1 Year: Results from a Prospective Cohort J. Clin. Endocrinol. Metab., August 1, 2003; 88(8): 3645 - 3650. [Abstract] [Full Text] [PDF]

				F. H. Bloomfield, M. H. Oliver, C. D. Giannoulias, P. D. Gluckman, J. E. Harding, and J. R. G. Challis Brief Undernutrition in Late-Gestation Sheep Programs the Hypothalamic-Pituitary-Adrenal Axis in Adult Offspring Endocrinology, July 1, 2003; 144(7): 2933 - 2940. [Abstract] [Full Text] [PDF]

				R. S. Lindsay, D. J. Wake, S. Nair, J. Bunt, D. E. W. Livingstone, P. A. Permana, P. A. Tataranni, and B. R. Walker Subcutaneous Adipose 11{beta}-Hydroxysteroid Dehydrogenase Type 1 Activity and Messenger Ribonucleic Acid Levels Are Associated with Adiposity and Insulinemia in Pima Indians and Caucasians J. Clin. Endocrinol. Metab., June 1, 2003; 88(6): 2738 - 2744. [Abstract] [Full Text] [PDF]

				R. A. Bazaes, T. E. Salazar, E. Pittaluga, V. Pena, A. Alegria, G. Iniguez, K. K. Ong, D. B. Dunger, and M. V. Mericq Glucose and Lipid Metabolism in Small For Gestational Age Infants at 48 Hours of Age Pediatrics, April 1, 2003; 111(4): 804 - 809. [Abstract] [Full Text] [PDF]

				S. Tenhola, E. Rahiala, A. Martikainen, P. Halonen, and R. Voutilainen Blood Pressure, Serum Lipids, Fasting Insulin, and Adrenal Hormones in 12-Year-Old Children Born with Maternal Preeclampsia J. Clin. Endocrinol. Metab., March 1, 2003; 88(3): 1217 - 1222. [Abstract] [Full Text] [PDF]

				H. Olausson, K. Uvnas-Moberg, and A. Sohlstrom Postnatal oxytocin alleviates adverse effects in adult rat offspring caused by maternal malnutrition Am J Physiol Endocrinol Metab, March 1, 2003; 284(3): E475 - E480. [Abstract] [Full Text] [PDF]

				K R Poore and A L Fowden The effect of birth weight on hypothalamo-pituitary-adrenal axis function in juvenile and adult pigs J. Physiol., February 15, 2003; 547(1): 107 - 116. [Abstract] [Full Text] [PDF]

				M. Leonhardt, J. Lesage, D. Croix, I. Dutriez-Casteloot, J. C. Beauvillain, and J. P. Dupouy Effects of Perinatal Maternal Food Restriction on Pituitary-Gonadal Axis and Plasma Leptin Level in Rat Pup at Birth and Weaning and on Timing of Puberty Biol Reprod, February 1, 2003; 68(2): 390 - 400. [Abstract] [Full Text] [PDF]

				R. C. Andrews, O. Herlihy, D. E. W. Livingstone, R. Andrew, and B. R. Walker Abnormal Cortisol Metabolism and Tissue Sensitivity to Cortisol in Patients with Glucose Intolerance J. Clin. Endocrinol. Metab., December 1, 2002; 87(12): 5587 - 5593. [Abstract] [Full Text] [PDF]

				E.J. Brunner, H. Hemingway, B.R. Walker, M. Page, P. Clarke, M. Juneja, M.J. Shipley, M. Kumari, R. Andrew, J.R. Seckl, et al. Adrenocortical, Autonomic, and Inflammatory Causes of the Metabolic Syndrome: Nested Case-Control Study Circulation, November 19, 2002; 106(21): 2659 - 2665. [Abstract] [Full Text] [PDF]

				E. Rask, B. R. Walker, S. Soderberg, D. E. W. Livingstone, M. Eliasson, O. Johnson, R. Andrew, and T. Olsson Tissue-Specific Changes in Peripheral Cortisol Metabolism in Obese Women: Increased Adipose 11{beta}-Hydroxysteroid Dehydrogenase Type 1 Activity J. Clin. Endocrinol. Metab., July 1, 2002; 87(7): 3330 - 3336. [Abstract] [Full Text] [PDF]

				C. H. D. Fall, E. Dennison, C. Cooper, J. Pringle, S. D. Kellingray, and P. Hindmarsh Does Birth Weight Predict Adult Serum Cortisol Concentrations? Twenty-Four-Hour Profiles in the United Kingdom 1920-1930 Hertfordshire Birth Cohort J. Clin. Endocrinol. Metab., May 1, 2002; 87(5): 2001 - 2007. [Abstract] [Full Text] [PDF]

				V. Grill, B. Dinesen, S. Carlsson, S. Efendic, O. Pedersen, and C.-G. Ostenson Hyperproinsulinemia and Proinsulin-to-Insulin Ratios in Swedish Middle-aged Men: Association with Glycemia and Insulin Resistance but Not with Family History of Diabetes Am. J. Epidemiol., May 1, 2002; 155(9): 834 - 841. [Abstract] [Full Text] [PDF]

				C. B. Whorwood, S. J. Donovan, D. Flanagan, D. I.W. Phillips, and C. D. Byrne Increased Glucocorticoid Receptor Expression in Human Skeletal Muscle Cells May Contribute to the Pathogenesis of the Metabolic Syndrome Diabetes, April 1, 2002; 51(4): 1066 - 1075. [Abstract] [Full Text] [PDF]

				C. L. Coe, M. Kramer, C. Kirschbaum, P. Netter, and E. Fuchs Prenatal Stress Diminishes the Cytokine Response of Leukocytes to Endotoxin Stimulation in Juvenile Rhesus Monkeys J. Clin. Endocrinol. Metab., February 1, 2002; 87(2): 675 - 681. [Abstract] [Full Text] [PDF]

				D. T. Lackland, B. M. Egan, H. E. Syddall, and D. J.P. Barker Associations Between Birth Weight and Antihypertensive Medication in Black and White Medicaid Recipients Hypertension, January 1, 2002; 39(1): 179 - 183. [Abstract] [Full Text] [PDF]

				C. Li, M. S. Johnson, and M. I. Goran Effects of Low Birth Weight on Insulin Resistance Syndrome in Caucasian and African-American Children Diabetes Care, December 1, 2001; 24(12): 2035 - 2042. [Abstract] [Full Text] [PDF]

				S. Sarkar, S.-W. Tsai, T. T. Nguyen, M. Plevyak, J. F. Padbury, and L. P. Rubin Inhibition of placental 11beta -hydroxysteroid dehydrogenase type 2 by catecholamines via alpha -adrenergic signaling Am J Physiol Regulatory Integrative Comp Physiol, December 1, 2001; 281(6): R1966 - R1974. [Abstract] [Full Text] [PDF]

				A. M Prentice Obesity and its potential mechanistic basis: Type 2 diabetes Br. Med. Bull., November 1, 2001; 60(1): 51 - 67. [Abstract] [Full Text] [PDF]

				C. E Bertram and M. A Hanson Animal models and programming of the metabolic syndrome: Type 2 diabetes Br. Med. Bull., November 1, 2001; 60(1): 103 - 121. [Abstract] [Full Text] [PDF]

				C. D Byrne Programming other hormones that affect insulin: Type 2 diabetes Br. Med. Bull., November 1, 2001; 60(1): 153 - 171. [Abstract] [Full Text] [PDF]

				C. THOMPSON, H. SYDDALL, I. RODIN, C. OSMOND, and D. J. P. BARKER Birth weight and the risk of depressive disorder in late life The British Journal of Psychiatry, November 1, 2001; 179(5): 450 - 455. [Abstract] [Full Text] [PDF]

				B. Blondeau, J. Lesage, P. Czernichow, J. P. Dupouy, and B. Breant Glucocorticoids impair fetal {beta}-cell development in rats Am J Physiol Endocrinol Metab, September 1, 2001; 281(3): E592 - E599. [Abstract] [Full Text] [PDF]

				C. Bertram, A. R. Trowern, N. Copin, A. A. Jackson, and C. B. Whorwood The Maternal Diet during Pregnancy Programs Altered Expression of the Glucocorticoid Receptor and Type 2 11{beta}-Hydroxysteroid Dehydrogenase: Potential Molecular Mechanisms Underlying the Programming of Hypertension in Utero Endocrinology, July 1, 2001; 142(7): 2841 - 2853. [Abstract] [Full Text] [PDF]

				L. A. Nolan, E. J. Hart, R. J. Windle, S. A. Wood, X. W. Hu, A. J. Levi, C. D. Ingram, and A. Levy Lack of Effect of Protein Deprivation-Induced Intrauterine Growth Retardation on Behavior and Corticosterone and Growth Hormone Secretion in Adult Male Rats: A Long-Term Follow-Up Study Endocrinology, July 1, 2001; 142(7): 2996 - 3005. [Abstract] [Full Text] [PDF]

				C. Nilsson, B.-M. Larsson, E. Jennische, E. Eriksson, P. Bjorntorp, D. A. York, and A. Holmang Maternal Endotoxemia Results in Obesity and Insulin Resistance in Adult Male Offspring Endocrinology, June 1, 2001; 142(6): 2622 - 2630. [Abstract] [Full Text] [PDF]

				C. B. Whorwood, S. J. Donovan, P. J. Wood, and D. I. W. Phillips Regulation of Glucocorticoid Receptor {{alpha}} and {beta} Isoforms and Type I 11{beta}-Hydroxysteroid Dehydrogenase Expression in Human Skeletal Muscle Cells: A Key Role in the Pathogenesis of Insulin Resistance? J. Clin. Endocrinol. Metab., May 1, 2001; 86(5): 2296 - 2308. [Abstract] [Full Text]

				R. M. Reynolds, B. R. Walker, H. E. Syddall, C. B. Whorwood, P. J. Wood, and D. I. W. Phillips Elevated Plasma Cortisol in Glucose-Intolerant Men: Differences in Responses to Glucose and Habituation to Venepuncture J. Clin. Endocrinol. Metab., March 1, 2001; 86(3): 1149 - 1153. [Abstract] [Full Text]

				D. S. Gardner, A. J. W. Fletcher, A. L. Fowden, and D. A. Giussani Plasma Adrenocorticotropin and Cortisol Concentrations during Acute Hypoxemia after a Reversible Period of Adverse Intrauterine Conditions in the Ovine Fetus During Late Gestation Endocrinology, February 1, 2001; 142(2): 589 - 598. [Abstract] [Full Text] [PDF]

				R. M. Reynolds, B. R. Walker, H. E. Syddall, R. Andrew, P. J. Wood, C. B. Whorwood, and D. I. W. Phillips Altered Control of Cortisol Secretion in Adult Men with Low Birth Weight and Cardiovascular Risk Factors J. Clin. Endocrinol. Metab., January 1, 2001; 86(1): 245 - 250. [Abstract] [Full Text]

				N. S. Levitt, E. V. Lambert, D. Woods, C. N. Hales, R. Andrew, and J. R. Seckl Impaired Glucose Tolerance and Elevated Blood Pressure in Low Birth Weight, Nonobese, Young South African Adults: Early Programming of Cortisol Axis J. Clin. Endocrinol. Metab., December 1, 2000; 85(12): 4611 - 4618. [Abstract] [Full Text]

				C. Cooper, K. Walker-Bone, N. Arden, and E. Dennison Novel insights into the pathogenesis of osteoporosis: the role of intrauterine programming Rheumatology, December 1, 2000; 39(12): 1312 - 1315. [Full Text] [PDF]

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