Elevated maternal cortisol leads to relative maternal hyperglycemia and increased stillbirth in ovine pregnancy

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 307, Issue 4, 2014, Pages

  Keller Wood, Maureen ^a   Feng, Xiaodi ^a   Wood, Charles E ^a   Richards, Elaine ^a   Anthony, Russell V ^b   Dahl, Geoffrey E ^a   Tao, Sha ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

Cortisol; Glucose; Insulin; Pregnancy

Indexed keywords

3 HYDROXYBUTYRIC ACID; ELECTROLYTE; ESTRONE; FATTY ACID; GLUCOSE; HYDROCORTISONE; INSULIN; PLACENTA LACTOGEN; PROGESTERONE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIRTH; CONTROLLED STUDY; EWE; FEMALE; FETUS DEATH; FETUS GROWTH; FETUS OUTCOME; FETUS WEIGHT; FOOD INTAKE; GLUCOSE BLOOD LEVEL; GLUCOSE HOMEOSTASIS; HYDROCORTISONE BLOOD LEVEL; HYPERGLYCEMIA; INSULIN BLOOD LEVEL; MATERNAL DIABETES MELLITUS; NONHUMAN; ORGAN WEIGHT; POST HOC ANALYSIS; PREGNANCY; PREGNANCY OUTCOME; PRIORITY JOURNAL; SHEEP; STILLBIRTH;

CORTISOL; GLUCOSE; INSULIN; PREGNANCY;

ANIMALS; BLOOD GLUCOSE; CUSHING SYNDROME; DIABETES, GESTATIONAL; DISEASE MODELS, ANIMAL; ENERGY METABOLISM; FEMALE; FETAL BLOOD; FETAL DEATH; GESTATIONAL AGE; HOMEOSTASIS; HYDROCORTISONE; HYPERGLYCEMIA; INFUSIONS, INTRAVENOUS; INSULIN; MATERNAL EXPOSURE; PLACENTA; PREGNANCY; SHEEP; STILLBIRTH; TIME FACTORS;

EID: 84907666198     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00530.2013     Document Type: Article

References (38)

1. Arumugam R, Horowitz E, Lu D, Collier JJ, Ronnebaum S, Fleenor D, Freemark M. The interplay of prolactin and the glucocorticoids in the regulation of β-cell gene expression, fatty acid oxidation, and glucosestimulated insulin secretion: implications for carbohydrate metabolism in pregnancy. Endocrinology 149: 5401-5414, 2008.
2. Balli S, Pac FA, Ece I, Oflaz MB, Kibar AE, Kandemir O. Assessment of cardiac functions in fetuses of gestational diabetic mothers. Pediatr Cardiol 35: 30-37, 2014.
3. Coletta J, Simpson LL. Maternal medical disease and stillbirth. Clin Obstet Gynecol 53: 607-616, 2010.
4. Debono M, Chadarevian R, Eastell R, Ross RJ, Newell-Price J. Mifepristone reduces insulin resistance in patient volunteers with adrenal incidentalomas that secrete low levels of cortisol: a pilot study. PLoS One 8: e60984, 2013.
5. Delaunay F, Khan A, Cintra A, Davani B, Ling ZC, Andersson A, Ostenson CG, Gustafsson J, Efendic S, Okret S. Pancreatic β cells are important targets for the diabetogenic effects of glucocorticoids. J Clin Invest 100: 2094-2098, 1997.
6. Dudley DJ. Diabetic-associated stillbirth: incidence, pathophysiology, and prevention. Obstet Gynecol Clin North Am 34: 293-307, ix, 2007.
7. Feng X, Reini S, Richards E, Wood CE, Keller-Wood M. Cortisol stimulates proliferation and apoptosis in the late gestation fetal heart: differential effects of mineralocorticoid and glucocorticoid receptors. Am J Physiol Regul Integr Comp Physiol 305: R343-R350, 2013.
8. Fleseriu M, Biller BM, Findling JW, Molitch ME, Schteingart DE, Gross C. Mifepristone, a glucocorticoid receptor antagonist, produces clinical and metabolic benefits in patients with Cushing's syndrome. J Clin Endocrinol Metab 97: 2039-2049, 2012.
9. Fletcher AJ, Gardner DS, Edwards CM, Fowden AL, Giussani DA. Cardiovascular and endocrine responses to acute hypoxaemia during and following dexamethasone infusion in the ovine fetus. J Physiol 549: 271-287, 2003.
10. Harding R, Poore ER. The effects of myometrial activity on fetal thoracic dimensions and uterine blood flow during late gestation in the sheep. Biol Neonate 45: 244-251, 1984.
11. Jellyman JK, Gardner DS, Edwards CM, Fowden AL, Giussani DA. Fetal cardiovascular, metabolic and endocrine responses to acute hypoxaemia during and following maternal treatment with dexamethasone in sheep. J Physiol 567: 673-688, 2005.
12. Jensen E, Wood C, Keller-Wood M. The normal increase in adrenal secretion during pregnancy contributes to maternal volume expansion and fetal homeostasis. J Soc Gynecol Investig 9: 362-371, 2002.
13. Jensen E, Wood CE, Keller-Wood M. Chronic alterations in ovine maternal corticosteroid levels influence uterine blood flow and placental and fetal growth. Am J Physiol Regul Integr Comp Physiol 288: R54-R61, 2005.
14. Kappes SM, Warren WC, Pratt SL, Liang R, Anthony RV. Quantification and cellular localization of ovine placental lactogen messenger ribonucleic acid expression during mid-and late gestation. Endocrinology 131: 2829-2838, 1992.
15. Kawai A, Kuzuya N. On the role of glucocorticoid in glucose-induced insulin secretion. Horm Metab Res 9: 361-365, 1977.
16. Lea RG, Wooding P, Stewart I, Hannah LT, Morton S, Wallace K, Aitken RP, Milne JS, Regnault TR, Anthony RV, Wallace JM. The expression of ovine placental lactogen, StAR and progesterone-associated steroidogenic enzymes in placentae of overnourished growing adolescent ewes. Reproduction 133: 785-796, 2007.
17. Lindsay JR, Jonklaas J, Oldfield EH, Nieman LK. Cushing's syndrome during pregnancy: personal experience and review of the literature. J Clin Endocrinol Metab 90: 3077-3083, 2005.
18. Ma R, Liu J, Wu L, Sun J, Yang Z, Yu C, Yuan P, Xiao X. Differential expression of placental 11β-hydroxysteroid dehydrogenases in pregnant women with diet-treated gestational diabetes mellitus. Steroids 77: 798-805, 2012.
19. Mace S, Hirschfield SS, Riggs T, Fanaroff AA, Merkatz IR. Echocardiographic abnormalities in infants of diabetic mothers. J Pediatr 95: 1013-1019, 1979.
20. Makino I, Matsuda Y, Yoneyama M, Hirasawa K, Takagi K, Ohta H, Konishi Y. Effect of maternal stress on fetal heart rate assessed by vibroacoustic stimulation. J Int Med Res 37: 1780-1788, 2009.
21. Mathiesen ER, Ringholm L, Damm P. Stillbirth in diabetic pregnancies. Best Pract Res Clin Obstet Gynaecol 25: 105-111, 2011.
22. Moss TJ, Nitsos I, Harding R, Newnham JP. Differential effects of maternal and fetal betamethasone injections in late-gestation fetal sheep. J Soc Gynecol Investig 10: 474-479, 2003.
23. Moss TJ, Sloboda DM, Gurrin LC, Harding R, Challis JR, Newnham JP. Programming effects in sheep of prenatal growth restriction and glucocorticoid exposure. Am J Physiol Regul Integr Comp Physiol 281: R960-R970, 2001.
24. Nosadini R, Del PS, Tiengo A, Valerio A, Muggeo M, Opocher G, Mantero F, Duner E, Marescotti C, Mollo F, Belloni F. Insulin resistance in Cushing's syndrome. J Clin Endocrinol Metab 57: 529-536, 1983.
25. Nyirenda MJ, Lindsay RS, Kenyon CJ, Burchell A, Seckl JR. Glucocorticoid exposure in late gestation permanently programs rat hepatic phosphoenolpyruvate carboxykinase and glucocorticoid receptor expression and causes glucose intolerance in adult offspring. J Clin Invest 101: 2174-2181, 1998.
26. Pickard J, Jochen AL, Sadur CN, Hofeldt FD. Cushing's syndrome in pregnancy. Obstet Gynecol Surv 45: 87-93, 1990.
27. Regnault TR, Oddy HV, Nancarrow C, Sriskandarajah N, Scaramuzzi RJ. Glucose-stimulated insulin response in pregnant sheep following acute suppression of plasma non-esterified fatty acid concentrations. Reprod Biol Endocrinol 2: 64, 2004.
28. Reini SA, Dutta G, Wood CE, Keller-Wood M. Cardiac corticosteroid receptors mediate the enlargement of the ovine fetal heart induced by chronic increases in maternal cortisol. J Endocrinol 198: 419-427, 2008.
29. Richards EM, Wood CE, Rabaglino MB, Antolic A, Keller-Wood M. Mechanisms for the adverse effects of late gestational increases in maternal cortisol on the heart revealed by transcriptomic analyses of the fetal septum. Physiol Genomics 46: 398-410, 2014.
30. Rueda BR, Dunn TG, Anthony RV, Moss GE. Influence of fetal death and fetectomy on gestation and the initiation of parturition in the ewe. Reprod Fertil Dev 7: 1221-1225, 1995.
31. Schafer-Graf UM, Wockel A. [Severe diabetic fetopathy due to undiagnosed gestational diabetes mellitus]. Dtsch Med Wochenschr 131: 1151-1154, 2006.
32. Sutherland HW, Fisher PM. Fetal loss and maternal glucose intolerance. A retrospective study. Padiatr Padol 17: 279-286, 1982.
33. Swali A, Walker EA, Lavery GG, Tomlinson JW, Stewart PM. 11β-Hydroxysteroid dehydrogenase type 1 regulates insulin and glucagon secretion in pancreatic islets. Diabetologia 51: 2003-2011, 2008.
34. Trainer PJ. Corticosteroids and pregnancy. Semin Reprod Med 20: 375-380, 2002.
35. Vilar L, Freitas MC, Lima LH, Lyra R, Kater CE. Cushing's syndrome in pregnancy: an overview. Arq Bras Endocrinol Metabol 51: 1293-1302, 2007.
36. Ward JW, Wooding FB, Fowden AL. The effects of cortisol on the binucleate cell population in the ovine placenta during late gestation. Placenta 23: 451-458, 2002.
37. Yli BM, Kallen K, Khoury J, Stray-Pedersen B, Amer-Wahlin I. Intrapartum cardiotocography (CTG) and ST-analysis of labor in diabetic patients. J Perinat Med 39: 457-465, 2011.
38. Yli BM, Kallen K, Stray-Pedersen B, Amer-Wahlin I. Intrapartum fetal ECG and diabetes. J Matern Fetal Neonatal Med 21: 231-238, 2008.