Maternal alcohol consumption in pregnancy enhances arterial stiffness and alters vasodilator function that varies between vascular beds in fetal sheep

Journal of Physiology

Volumn 592, Issue 12, 2014, Pages 2591-2603

  Parkington, Helena C ^a   Kenna, Kelly R ^a   Sozo, Foula ^a   Coleman, Harold A ^a   Bocking, Alan ^b   Brien, James F ^c   Harding, Richard ^a   Walker, David W ^a   Morley, Ruth ^d   Tare, Marianne ^a  

^a MONASH UNIVERSITY   (Australia)

^b UNIVERSITY OF TORONTO   (Canada)

^c QUEEN S UNIVERSITY   (Canada)

^d ROYAL CHILDREN'S HOSPITAL   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ALCOHOL; BETA ACTIN; COLLAGEN TYPE 1; COLLAGEN TYPE 2; COLLAGEN TYPE 3; ELASTASE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; MESSENGER RNA; NITRIC OXIDE SYNTHASE; RIBOSOME PROTEIN; RNA 18S; TRANSFORMING GROWTH FACTOR BETA1; TROPOELASTIN;

18S RNA GENE; ALCOHOL BLOOD LEVEL; ALCOHOL CONSUMPTION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTERIAL STIFFNESS; ARTERY BLOOD FLOW; ARTERY CONSTRICTION; ARTERY DILATATION; ARTICLE; AUTOPSY; BETA ACTIN GENE; BRAIN ARTERY; COLLAGEN I ALPHA 1 GENE; COLLAGEN I ALPHA 2 GENE; COLLAGEN III GENE; CONTROLLED STUDY; CORONARY ARTERY; CORONARY ARTERY DISEASE; DIGESTIVE TRACT BLOOD VESSEL; ELASTASE 2 GENE; ENOS GENE; FEMALE; FETUS; FETUS DEVELOPMENT; GENE; GENE EXPRESSION; GROWTH RETARDATION; KIDNEY ARTERY; LEG ARTERY; NONHUMAN; PRENATAL EXPOSURE; PRIORITY JOURNAL; S29 GENE; SHEEP; TGF BETA 1 GENE; TROPOELASTIN GENE; YOUNG MODULUS; ANIMAL; ARTERY; BRAIN; CORONARY BLOOD VESSEL; DRINKING BEHAVIOR; DRUG EFFECTS; FETOMATERNAL TRANSFUSION; GASTROINTESTINAL TRACT; KIDNEY; PHYSIOLOGY; PREGNANCY; SKELETAL MUSCLE; VASCULARIZATION; VASODILATATION;

ALCOHOL DRINKING; ANIMALS; ARTERIES; BRAIN; CORONARY VESSELS; FEMALE; FETUS; GASTROINTESTINAL TRACT; KIDNEY; MATERNAL-FETAL EXCHANGE; MUSCLE, SKELETAL; PREGNANCY; SHEEP; VASCULAR STIFFNESS; VASODILATION;

EID: 84902286354     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2013.262873     Document Type: Article

References (51)

1. Altura BM & Gebrewold A (2002). Inhibitor of nuclear factor-Kappa B activation attenuates venular constriction, leukocyte rolling-adhesion and microvessel rupture induced by ethanol in intact rat brain microcirculation: relation to ethanol-induced brain injury. Neurosci Lett 334, 21-24.
2. Andrews KL, Irvine JC, Tare M, Apostolopoulos J, Favaloro JL, Triggle CR & Kemp-Harper BK (2009). A role for nitroxyl (HNO) as an endothelium-derived relaxing and hyperpolarizing factor in resistance arteries. Br J Pharmacol 157, 540-550.
3. Assadi FK (1990). Renal tubular dysfunction in fetal alcohol syndrome. Pediatr Nephrol 4, 48-51.
4. Brien JF, Clarke DW, Richardson B & Patrick J (1985). Disposition of ethanol in maternal blood, fetal blood, and amniotic fluid of third-trimester pregnant ewes. Am J Obstet Gynecol 152, 583-590.
5. Bubb KJ, Cock ML, Black MJ, Dodic M, Boon W-M, Parkington HC, Harding R & Tare M (2007). Intrauterine growth restriction delays cardiomyocyte maturation and alters coronary artery function in the fetal sheep. J Physiol 578, 871-881.
6. Bullen ML, Miller AA, Andrews KL, Irvine JC, Ritchie RH, Sobey CG & Kemp-Harper BK (2011). Nitroxyl (HNO) as a vasoprotective signaling molecule. Antioxid Redox Signal 14, 1675-1686.
7. Chang PY, Lu SC, Lee CM, Chen YJ, Dugan TA, Huang WH, Chang SF, Liao WS, Chen CH & Lee YT (2008). Homocysteine inhibits arterial endothelial cell growth through transcriptional downregulation of fibroblast growth factor-2 involving G protein and DNA methylation. Circ Res 102, 933-941.
8. Colvin L, Payne J, Parsons D, Kurinczuk JJ & Bower C (2007). Alcohol consumption during pregnancy in nonindigenous west Australian women. Alcohol Clin Exp Res 31, 276-284.
9. Cudd TA, Chen WJ, Parnell SE & West JR (2001). Third trimester binge ethanol exposure results in fetal hypercapnea and acidemia but not hypoxemia in pregnant sheep. Alcohol Clin Exp Res 25, 269-276.
10. DeLoach SS & Townsend RR (2008). Vascular stiffness: its measurement and significance for epidemiologic and outcome studies. Clin J Am Soc Nephrol 3, 184-192.
11. Di Castelnuovo A, Costanzo S, Bagnardi V, Donati MB, Iacoviello L & de Gaetano G (2006). Alcohol dosing and total mortality in men and women: an updated meta-analysis of 34 prospective studies. Arch Intern Med 166, 2437-2445.
12. Djousse L, Lee IM, Buring JE & Gaziano JM (2009). Alcohol consumption and risk of cardiovascular disease and death in women: potential mediating mechanisms. Circulation 120, 237-244.
13. 2+ channel in chronic alcoholic subjects without cardiomyopathy. Alcohol Clin Exp Res 31, 1099-1105.
14. Fenelon G, Balbao CE, Fernandes R, Arfelli E, Landim P, Ayres O & Paola AA (2007). Characterization of the acute cardiac electrophysiologic effects of ethanol in dogs. Alcohol Clin Exp Res 31, 1574-1580.
15. Gibson A, Woodside JV, Young IS, Sharpe PC, Mercer C, Patterson CC, McKinley MC, Kluijtmans LA, Whitehead AS & Evans A (2008). Alcohol increases homocysteine and reduces B vitamin concentration in healthy male volunteers - a randomized, crossover intervention study. QJM 101, 881-887.
16. Gleason CA, Iida H, Hotchkiss KJ, Northington FJ & Traystman RJ (1997). Newborn cerebrovascular responses after first trimester moderate maternal ethanol exposure in sheep. Pediatr Res 42, 39-45.
17. Gray SP, Denton KM, Cullen-McEwen L, Bertram JF & Moritz KM (2010). Prenatal exposure to alcohol reduces nephron number and raises blood pressure in progeny. J Am Soc Nephrol 21, 1891-1902.
18. Gray SP, Kenna K, Bertram JF, Hoy WE, Yan EB, Bocking AD, Brien JF, Walker DW, Harding R & Moritz KM (2008). Repeated ethanol exposure during late gestation decreases nephron endowment in fetal sheep. Am J Physiol Regul Integr Comp Physiol 295, R568-R574.
19. Herrera EA, Verkerk MM, Derks JB & Giussani DA (2010). Antioxidant treatment alters peripheral vascular dysfunction induced by postnatal glucocorticoid therapy in rats. PLoS One 5, e9250.
20. Iveli MF, Morales S, Rebolledo A, Savietto V, Salemme S, Apezteguia M, Cecotti N, Drut R & Milesi V (2007). Effects of light ethanol consumption during pregnancy: increased frequency of minor anomalies in the newborn and altered contractility of umbilical cord artery. Pediatr Res 61, 456-461.
21. Izzard AS, Horton S, Heerkens EH, Shaw L & Heagerty AM (2006). Middle cerebral artery structure and distensibility during developing and established phases of hypertension in the spontaneously hypertensive rat. J Hypertens 24, 875-880.
22. Kenna K, De Matteo R, Hanita T, Rees S, Sozo F, Stokes V, Walker D, Bocking A, Brien J & Harding R (2011). Daily ethanol exposure during late ovine pregnancy: physiological effects in the mother and fetus in the apparent absence of overt fetal cerebral dysmorphology. Am J Physiol Regul Integr Comp Physiol 301, R926-R936.
23. Klatsky AL (2009). Alcohol and cardiovascular diseases. Expert Rev Cardiovasc Ther 7, 499-506.
24. Kurihara T, Tomiyama H, Hashimoto H, Yamamoto Y, Yano E & Yamashina A (2004). Excessive alcohol intake increases the risk of arterial stiffening in men with normal blood pressure. Hypertens Res 27, 669-673.
25. Kvigne VL, Leonardson GR, Neff-Smith M, Brock E, Borzelleca J & Welty TK (2004). Characteristics of children who have full or incomplete fetal alcohol syndrome. J Pediatr 145, 635-640.
26. Lamireau D, Nuyt AM, Hou X, Bernier S, Beauchamp M, Gobeil F Jr, Lahaie I, Varma DR & Chemtob S (2002). Altered vascular function in fetal programming of hypertension. Stroke 33, 2992-2998.
27. Laurent S, Boutouyrie P, Asmar R, Gautier I, Laloux B, Guize L, Ducimetiere P & Benetos A (2001). Aortic stiffness is an independent predictor of all-cause and cardiovascular mortality in hypertensive patients. Hypertension 37, 1236-1241.
28. Lutz UC (2008). Alterations in homocysteine metabolism among alcohol dependent patients - clinical, pathobiochemical and genetic aspects. Curr Drug Abuse Rev 1, 47-55.
29. Martyn CN & Greenwald SE (1997). Impaired synthesis of elastin in walls of aorta and large conduit arteries during early development as an initiating event in pathogenesis of systemic hypertension. Lancet 350, 953-955.
30. Martyn CN & Greenwald SE (2001). A hypothesis about a mechanism for the programming of blood pressure and vascular disease in early life. Clin Exp Pharmacol Physiol 28, 948-951.
31. Mazzuca MQ, Wlodek ME, Dragomir NM, Parkington HC & Tare M (2010). Uteroplacental insufficiency programs regional vascular dysfunction and alters arterial stiffness in female offspring. J Physiol 588, 1997-2010.
32. Moore S, Shepherd J, Perham N & Cusens B (2007). The prevalence of alcohol intoxication in the night-time economy. Alcohol Alcohol 42, 629-634.
33. Morley R, Dwyer T, Hynes KL, Cochrane J, Ponsonby AL, Parkington HC & Carlin JB (2010). Maternal alcohol intake and offspring pulse wave velocity. Neonatology 97, 204-211.
34. Parnell SE, Ramadoss J, Delp MD, Ramsey MW, Chen WJ, West JR & Cudd TA (2007). Chronic ethanol increases fetal cerebral blood flow specific to the ethanol-sensitive cerebellum under normoxaemic, hypercapnic and acidaemic conditions: ovine model. Exp Physiol 92, 933-943.
35. Payne JA, Alexander BT & Khalil RA (2003). Reduced endothelial vascular relaxation in growth-restricted offspring of pregnant rats with reduced uterine perfusion. Hypertension 42, 768-774.
36. Piano MR, Geenen DL, Schwertz DW, Chowdhury SA & Yuzhakova M (2007). Long-term effects of alcohol consumption in male and female rats. Cardiovasc Toxicol 7, 247-254.
37. Poston L (2007). Influences of maternal nutritional status on vascular function in the offspring. Curr Drug Targets 8, 914-922.
38. Prevention CfDCa (2010). Fetal alcohol spectrum disorders. http://www.cdc.gov/ncbddd/fasd/data.html.
39. Pruett D, Waterman EH & Caughey AB (2013). Fetal alcohol exposure: consequences, diagnosis, and treatment. Obstet Gynecol Surv 68, 62-69.
40. Ramadoss J & Magness RR (2012). Vascular effects of maternal alcohol consumption. Am J Physiol Heart Circ Physiol 303, H414-H421.
41. Taylor CL, Jones KL, Jones MC & Kaplan GW (1994). Incidence of renal anomalies in children prenatally exposed to ethanol. Pediatrics 94, 209-212.
42. Tikkanen J & Heinonen OP (1991). Maternal exposure to chemical and physical factors during pregnancy and cardiovascular malformations in the offspring. Teratology 43, 591-600.
43. Tirapelli CR, Casolari DA, Montezano AC, Yogi A, Tostes RC, Legros E, D'Orleans-Juste P, Lanchote VL, Uyemura SA & de Oliveira AM (2006). Ethanol consumption enhances endothelin-1-induced contraction in the isolated rat carotid. J Pharmacol Exp Ther 318, 819-827.
44. Turcotte LA, Aberle NS, Norby FL, Wang GJ & Ren J (2002). Influence of prenatal ethanol exposure on vascular contractile response in rat thoracic aorta. Alcohol 26, 75-81.
45. van Driel LM, de Jonge R, Helbing WA, van Zelst BD, Ottenkamp J, Steegers EA & Steegers-Theunissen RP (2008). Maternal global methylation status and risk of congenital heart diseases. Obstet Gynecol 112, 277-283.
46. van Trijp MJ, Beulens JW, Bos WJ, Uiterwaal CS, Grobbee DE, Hendriks HF & Bots ML (2005). Alcohol consumption and augmentation index in healthy young men: the ARYA study. Am J Hypertens 18, 792-796.
47. Vanhoutte PM, Shimokawa H, Tang EH & Feletou M (2009). Endothelial dysfunction and vascular disease. Acta Physiol 196, 193-222.
48. Wigg SJ, Tare M, Forbes J, Cooper ME, Thomas MC, Coleman HA, Parkington HC & O'Brien RC (2004). Early vitamin E supplementation attenuates diabetes-associated vascular dysfunction and the rise in protein kinase C-β in mesenteric artery and ameliorates wall stiffness in femoral artery in rats. Diabetologia 47, 1038-1046.
49. Yang ZW, Wang J, Zheng T, Altura BT & Altura BM (2001). Ethanol-induced contractions in cerebral arteries: role of tyrosine and mitogen-activated protein kinases. Stroke 32, 249-257.
50. Yeligar S, Tsukamoto H & Kalra VK (2009). Ethanol-induced expression of ET-1 and ET-BR in liver sinusoidal endothelial cells and human endothelial cells involves hypoxia-inducible factor-1alpha and microrNA-199. J Immunol 183, 5232-5243.
51. Zieman SJ, Melenovsky V & Kass DA (2005). Mechanisms, pathophysiology, and therapy of arterial stiffness. Arterioscler Thromb Vasc Biol 25, 932-943.