A rodent model of low- to moderate-dose ethanol consumption during pregnancy: patterns of ethanol consumption and effects on fetal and offspring growth
Megan E. Probyn A D , Simone Zanini A , Leigh C. Ward B , John F. Bertram C and Karen M. Moritz A
+ Author Affiliations
- Author Affiliations
A School of Biomedical Sciences, The University of Queensland, St Lucia, Qld 4072, Australia.
B School of Chemistry and Molecular Biosciences, The University of Queensland, St Lucia, Qld 4072, Australia.
C Department of Anatomy and Developmental Biology, Monash University, Clayton, Vic. 3800, Australia.
D Corresponding author. Email: m.probyn@uq.edu.au
Reproduction, Fertility and Development 24(6) 859-870 https://doi.org/10.1071/RD11200
Submitted: 10 August 2011 Accepted: 23 January 2012 Published: 24 February 2012
Abstract
It is unknown whether low to moderate maternal alcohol consumption adversely affects postnatal health. The aim of the present study was to develop a rodent model of low–moderate-dose prenatal ethanol (EtOH) exposure. Sprague-Dawley rats were fed a liquid diet with or without 6% v/v EtOH throughout gestation and the pattern of dietary consumption determined. Fetal bodyweights and hepatic alcohol-metabolising gene expression were measured on embryonic Day (E) 20 and offspring growth studied until 1 year. At E8 the plasma EtOH concentration was 0.03%. There was little difference in dietary consumption between the two treatment groups. At E20, EtOH-exposed fetuses were significantly lighter than controls and had significantly decreased ADH4 and increased CYP2E1 gene expression. Offspring killed on postnatal Day (PN) 30 did not exhibit any growth deficits. Longitudinal repeated measures of offspring growth demonstrated slower growth in males from EtOH-fed dams between 7 and 12 months of age; a cohort of male pups killed at 8 months of age had a reduced crown–rump length and kidney weight. In conclusion, a liquid diet of 6% v/v EtOH fed to pregnant dams throughout gestation caused a 3–8% reduction in fetal growth and brain sparing, with growth differences observed in male offspring later in life. This model will be useful for future studies on the effects of low–moderate EtOH on the developmental origins of health and disease.
Additional keywords: ethanol, fetus, offspring, postnatal growth, pregnancy, rat.
References
Abel, E. L., and Dintcheff, B. A. (1978). Effects of prenatal alcohol exposure on growth and development in rats. J. Pharmacol. Exp. Ther. 207, 916–921.| 1:CAS:528:DyaE1MXotFyktw%3D%3D&md5=cf424f5cd24c79070c2cc28396abde31CAS | 731439PubMed |
Barker, D. J. (2007). The origins of the developmental origins theory. J. Intern. Med. 261, 412–417.
| The origins of the developmental origins theory.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2s3js1CqsA%3D%3D&md5=bef140a6d9e27d08698b44675b720c05CAS | 17444880PubMed |
Barker, D. J., and Osmond, C. (1986). Infant mortality, childhood nutrition, and ischaemic heart disease in England and Wales. The Lancet 327, 1077–1081.
| Infant mortality, childhood nutrition, and ischaemic heart disease in England and Wales.Crossref | GoogleScholarGoogle Scholar |
Barker, D. J., Hales, C. N., Fall, C. H., Osmond, C., Phipps, K., and Clark, P. M. (1993). Type 2 (non-insulin-dependent) diabetes mellitus, hypertension and hyperlipidaemia (syndrome X): relation to reduced fetal growth. Diabetologia 36, 62–67.
| Type 2 (non-insulin-dependent) diabetes mellitus, hypertension and hyperlipidaemia (syndrome X): relation to reduced fetal growth.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3s7ntVKjuw%3D%3D&md5=8de53fce0b2e5757a58f69baaeff1fabCAS | 8436255PubMed |
Boé, D. M., Richens, T. R., Horstmann, S. A., Burnham, E. L., Janssen, W. J., Henson, P. M., Moss, M., and Vandivier, R. W. (2010). Acute and chronic alcohol exposure impair the phagocytosis of apoptotic cells and enhance the pulmonary inflammatory response. Alcohol. Clin. Exp. Res , .
| Acute and chronic alcohol exposure impair the phagocytosis of apoptotic cells and enhance the pulmonary inflammatory response.Crossref | GoogleScholarGoogle Scholar | 20608904PubMed |
Bond, N. W. (1982). Prenatal exposure to ethanol: association between increased gestational length and offspring mortality. Neurobehav. Toxicol. Teratol. 4, 501–503.
| 1:CAS:528:DyaL3sXivFGgsg%3D%3D&md5=6421076beab0c6cbc07878f618c9e083CAS | 7177299PubMed |
Campbell, M. A., and Fantel, A. G. (1983). Teratogenicity of acetaldehyde in vitro: relevance to the fetal alcohol syndrome. Life Sci. 32, 2641–2647.
| Teratogenicity of acetaldehyde in vitro: relevance to the fetal alcohol syndrome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXktVWlur8%3D&md5=fb4d6bc3e2caa1104faf3d33d93b4d45CAS | 6855459PubMed |
Chen, J. S., Driscoll, C. D., and Riley, E. P. (1982). Ontogeny of suckling behavior in rats prenatally exposed to alcohol. Teratology 26, 145–153.
| Ontogeny of suckling behavior in rats prenatally exposed to alcohol.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXivFGhuw%3D%3D&md5=870726290f807156a94d0c13ca84f3c3CAS | 7157191PubMed |
Chen, L., and Nyomba, B. L. (2003). Effects of prenatal alcohol exposure on glucose tolerance in the rat offspring. Metabolism 52, 454–462.
| Effects of prenatal alcohol exposure on glucose tolerance in the rat offspring.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjtVKitbY%3D&md5=16b8cd1af4226a2332c0fb59fe48fcb4CAS | 12701058PubMed |
Curhan, G. C., Willett, W. C., Rimm, E. B., Spiegelman, D., Ascherio, A. L., and Stampfer, M. J. (1996). Birth weight and adult hypertension, diabetes mellitus, and obesity in US men. Circulation 94, 3246–3250.
| 1:STN:280:DyaK2s7ktlWhtw%3D%3D&md5=a1bac874f6ed12de5cbe123a7e11230cCAS | 8989136PubMed |
Detering, N., Reed, W. D., Ozand, P. T., and Karahasan, A. (1979). The effects of maternal ethanol consumption in the rat on the development of their offspring. J. Nutr. 109, 999–1009.
| 1:CAS:528:DyaE1MXkvVCktbk%3D&md5=bee0c81d387158b46fe588622d2afa1dCAS | 448456PubMed |
Dodic, M., May, C. N., Wintour, E. M., and Coghlan, J. P. (1998). An early prenatal exposure to excess glucocorticoid leads to hypertensive offspring in sheep. Clin. Sci. 94, 149–155.
| 1:CAS:528:DyaK1cXht1yms7o%3D&md5=fa29c21b5aad9ba7239e01757753a555CAS | 9536923PubMed |
Gatford, K. L., Dalitz, P. A., Cock, M. L., Harding, R., and Owens, J. A. (2007). Acute ethanol exposure in pregnancy alters the insulin-like growth factor axis of fetal and maternal sheep. Am. J. Physiol. Endocrinol. Metab. 292, E494–E500.
| Acute ethanol exposure in pregnancy alters the insulin-like growth factor axis of fetal and maternal sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjt1Gls7c%3D&md5=8739108a8abfcf01c45a14111f813dfeCAS | 17003241PubMed |
Giglia, R. C., and Binns, C. W. (2008). Alcohol, pregnancy and breastfeeding; a comparison of the 1995 and 2001 National Health Survey data. Breastfeed. Rev. 16, 17–24.
| 18546573PubMed |
Godfrey, K. M., and Barker, D. J. (2000). Fetal nutrition and adult disease. Am. J. Clin. Nutr. 71, 1344S–1352S.
| 1:CAS:528:DC%2BD3cXivFymurY%3D&md5=ee96bd785faaf7838d4a77b40d4132a4CAS | 10799412PubMed |
Gray, S. P., Kenna, K., Bertram, J. F., Hoy, W. E., Yan, E. B., Bocking, A. D., Brien, J. F., Walker, D. W., Harding, R., and Moritz, K. M. (2008). Repeated ethanol exposure during late gestation decreases nephron endowment in fetal sheep. Am. J. Physiol. Regul. Integr. Comp. Physiol. 295, R568–R574.
| Repeated ethanol exposure during late gestation decreases nephron endowment in fetal sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVakt7bO&md5=718d0a99d8e4e37aa1c76311e3d84545CAS | 18565833PubMed |
Gray, S. P., Denton, K. M., Cullen-McEwen, L., Bertram, J. F., and Moritz, K. M. (2010). Prenatal exposure to alcohol reduces nephron number and raises blood pressure in progeny. J. Am. Soc. Nephrol. 21, 1891–1902.
| Prenatal exposure to alcohol reduces nephron number and raises blood pressure in progeny.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFCnsrbI&md5=6824184161c743d7540bb93ed9f6e405CAS | 20829403PubMed |
Hales, C. N., and Ozanne, S. E. (2003). For debate: fetal and early postnatal growth restriction lead to diabetes, the metabolic syndrome and renal failure. Diabetologia 46, 1013–1019.
| For debate: fetal and early postnatal growth restriction lead to diabetes, the metabolic syndrome and renal failure.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3szmtlSgsQ%3D%3D&md5=a19a2de95129c3cc6062da074001c05cCAS | 12827239PubMed |
Harkness, J. E., and Wagner, J. E. (1989). ‘The Biology and Medicine of Rabbits and Rodents.’ (Lea & Febiger: London.)
Harvey, N., and Cooper, C. (2004). The developmental origins of osteoporotic fracture. J. Br. Menopause Soc. 10, 14–29.
| The developmental origins of osteoporotic fracture.Crossref | GoogleScholarGoogle Scholar | 15107206PubMed |
International Center for Alcohol Policies (1995–2009) Annex 1. The basics about alcohol. In ‘ICAP Blue Book’. Available at http://www.icap.org/PolicyTools/ICAPBlueBook/Annex1TheBasicsaboutAlcohol/tabid/116/Default.aspx [Verified 2 February 2012].
Keppen, L. D., Pysher, T., and Rennert, O. M. (1985). Zinc deficiency acts as a co-teratogen with alcohol in fetal alcohol syndrome. Pediatr. Res. 19, 944–947.
| Zinc deficiency acts as a co-teratogen with alcohol in fetal alcohol syndrome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXltlKqsL0%3D&md5=dca4e9a4ed732a2e18e11c5013e8f46cCAS | 4047764PubMed |
Langley-Evans, S. C., Welham, S. J., and Jackson, A. A. (1999). Fetal exposure to a maternal low protein diet impairs nephrogenesis and promotes hypertension in the rat. Life Sci. 64, 965–974.
| Fetal exposure to a maternal low protein diet impairs nephrogenesis and promotes hypertension in the rat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhsFelsL8%3D&md5=c1d9701ed1f0fe79b076782eeef10cf2CAS | 10201645PubMed |
Lee, R. D., An, S. M., Kim, S. S., Rhee, G. S., Kwack, S. J., Seok, J. H., Chae, S. Y., Park, C. H., Choi, Y. W., Kim, H. S., Cho, H. Y., Lee, B. M., and Park, K. L. (2005). Neurotoxic effects of alcohol and acetaldehyde during embryonic development. J. Toxicol. Environ. Health A 68, 2147–2162.
| Neurotoxic effects of alcohol and acetaldehyde during embryonic development.Crossref | GoogleScholarGoogle Scholar | 16326430PubMed |
Lieber, C. S., and DeCarli, L. M. (1982). The feeding of alcohol in liquid diets: two decades of applications and 1982 update. Alcohol. Clin. Exp. Res. 6, 523–531.
| The feeding of alcohol in liquid diets: two decades of applications and 1982 update.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXjtlCnsQ%3D%3D&md5=0c9e7d16a9d8109ad6667868e65e3378CAS | 6758624PubMed |
Lieber, C. S., and DeCarli, L. M. (1989). Liquid diet technique of ethanol administration: 1989 update. Alcohol Alcohol. 24, 197–211.
| 1:CAS:528:DyaL1MXlt1yhur4%3D&md5=31930bd46ac6115b2f2648db03020a46CAS | 2667528PubMed |
Louey, S., Cock, M. L., Stevenson, K. M., and Harding, R. (2000). Placental insufficiency and fetal growth restriction lead to postnatal hypotension and altered postnatal growth in sheep. Pediatr. Res. 48, 808–814.
| Placental insufficiency and fetal growth restriction lead to postnatal hypotension and altered postnatal growth in sheep.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M7hsVGrtQ%3D%3D&md5=18451e9b344776b1543c3443e9f73578CAS | 11102551PubMed |
Lucas, J. S., Inskip, H. M., Godfrey, K. M., Foreman, C. T., Warner, J. O., Gregson, R. K., and Clough, J. B. (2004). Small size at birth and greater postnatal weight gain: relationships to diminished infant lung function. Am. J. Respir. Crit. Care Med. 170, 534–540.
| Small size at birth and greater postnatal weight gain: relationships to diminished infant lung function.Crossref | GoogleScholarGoogle Scholar | 15172897PubMed |
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.
| Prenatal dexamethasone programs hypertension and renal injury in the rat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXnsFShsQ%3D%3D&md5=8b793ddfd5e1d4bab1254acde0c804dcCAS | 12574103PubMed |
Pikkarainen, P. H., and Raiha, N. C. (1967). Development of alcohol dehydrogenase activity in the human liver. Pediatr. Res. 1, 165–168.
| Development of alcohol dehydrogenase activity in the human liver.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF1cXhvV2qsg%3D%3D&md5=5ddc6b6ef3f8140d8c3b04bd2b1c295bCAS | 6080860PubMed |
Raiha, N. C., Koskinen, M., and Pikkarainen, P. (1967). Developmental changes in alcohol-dehydrogenase activity in rat and guinea-pig liver. Biochem. J. 103, 623–626.
| 1:CAS:528:DyaF2sXhtFels70%3D&md5=875e99e7651d715f9126fc75937cea96CAS | 6069164PubMed |
Robinson, R. S., and Seelig, L. L. (2002). Effects of maternal ethanol consumption on hematopoietic cells in the rat fetal liver. Alcohol 28, 151–156.
| Effects of maternal ethanol consumption on hematopoietic cells in the rat fetal liver.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmsFahsg%3D%3D&md5=236f47d14997486182b3c17e1081e9d1CAS | 12551756PubMed |
Rockwood, G. A., and Riley, E. P. (1986). Suckling deficits in rat pups exposed to alcohol in utero. Teratology 33, 145–151.
| Suckling deficits in rat pups exposed to alcohol in utero.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28Xit1Smtbo%3D&md5=498df8625b6df7947a0f662f846cf7d8CAS | 3738815PubMed |
Roseboom, T. J., van der Meulen, J. H., Osmond, C., Barker, D. J., Ravelli, A. C., Schroeder-Tanka, J. M., van Montfrans, G. A., Michels, R. P., and Bleker, O. P. (2000). Coronary heart disease after prenatal exposure to the Dutch famine, 1944–45. Heart 84, 595–598.
| Coronary heart disease after prenatal exposure to the Dutch famine, 1944–45.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M%2FksFeqsQ%3D%3D&md5=bf87dbdeafe1ac021654efb98593671bCAS | 11083734PubMed |
Rudeen, P. K., Kappel, C. A., and Lear, K. (1986). Postnatal or in utero ethanol exposure reduction of the volume of the sexually dimorphic nucleus of the preoptic area in male rats. Drug Alcohol Depend. 18, 247–252.
| Postnatal or in utero ethanol exposure reduction of the volume of the sexually dimorphic nucleus of the preoptic area in male rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXhsFWgur4%3D&md5=aaa8f18340ff58935f23c6038301a78bCAS | 3803195PubMed |
Sanchis, R., and Guerri, C. (1986a). Alcohol-metabolizing enzymes in placenta and fetal liver: effect of chronic ethanol intake. Alcohol. Clin. Exp. Res. 10, 39–44.
| Alcohol-metabolizing enzymes in placenta and fetal liver: effect of chronic ethanol intake.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28XhsVeksb0%3D&md5=b0bc413ebeec3022108ef633b301fac6CAS | 3515990PubMed |
Sanchis, R., Sancho-Tello, M., and Guerri, C. (1986b). The effects of chronic alcohol consumption on pregnant rats and their offspring. Alcohol Alcohol. 21, 295–305.
| 1:CAS:528:DyaL28Xmt1SkurY%3D&md5=917408bff8b839890565c5cf2091e35bCAS | 3768104PubMed |
Sigh, S. P., and Snyder, A. K. (1982). Ethanol ingestion during pregnancy: effects on pregnant rats and their offspring. J. Nutr. 112, 98–103.
| 1:CAS:528:DyaL38XpvFajug%3D%3D&md5=12fce1ce6f3ea551a4f72c8428a4fe07CAS | 7054474PubMed |
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.
| Prenatal corticosterone exposure results in altered AT1/AT2, nephron deficit and hypertension in the rat offspring.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjvVSgsbc%3D&md5=3c878637cb799fb9234300d976da9f06CAS | 17204493PubMed |
Sjoblom, M., Pilstrom, L., and Morland, J. (1978). Activity of alcohol dehydrogenase and acetaldehyde dehydrogenases in the liver and placenta during the development of the rat. Enzyme 23, 108–115.
| 1:CAS:528:DyaE1cXhs1OntLk%3D&md5=09e68a33c4ee1b7abdde7216d7591adfCAS | 639776PubMed |
Subramanian, M. G. (1992). Lactation and prolactin release in foster dams suckling prenatally ethanol exposed pups. Alcohol. Clin. Exp. Res. 16, 891–894.
| Lactation and prolactin release in foster dams suckling prenatally ethanol exposed pups.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXnsFWksQ%3D%3D&md5=d5e70a82e79e13a930ff28c2041ecd9aCAS | 1443427PubMed |
Susser, E., Neugebauer, R., Hoek, H. W., Brown, A. S., Lin, S., Labovitz, D., and Gorman, J. M. (1996). Schizophrenia after prenatal famine. Further evidence. Arch. Gen. Psychiatry 53, 25–31.
| Schizophrenia after prenatal famine. Further evidence.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK287jtlelsQ%3D%3D&md5=bebeb5147c154d267ca08e250cb904c6CAS | 8540774PubMed |
Tewari, S., Diano, M., Bera, R., Nguyen, Q., and Parekh, H. (1992). Alterations in brain polyribosomal RNA translation and lymphocyte proliferation in prenatal ethanol-exposed rats. Alcohol. Clin. Exp. Res. 16, 436–442.
| Alterations in brain polyribosomal RNA translation and lymphocyte proliferation in prenatal ethanol-exposed rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XmtVKrsbY%3D&md5=127d2212c2e68c8d6e5c9b72168588e3CAS | 1626642PubMed |
Thompson, P. A., and Folb, P. I. (1982). An in vitro model of alcohol and acetaldehyde teratogenicity. J. Appl. Toxicol. 2, 190–195.
| An in vitro model of alcohol and acetaldehyde teratogenicity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XmtFShs70%3D&md5=1095213582ab4d3eacfaabcd19eaef07CAS | 7185900PubMed |
Tuma, D. J., and Casey, C. A. (2003). Dangerous byproducts of alcohol breakdown: focus on adducts. Alcohol Res. Health 27, 285–290.
| 15540799PubMed |
Vilaró, S., Viñas, O., Remesar, X., and Herrera, E. (1987). Effects of chronic ethanol consumption on lactational performance in rat: mammary gland and milk composition and pups’ growth and metabolism. Pharmacol. Biochem. Behav. 27, 333–339.
| Effects of chronic ethanol consumption on lactational performance in rat: mammary gland and milk composition and pups’ growth and metabolism.Crossref | GoogleScholarGoogle Scholar | 3628448PubMed |
Ward, L. C. (2009). Assessment of body composition of rats by bioimpedance spectroscopy: validation against a dual-energy X-ray absorptiometry. Scand. J. Lab. Anim. Sci. 36, 253–261.
| 1:CAS:528:DC%2BC3cXisVCit74%3D&md5=e28cc52027e5eff2325f116a3e42fc41CAS |
Weinberg, J. (1985). Effects of ethanol and maternal nutritional status on fetal development. Alcohol. Clin. Exp. Res. 9, 49–55.
| Effects of ethanol and maternal nutritional status on fetal development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXhsVClsbw%3D&md5=801d85df60c560f9a07061921f9d90e1CAS | 3887968PubMed |
Witek-Janusek, L. (1986). Maternal ethanol ingestion: effect on maternal and neonatal glucose balance. Am. J. Physiol. 251, E178–E184.
| 1:CAS:528:DyaL28Xlt12hsbY%3D&md5=a4374e9447922b329d28e08b09779d37CAS | 3526919PubMed |
Wlodek, M. E., Mibus, A., Tan, A., Siebel, A. L., Owens, J. A., and Moritz, K. M. (2007). Normal lactational environment restores nephron endowment and prevents hypertension after placental restriction in the rat. J. Am. Soc. Nephrol. 18, 1688–1696.
| Normal lactational environment restores nephron endowment and prevents hypertension after placental restriction in the rat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXnt1Squrg%3D&md5=dbb14d89374052ec034d5b1d90e1fb2dCAS | 17442788PubMed |
Woodall, S. M., Johnston, B. M., Breier, B. H., and Gluckman, P. D. (1996). Chronic maternal undernutrition in the rat leads to delayed postnatal growth and elevated blood pressure of offspring. Pediatr. Res. 40, 438–443.
| Chronic maternal undernutrition in the rat leads to delayed postnatal growth and elevated blood pressure of offspring.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2s%2FhvVKltw%3D%3D&md5=36fdd5f4a5414ce776096687659cc78dCAS | 8865281PubMed |
Woods, L. L., Weeks, D. A., and Rasch, R. (2004). Programming of adult blood pressure by maternal protein restriction: role of nephrogenesis. Kidney Int. 65, 1339–1348.
| Programming of adult blood pressure by maternal protein restriction: role of nephrogenesis.Crossref | GoogleScholarGoogle Scholar | 15086473PubMed |
Zakhari, S. (2006). Overview: how is alcohol metabolized by the body? Alcohol Res. Health 29, 245–254.
| 17718403PubMed |
