Hostname: page-component-8448b6f56d-c47g7 Total loading time: 0 Render date: 2024-04-16T11:29:32.862Z Has data issue: false hasContentIssue false
  • English
  • Français

Early life programming and the risk of non-alcoholic fatty liver disease

Published online by Cambridge University Press:  23 January 2017

C. Lynch ,
C. S. Chan  and
A. J. Drake
C. Lynch
Affiliation:
Edinburgh Medical School, College of Medicine and Veterinary Medicine, University of Edinburgh, Edinburgh, UK
C. S. Chan
Affiliation:
Edinburgh Medical School, College of Medicine and Veterinary Medicine, University of Edinburgh, Edinburgh, UK
A. J. Drake*
Affiliation:
University/BHF Centre for Cardiovascular Science, University of Edinburgh, Queen’s Medical Research Institute, Edinburgh, UK
*
*Address for correspondence: A. J. Drake, University/BHF Centre for Cardiovascular Science, University of Edinburgh, Queen’s Medical Research Institute, 47, Little France Crescent, Edinburgh EH16 4TJ, UK. (Email mandy.drake@ed.ac.uk)
Get access Rights & Permissions [Opens in a new window]

Abstract

Non-alcoholic fatty liver disease (NAFLD) is associated with obesity, insulin resistance, type 2 diabetes and cardiovascular disease and can be considered the hepatic manifestation of the metabolic syndrome. NAFLD represents a spectrum of disease, from the relatively benign simple steatosis to the more serious non-alcoholic steatohepatitis, which can progress to liver cirrhosis, hepatocellular carcinoma and end-stage liver failure, necessitating liver transplantation. Although the increasing prevalence of NAFLD in developed countries has substantial implications for public health, many of the precise mechanisms accounting for the development and progression of NAFLD are unclear. The environment in early life is an important determinant of cardiovascular disease risk in later life and studies suggest this also extends to NAFLD. Here we review data from animal models and human studies which suggest that fetal and early life exposure to maternal under- and overnutrition, excess glucocorticoids and environmental pollutants may confer an increased susceptibility to NAFLD development and progression in offspring and that such effects may be sex-specific. We also consider studies aimed at identifying potential dietary and pharmacological interventions aimed at reducing this risk. We suggest that further human epidemiological studies are needed to ensure that data from animal models are relevant to human health.

Keywords

early life programmingglucocorticoidsmaternal nutritionnon-alcoholic fatty liver disease
Type
Review
Information
Journal of Developmental Origins of Health and Disease , Volume 8 , Issue 3 , June 2017 , pp. 263 - 272
Check for updates
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

†

These authors contributed equally to this work.

References

1. Brown, GT, Kleiner, DE. Histopathology of nonalcoholic fatty liver disease and nonalcoholic steatohepatitis. Metabolism. 2016; 65, 1080–1086.Google Scholar
2. Leite, NC, Salles, GF, Araujo, AL, Villela-Nogueira, CA, Cardoso, CR. Prevalence and associated factors of non-alcoholic fatty liver disease in patients with type-2 diabetes mellitus. Liver Int. 2009; 29, 113–119.CrossRefGoogle ScholarPubMed
3. Molleston, JP, Schwimmer, JB, Yates, KP, et al. Histological abnormalities in children with nonalcoholic fatty liver disease and normal or mildly elevated alanine aminotransferase levels. J Pediatr. 2014; 164, 707–713.e3.CrossRefGoogle ScholarPubMed
4. AlKhater, SA. Paediatric non-alcoholic fatty liver disease: an overview. Obes Rev. 2015; 16, 393–405.CrossRefGoogle ScholarPubMed
5. Dyson, JK, Anstee, QM, McPherson, S. Non-alcoholic fatty liver disease: a practical approach to treatment. Frontline Gastroenterol. 2014; 5, 277–286.Google Scholar
6. Zezos, P, Renner, EL. Liver transplantation and non-alcoholic fatty liver disease. World J Gastroenterol. 2014; 20, 15532–15538.Google Scholar
7. Charlton, MR, Burns, JM, Pedersen, RA, et al. Frequency and outcomes of liver transplantation for nonalcoholic steatohepatitis in the United States. Gastroenterology. 2011; 141, 1249–1253.CrossRefGoogle ScholarPubMed
8. Bhatia, LS, Curzen, NP, Byrne, CD. Nonalcoholic fatty liver disease and vascular risk. Curr Opin Cardiol. 2012; 27, 420–428.Google Scholar
9. Noureddin, M, Mato, JM, Lu, SC. Nonalcoholic fatty liver disease: update on pathogenesis, diagnosis, treatment and the role of S-adenosylmethionine. Exp Biol Med (Maywood). 2015; 240, 809–820.Google Scholar
10. Oliveira, CP, de Lima Sanches, P, de Abreu-Silva, EO, Marcadenti, A. Nutrition and physical activity in nonalcoholic fatty liver disease. J Diabetes Res. 2016; 2016, 4597246.CrossRefGoogle ScholarPubMed
11. Gaggini, M, Morelli, M, Buzzigoli, E, et al. Non-alcoholic fatty liver disease (NAFLD) and its connection with insulin resistance, dyslipidemia, atherosclerosis and coronary heart disease. Nutrients. 2013; 5, 1544–1560.Google Scholar
12. Dowman, JK, Tomlinson, JW, Newsome, PN. Pathogenesis of non-alcoholic fatty liver disease. QJM. 2010; 103, 71–83.CrossRefGoogle ScholarPubMed
13. Guerrero, R, Vega, GL, Grundy, SM, Browning, JD. Ethnic differences in hepatic steatosis: an insulin resistance paradox? Hepatology. 2009; 49, 791–801.CrossRefGoogle ScholarPubMed
14. Weston, SR, Leyden, W, Murphy, R, et al. Racial and ethnic distribution of nonalcoholic fatty liver in persons with newly diagnosed chronic liver disease. Hepatology. 2005; 41, 372–379.Google Scholar
15. Romeo, S, Kozlitina, J, Xing, C, et al. Genetic variation in PNPLA3 confers susceptibility to nonalcoholic fatty liver disease. Nat Genet. 2008; 40, 1461–1465.CrossRefGoogle ScholarPubMed
16. Roseboom, TJ, van der Meulen, JH, Osmond, C, et al. Coronary heart disease after prenatal exposure to the Dutch famine, 1944–45. Heart. 2000; 84, 595–598.CrossRefGoogle Scholar
17. Ravelli, AC, van Der Meulen, JH, Osmond, C, Barker, DJ, Bleker, OP. Obesity at the age of 50 y in men and women exposed to famine prenatally. Am J Clin Nutr. 1999; 70, 811–816.Google Scholar
18. Wang, Y, Wang, X, Kong, Y, Zhang, JH, Zeng, Q. The Great Chinese Famine leads to shorter and overweight females in Chongqing Chinese population after 50 years. Obesity (Silver Spring). 2010; 18, 588–592.Google Scholar
19. Barker, DJ, Osmond, C, Golding, J, Kuh, D, Wadsworth, ME. Growth in utero, blood pressure in childhood and adult life, and mortality from cardiovascular disease. Br Med J. 1989; 298, 564–567.CrossRefGoogle ScholarPubMed
20. Fraser, A, Ebrahim, S, Davey Smith, G, Lawlor, DA. The associations between birthweight and adult markers of liver damage and function. Paediatr Perinat Epidemiol. 2008; 22, 12–21.CrossRefGoogle ScholarPubMed
21. Nobili, V, Marcellini, M, Marchesini, G, et al. Intrauterine growth retardation, insulin resistance, and nonalcoholic fatty liver disease in children. Diabetes Care. 2007; 30, 2638–2640.Google Scholar
22. Breij, LM, Kerkhof, GF, Hokken-Koelega, AC. Accelerated infant weight gain and risk for nonalcoholic fatty liver disease in early adulthood. J Clin Endocrinol Metab. 2014; 99, 1189–1195.Google Scholar
23. Wang, N, Chen, Y, Ning, Z, et al. Exposure to famine in early life and nonalcoholic fatty liver disease in adulthood. J Clin Endocrinol Metab. 2016; 101, 2218–2225.CrossRefGoogle ScholarPubMed
24. Sandboge, S, Perala, MM, Salonen, MK, et al. Early growth and non-alcoholic fatty liver disease in adulthood-the NAFLD liver fat score and equation applied on the Helsinki Birth Cohort Study. Ann Med. 2013; 45, 430–437.Google Scholar
25. Erhuma, A, Salter, AM, Sculley, DV, Langley-Evans, SC, Bennett, AJ. Prenatal exposure to a low-protein diet programs disordered regulation of lipid metabolism in the aging rat. Am J Physiol Endocrinol Metab. 2007; 292, E1702–E1714.Google Scholar
26. Carr, SK, Chen, J-H, Cooper, WN, et al. Maternal diet amplifies the hepatic aging trajectory of Cidea in male mice and leads to the development of fatty liver. FASEB J. 2014; 28, 2191–2201.CrossRefGoogle Scholar
27. Wolfe, D, Gong, M, Han, G, et al. Nutrient sensor-mediated programmed nonalcoholic fatty liver disease in low birthweight offspring. Am J Obstet Gynecol. 2012; 207, 308 e1–e6.Google Scholar
28. Hyatt, MA, Gardner, DS, Sebert, S, et al. Suboptimal maternal nutrition, during early fetal liver development, promotes lipid accumulation in the liver of obese offspring. Reproduction. 2011; 141, 119–126.Google Scholar
29. Souza-Mello, V, Mandarim-de-Lacerda, CA, Aguila, MB. Hepatic structural alteration in adult programmed offspring (severe maternal protein restriction) is aggravated by post-weaning high-fat diet. Br J Nutr. 2007; 98, 1159–1169.CrossRefGoogle ScholarPubMed
30. Nascimento, FA, Ceciliano, TC, Aguila, MB, Mandarim-de-Lacerda, CA. Transgenerational effects on the liver and pancreas resulting from maternal vitamin D restriction in mice. J Nutr Sci Vitaminol (Tokyo). 2013; 59, 367–374.Google Scholar
31. Reynolds, RM, Allan, KM, Raja, EA, et al. Maternal obesity during pregnancy and premature mortality from cardiovascular event in adult offspring: follow-up of 1 323 275 person years. BMJ. 2013; 347, f4539.Google Scholar
32. Modi, N, Murgasova, D, Ruager-Martin, R, et al. The influence of maternal body mass index on infant adiposity and hepatic lipid content. Pediatr Res. 2011; 70, 287–291.Google Scholar
33. Brumbaugh, DE, Tearse, P, Cree-Green, M, et al. Intrahepatic fat is increased in the neonatal offspring of obese women with gestational diabetes. J Pediatr. 2013; 162, 930–936.e1.Google Scholar
34. Bayol, SA, Simbi, BH, Fowkes, RC, Stickland, NC. A maternal ‘junk food’ diet in pregnancy and lactation promotes nonalcoholic fatty liver disease in rat offspring. Endocrinology. 2010; 151, 1451–1461.Google Scholar
35. Oben, JA, Mouralidarane, A, Samuelsson, A-M, et al. Maternal obesity during pregnancy and lactation programs the development of offspring non-alcoholic fatty liver disease in mice. J Hepatol. 2010; 52, 913–920.CrossRefGoogle ScholarPubMed
36. Bringhenti, I, Ornellas, F, Martins, MA, Mandarim-de-Lacerda, CA, Aguila, MB. Early hepatic insult in the offspring of obese maternal mice. Nutr Res. 2015; 35, 136–145.Google Scholar
37. Drake, AJ, Reynolds, RM. Impact of maternal obesity on offspring obesity and cardiometabolic disease risk. Reproduction. 2010; 140, 387–398.CrossRefGoogle ScholarPubMed
38. Hellgren, LI, Jensen, RI, Waterstradt, MS, Quistorff, B, Lauritzen, L. Acute and perinatal programming effects of a fat-rich diet on rat muscle mitochondrial function and hepatic lipid accumulation. Acta Obstet Gynecol Scand. 2014; 93, 1170–1180.Google Scholar
39. King, V, Dakin, RS, Liu, L, et al. Maternal obesity has little effect on the immediate offspring but impacts on the next generation. Endocrinology. 2013; 154, 2514–2524.CrossRefGoogle ScholarPubMed
40. King, V, Norman, J, Seckl, J, Drake, A. Post-weaning diet determines metabolic risk in mice exposed to overnutrition in early life. Reprod Biol Endocrinol. 2014; 12, 73.Google Scholar
41. Kjaergaard, M, Nilsson, C, Rosendal, A, Nielsen, MO, Raun, K. Maternal chocolate and sucrose soft drink intake induces hepatic steatosis in rat offspring associated with altered lipid gene expression profile. Acta Physiol (Oxf). 2014; 210, 142–153.Google Scholar
42. Zhang, ZY, Dai, YB, Wang, HN, Wang, MW. Supplementation of the maternal diet during pregnancy with chocolate and fructose interacts with the high-fat diet of the young to facilitate the onset of metabolic disorders in rat offspring. Clin Exp Pharmacol Physiol. 2013; 40, 652–661.Google Scholar
43. Llopis, M, Sanchez, J, Priego, T, Palou, A, Pico, C. Maternal fat supplementation during late pregnancy and lactation influences the development of hepatic steatosis in offspring depending on the fat source. J Agric Food Chem. 2014; 62, 1590–1601.Google Scholar
44. El-Sayyad, HI, Al-Haggar, MM, El-Ghawet, HA, Bakr, IH. Effect of maternal diabetes and hypercholesterolemia on fetal liver of albino Wistar rats. Nutrition. 2014; 30, 326–336.Google Scholar
45. Song, Y, Li, J, Zhao, Y, et al. Severe maternal hyperglycemia exacerbates the development of insulin resistance and fatty liver in the offspring on high fat diet. Exp Diabetes Res. 2012; 2012, 254976.Google Scholar
46. Alfaradhi, MZ, Fernandez-Twinn, DS, Martin-Gronert, MS, et al. Oxidative stress and altered lipid homeostasis in the programming of offspring fatty liver by maternal obesity. Am J Physiol Regul Integr Comp Physiol. 2014; 307, R26–R34.CrossRefGoogle ScholarPubMed
47. Bouanane, S, Merzouk, H, Benkalfat, NB, et al. Hepatic and very low-density lipoprotein fatty acids in obese offspring of overfed dams. Metabolism. 2010; 59, 1701–1709.CrossRefGoogle ScholarPubMed
48. Zhou, D, Wang, H, Cui, H, Chen, H, Pan, YX. Early-life exposure to high-fat diet may predispose rats to gender-specific hepatic fat accumulation by programming Pepck expression. J Nutr Biochem. 2015; 26, 433–440.CrossRefGoogle ScholarPubMed
49. Bruce, KD, Cagampang, FR, Argenton, M, et al. Maternal high-fat feeding primes steatohepatitis in adult mice offspring, involving mitochondrial dysfunction and altered lipogenesis gene expression. Hepatology. 2009; 50, 1796–1808.CrossRefGoogle ScholarPubMed
50. Matsuzawa-Nagata, N, Takamura, T, Ando, H, et al. Increased oxidative stress precedes the onset of high-fat diet-induced insulin resistance and obesity. Metabolism. 2008; 57, 1071–1077.Google Scholar
51. McCurdy, CE, Bishop, JM, Williams, SM, et al. Maternal high-fat diet triggers lipotoxicity in the fetal livers of nonhuman primates. J Clin Invest. 2009; 119, 323–335.Google Scholar
52. Reitman, ML. Leptin in the liver: a toxic or beneficial mix? Cell Metab. 2012; 16, 1–2.CrossRefGoogle ScholarPubMed
53. Thorn, SR, Baquero, KC, Newsom, SA, et al. Early life exposure to maternal insulin resistance has persistent effects on hepatic NAFLD in juvenile nonhuman primates. Diabetes. 2014; 63, 2702–2713.Google Scholar
54. Pruis, MG, Lendvai, A, Bloks, VW, et al. Maternal western diet primes non-alcoholic fatty liver disease in adult mouse offspring. Acta Physiol (Oxf). 2014; 210, 215–227.Google Scholar
55. Aagaard-Tillery, KM, Grove, K, Bishop, J, et al. Developmental origins of disease and determinants of chromatin structure: maternal diet modifies the primate fetal epigenome. J Mol Endocrinol. 2008; 41, 91–102.Google Scholar
56. Xue, Y, Shen, SQ, Corbo, JC, Kefalov, VJ. Circadian and light-driven regulation of rod dark adaptation. Sci Rep. 2015; 5, 17616.Google Scholar
57. Mouralidarane, A, Soeda, J, Visconti-Pugmire, C, et al. Maternal obesity programs offspring nonalcoholic fatty liver disease by innate immune dysfunction in mice. Hepatology. 2013; 58, 128–138.Google Scholar
58. Gregorio, BM, Souza-Mello, V, Carvalho, JJ, Mandarim-de-Lacerda, CA, Aguila, MB. Maternal high-fat intake predisposes nonalcoholic fatty liver disease in C57BL/6 offspring. Am J Obstet Gynecol. 2010; 203, 495.e1–e8.Google Scholar
59. Kruse, M, Seki, Y, Vuguin, PM, et al. High-fat intake during pregnancy and lactation exacerbates high-fat diet-induced complications in male offspring in mice. Endocrinology. 2013; 154, 3565–3576.CrossRefGoogle ScholarPubMed
60. Li, J, Olsen, J, Vestergaard, M, et al. Prenatal stress exposure related to maternal bereavement and risk of childhood overweight. PLoS One. 2010; 5, e11896.Google Scholar
61. Virk, J, Li, J, Vestergaard, M, et al. Early life disease programming during the preconception and prenatal period: making the link between stressful life events and type-1 diabetes. PLoS One. 2010; 5, e11523.Google Scholar
62. Wang, L, Anderson, JL, Dalton Iii, WT, et al. Maternal depressive symptoms and the risk of overweight in their children. Matern Child Health J. 2013; 17, 940–948.Google Scholar
63. Dalziel, SR, Walker, NK, Parag, V, et al. Cardiovascular risk factors after antenatal exposure to betamethasone: 30-year follow-up of a randomised controlled trial. Lancet. 2005; 365, 1856–1862.Google Scholar
64. Khulan, B, Drake, AJ. Glucocorticoids as mediators of developmental programming effects. Best Pract Res Clin Endocrinol Metab. 2012; 26, 689–700.Google Scholar
65. Cleasby, M, Kelly, PA, Walker, BR, Seckl, JR. Programming of rat muscle and fat metabolism by in utero over-exposure to glucocorticoids. Endocrinology. 2003; 144, 999–1007.Google Scholar
66. Drake, AJ, Raubenheimer, PJ, Kerrigan, D, et al. Prenatal dexamethasone programs expression of genes in liver and adipose tissue and increased hepatic lipid accumulation but not obesity on a high-fat diet. Endocrinology. 2010; 151, 1581–1587.Google Scholar
67. Huang, YH, Chen, CJ, Tang, KS, et al. Postnatal high-fat Diet increases liver steatosis and apoptosis threatened by prenatal dexamethasone through the oxidative effect. Int J Mol Sci. 2016; 17, 369.Google Scholar
68. Alkhouri, N, Carter-Kent, C, Feldstein, AE. Apoptosis in nonalcoholic fatty liver disease: diagnostic and therapeutic implications. Expert Rev Gastroenterol Hepatol. 2011; 5, 201–212.Google Scholar
69. Carbone, DL, Zuloaga, DG, Hiroi, R, et al. Prenatal dexamethasone exposure potentiates diet-induced hepatosteatosis and decreases plasma IGF-I in a sex-specific fashion. Endocrinology. 2012; 153, 295–306.Google Scholar
70. Maeyama, H, Hirasawa, T, Tahara, Y, et al. Maternal restraint stress during pregnancy in mice induces 11beta-HSD1-associated metabolic changes in the livers of the offspring. J Dev Orig Health Dis. 2015; 6, 105–114.Google Scholar
71. Calafat, AM, Kuklenyik, Z, Reidy, JA, et al. Urinary concentrations of bisphenol A and 4-nonylphenol in a human reference population. Environ Health Perspect. 2005; 113, 391–395.Google Scholar
72. Somm, E, Schwitzgebel, VM, Toulotte, A, et al. Perinatal exposure to bisphenol a alters early adipogenesis in the rat. Environ Health Perspect. 2009; 117, 1549–1555.Google Scholar
73. Alonso-Magdalena, P, Vieira, E, Soriano, S, et al. Bisphenol A exposure during pregnancy disrupts glucose homeostasis in mothers and adult male offspring. Environ Health Perspect. 2010; 118, 1243–1250.Google Scholar
74. Wei, J, Sun, X, Chen, Y, et al. Perinatal exposure to bisphenol A exacerbates nonalcoholic steatohepatitis-like phenotype in male rat offspring fed on a high-fat diet. J Endocrinol. 2014; 222, 313–325.Google Scholar
75. Jiang, Y, Xia, W, Zhu, Y, et al. Mitochondrial dysfunction in early life resulted from perinatal bisphenol A exposure contributes to hepatic steatosis in rat offspring. Toxicol Lett. 2014; 228, 85–92.Google Scholar
76. Strakovsky, RS, Wang, H, Engeseth, NJ, et al. Developmental bisphenol A (BPA) exposure leads to sex-specific modification of hepatic gene expression and epigenome at birth that may exacerbate high-fat diet-induced hepatic steatosis. Toxicol Appl Pharmacol. 2015; 284, 101–112.Google Scholar
77. Elsby, R, Maggs, JL, Ashby, J, Park, BK. Comparison of the modulatory effects of human and rat liver microsomal metabolism on the estrogenicity of bisphenol A: implications for extrapolation to humans. J Pharmacol Exp Ther. 2001; 297, 103–113.Google Scholar
78. Silva, MJ, Barr, DB, Reidy, JA, et al. Urinary levels of seven phthalate metabolites in the U.S. population from the National Health and Nutrition Examination Survey (NHANES) 1999–2000. Environ Health Perspect. 2004; 112, 331–338.Google Scholar
79. Peraza, MA, Burdick, AD, Marin, HE, Gonzalez, FJ, Peters, JM. The toxicology of ligands for peroxisome proliferator-activated receptors (PPAR). Toxicol Sci. 2006; 90, 269–295.Google Scholar
80. Pereira, C, Rao, CV. Toxicity study of maternal transfer of polychlorinated biphenyls and diethyl phthalate to 21-day-old male and female weanling pups of Wistar rats. Ecotoxicol Environ Saf. 2007; 68, 118–125.Google Scholar
81. Marsee, K, Woodruff, TJ, Axelrad, DA, Calafat, AM, Swan, SH. Estimated daily phthalate exposures in a population of mothers of male infants exhibiting reduced anogenital distance. Environ Health Perspect. 2006; 114, 805–809.Google Scholar
82. Maranghi, F, Lorenzetti, S, Tassinari, R, et al. In utero exposure to di-(2-ethylhexyl) phthalate affects liver morphology and metabolism in post-natal CD-1 mice. Reprod Toxicol. 2010; 29, 427–432.Google Scholar
83. Gilliland, FD, Berhane, K, McConnell, R, et al. Maternal smoking during pregnancy, environmental tobacco smoke exposure and childhood lung function. Thorax. 2000; 55, 271–276.Google Scholar
84. Huang, RC, Burke, V, Newnham, JP, et al. Perinatal and childhood origins of cardiovascular disease. Int J Obes (Lond). 2007; 31, 236–244.Google Scholar
85. Cupul-Uicab, LA, Skjaerven, R, Haug, K, et al. Exposure to tobacco smoke in utero and subsequent plasma lipids, ApoB, and CRP among adult women in the MoBa cohort. Environ Health Perspect. 2012; 120, 1532–1537.Google Scholar
86. Power, C, Atherton, K, Thomas, C. Maternal smoking in pregnancy, adult adiposity and other risk factors for cardiovascular disease. Atherosclerosis. 2010; 211, 643–648.Google Scholar
87. Ortiz, L, Nakamura, B, Li, X, Blumberg, B, Luderer, U. In utero exposure to benzo[a]pyrene increases adiposity and causes hepatic steatosis in female mice, and glutathione deficiency is protective. Toxicol Lett. 2013; 223, 260–267.Google Scholar
88. Regnault, C, Worms, IA, Oger-Desfeux, C, et al. Impaired liver function in Xenopus tropicalis exposed to benzo[a]pyrene: transcriptomic and metabolic evidence. BMC Genomics. 2014; 15, 666.Google Scholar
89. Wickstrom, R. Effects of nicotine during pregnancy: human and experimental evidence. Curr Neuropharmacol. 2007; 5, 213–222.Google Scholar
90. Holloway, AC, Cuu, DQ, Morrison, KM, Gerstein, HC, Tarnopolsky, MA. Transgenerational effects of fetal and neonatal exposure to nicotine. Endocrine. 2007; 31, 254–259.Google Scholar
91. Ma, N, Nicholson, CJ, Wong, M, Holloway, AC, Hardy, DB. Fetal and neonatal exposure to nicotine leads to augmented hepatic and circulating triglycerides in adult male offspring due to increased expression of fatty acid synthase. Toxicol Appl Pharmacol. 2014; 275, 1–11.Google Scholar
92. Ornoy, A, Ergaz, Z. Alcohol abuse in pregnant women: effects on the fetus and newborn, mode of action and maternal treatment. Int J Environ Res Public Health. 2010; 7, 364–379.Google Scholar
93. Xia, LP, Shen, L, Kou, H, et al. Prenatal ethanol exposure enhances the susceptibility to metabolic syndrome in offspring rats by HPA axis-associated neuroendocrine metabolic programming. Toxicol Lett. 2014; 226, 98–105.CrossRefGoogle ScholarPubMed
94. Shen, L, Liu, Z, Gong, J, et al. Prenatal ethanol exposure programs an increased susceptibility of non-alcoholic fatty liver disease in female adult offspring rats. Toxicol Appl Pharmacol. 2014; 274, 263–273.Google Scholar
95. Godfrey, KM, Gluckman, PD, Hanson, MA. Developmental origins of metabolic disease: life course and intergenerational perspectives. Trends Endocrinol Metab. 2010; 21, 199–205.Google Scholar
96. Gentile, CL, Nivala, AM, Gonzales, JC, et al. Experimental evidence for therapeutic potential of taurine in the treatment of nonalcoholic fatty liver disease. Am J Physiol Regul Integr Comp Physiol. 2011; 301, R1710–R1722.Google Scholar
97. Li, M, Reynolds, CM, Sloboda, DM, Gray, C, Vickers, MH. Maternal taurine supplementation attenuates maternal fructose-induced metabolic and inflammatory dysregulation and partially reverses adverse metabolic programming in offspring. J Nutr Biochem. 2015; 26, 267–276.CrossRefGoogle ScholarPubMed
98. Li, M. Effects of taurine supplementation on hepatic markers of inflammation and lipid metabolism in mothers and offspring in the setting of maternal obesity. PLoS One. 2013; 8, e76961.Google Scholar
99. Alwayn, IP, Gura, K, Nose, V, et al. Omega-3 fatty acid supplementation prevents hepatic steatosis in a murine model of nonalcoholic fatty liver disease. Pediatr Res. 2005; 57, 445–452.CrossRefGoogle Scholar
100. Bringhenti, I, Schultz, A, Rachid, T, et al. An early fish oil-enriched diet reverses biochemical, liver and adipose tissue alterations in male offspring from maternal protein restriction in mice. J Nutr Biochem. 2011; 22, 1009–1014.Google Scholar
101. Torres Dde, O, Dos Santos, AC, Silva, AK, et al. Effect of maternal diet rich in omega-6 and omega-9 fatty acids on the liver of LDL receptor-deficient mouse offspring. Birth Defects Res B Dev Reprod Toxicol. 2010; 89, 164–170.Google Scholar
102. Teramoto, T, Shirai, K, Daida, H, Yamada, N. Effects of bezafibrate on lipid and glucose metabolism in dyslipidemic patients with diabetes: the J-BENEFIT study. Cardiovasc Diabetol. 2012; 11, 29.Google Scholar
103. Magliano, DC, Bargut, TC, de Carvalho, SN, et al. Peroxisome proliferator-activated receptors-alpha and gamma are targets to treat offspring from maternal diet-induced obesity in mice. PLoS One. 2013; 8, e64258.Google Scholar
104. Grube, MM, von der Lippe, E, Schlaud, M, Brettschneider, AK. Does breastfeeding help to reduce the risk of childhood overweight and obesity? A propensity score analysis of data from the KiGGS study. PLoS One. 2015; 10, e0122534.Google Scholar
105. Nobili, V, Bedogni, G, Alisi, A, et al. A protective effect of breastfeeding on the progression of non-alcoholic fatty liver disease. Arch Dis Child. 2009; 94, 801–805.Google Scholar
106. Dentin, R, Benhamed, F, Pegorier, JP, et al. Polyunsaturated fatty acids suppress glycolytic and lipogenic genes through the inhibition of ChREBP nuclear protein translocation. J Clin Invest. 2005; 115, 2843–2854.Google Scholar
107. Yamada, M, Wolfe, D, Han, G, et al. Early onset of fatty liver in growth-restricted rat fetuses and newborns. Congenit Anom (Kyoto). 2011; 51, 167–173.Google Scholar
108. Cao, L, Mao, C, Li, S, et al. Hepatic insulin signaling changes: possible mechanism in prenatal hypoxia-increased susceptibility of fatty liver in adulthood. Endocrinology. 2012; 153, 4955–4965.Google Scholar
109. Dahlhoff, M, Pfister, S, Blutke, A, et al. Peri-conceptional obesogenic exposure induces sex-specific programming of disease susceptibilities in adult mouse offspring. Biochim Biophys Acta. 2014; 1842, 304–317.Google Scholar
110. Ashino, NG, Saito, KN, Souza, FD, et al. Maternal high-fat feeding through pregnancy and lactation predisposes mouse offspring to molecular insulin resistance and fatty liver. J Nutr Biochem. 2012; 23, 341–348.Google Scholar