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Strategies to reduce non-communicable diseases in the offspring: negative and positive in utero programming

Published online by Cambridge University Press:  16 August 2018

H. Rodriguez-Caro  and
S. A. Williams
H. Rodriguez-Caro
Affiliation:
Nuffield Department of Women’s & Reproductive Health, University of Oxford, Women’s Centre, Level 3, John Radcliffe Hospital, Oxford, UK
S. A. Williams*
Affiliation:
Nuffield Department of Women’s & Reproductive Health, University of Oxford, Women’s Centre, Level 3, John Radcliffe Hospital, Oxford, UK
*
*Address for correspondence: Dr Suzannah A. Williams, Nuffield Department of Women’s & Reproductive Health, University of Oxford, Women’s Centre, Level 3, John Radcliffe Hospital, Oxford OX3 9DU, UK. E-mail: [email protected]
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Abstract

Non-communicable diseases (NCDs) are a major problem as they are the leading cause of death and represent a substantial economic cost. The ‘Developmental Origins of Health and Disease Hypothesis’ proposes that adverse stimuli at different life stages can increase the predisposition to these diseases. In fact, adverse in utero programming is a major origin of these diseases due to the high malleability of embryonic development. This review provides a comprehensive analysis of the scientific literature on in utero programming and NCDs highlighting potential medical strategies to prevent these diseases based upon this programming. We fully address the concept and mechanisms involved in this programming (anatomical disruptions, epigenetic modifications and microbiota alterations). We also examine the negative role of in utero programming on the increased predisposition of NCDs in the offspring, which introduces the passive medical approach that consists of avoiding adverse stimuli including an unhealthy diet and environmental chemicals. Finally, we extensively discuss active medical approaches that target the causes of NCDs and have the potential to significantly and rapidly reduce the incidence of NCDs. These approaches can be classified as direct in utero programming modifications and personalized lifestyle pregnancy programs; they could potentially provide transgenerational NCDs protection. Active strategies against NCDs constitute a promising tool for the reduction in NCDs.

Keywords

DOHaDepigeneticsmicrobiotapreventive medicine
Type
Review
Information
Journal of Developmental Origins of Health and Disease , Volume 9 , Issue 6 , December 2018 , pp. 642 - 652
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2018 

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References

1. Barker, DJ, Osmond, C. Infant mortality, childhood nutrition, and ischaemic heart disease in England and Wales. Lancet. 1986; 1, 1077–1081.Google Scholar
2. Barker, DJ, Osmond, C, Simmonds, SJ, Wield, GA. The relation of small head circumference and thinness at birth to death from cardiovascular disease in adult life. BMJ. 1993; 306, 422–426.Google Scholar
3. Barker, DJ, Winter, PD, Osmond, C, Margetts, B, Simmonds, SJ. Weight in infancy and death from ischaemic heart disease. Lancet. 1989; 2, 577–580.Google Scholar
4. Ellison, PT. Evolutionary perspectives on the fetal origins hypothesis. Am J Hum Biol. 2005; 17, 113–118.Google Scholar
5. de Boo, HA, Harding, JE. The developmental origins of adult disease (Barker) hypothesis. Aust N Z J Obstet Gynaecol. 2006; 46, 4–14.Google Scholar
6. Roura, LC, Arulkumaran, SS. Facing the noncommunicable disease (NCD) global epidemic—the battle of prevention starts in utero – the FIGO challenge. Best Pract Res Clin Obstet Gynaecol. 2015; 29, 5–14.Google Scholar
7. Ng, SP, Conklin, DJ, Bhatnagar, A, et al. Prenatal exposure to cigarette smoke induces diet- and sex-dependent dyslipidemia and weight gain in adult murine offspring. Environ Health Perspect. 2009; 117, 1042–1048.Google Scholar
8. Sandovici, I, Hoelle, K, Angiolini, E, Constancia, M. Placental adaptations to the maternal-fetal environment: implications for fetal growth and developmental programming. Reprod Biomed Online. 2012; 25, 68–89.Google Scholar
9. Palinski, W, Napoli, C. The fetal origins of atherosclerosis: maternal hypercholesterolemia, and cholesterol-lowering or antioxidant treatment during pregnancy influence in utero programming and postnatal susceptibility to atherogenesis. FASEB J. 2002; 16, 1348–1360.Google Scholar
10. Napoli, C, Infante, T, Casamassimi, A. Maternal-foetal epigenetic interactions in the beginning of cardiovascular damage. Cardiovasc Res. 2011; 92, 367–374.Google Scholar
11. Davis, EF, Lazdam, M, Lewandowski, AJ, et al. Cardiovascular risk factors in children and young adults born to preeclamptic pregnancies: a systematic review. Pediatrics. 2012; 129, e1552–e1561.Google Scholar
12. Christensen, S, Jaffar, Z, Cole, E, et al. Prenatal environmental tobacco smoke exposure increases allergic asthma risk with methylation changes in mice. Environ Mol Mutagen. 2017; 58, 423–433.Google Scholar
13. Bousquet, J, Jacot, W, Yssel, H, Vignola, AM, Humbert, M. Epigenetic inheritance of fetal genes in allergic asthma. Allergy. 2004; 59, 138–147.Google Scholar
14. Govindarajah, V, Leung, YK, Ying, J, et al. In utero exposure of rats to high-fat diets perturbs gene expression profiles and cancer susceptibility of prepubertal mammary glands. J Nutr Biochem. 2016; 29, 73–82.Google Scholar
15. Baik, I, Becker, PS, DeVito, WJ, et al. Stem cells and prenatal origin of breast cancer. Cancer Causes Control. 2004; 15, 517–530.Google Scholar
16. Grotmol, T, Weiderpass, E, Tretli, S. Conditions in utero and cancer risk. Eur J Epidemiol. 2006; 21, 561–570.Google Scholar
17. Mazaud-Guittot, S, Nicolas Nicolaz, C, Desdoits-Lethimonier, C, et al. Paracetamol, aspirin, and indomethacin induce endocrine disturbances in the human fetal testis capable of interfering with testicular descent. J Clin Endocrinol Metab. 2013; 98, E1757–E1767.Google Scholar
18. Holm, JB, Mazaud-Guittot, S, Danneskiold-Samsoe, NB, et al. Intrauterine exposure to paracetamol and aniline impairs female reproductive development by reducing follicle reserves and fertility. Toxicol Sci. 2016; 150, 178–189.Google Scholar
19. Palmer, JR, Hatch, EE, Rosenberg, CL, et al. Risk of breast cancer in women exposed to diethylstilbestrol in utero: prelimiinary results (United States). Cancer Causes Control. 2002; 13, 753–758.Google Scholar
20. Markham, JA, Taylor, AR, Taylor, SB, Bell, DB, Koenig, JI. Characterization of the cognitive impairments induced by prenatal exposure to stress in the rat. Front Behav Neurosci. 2010; 4, 173.Google Scholar
21. Booij, L, Benkelfat, C, Leyton, M, et al. Perinatal effects on in vivo measures of human brain serotonin synthesis in adulthood: a 27-year longitudinal study. Eur Neuropsychopharmacol. 2012; 22, 419–423.Google Scholar
22. Holloway, T, Moreno, JL, Umali, A, et al. Prenatal stress induces schizophrenia-like alterations of serotonin 2A and metabotropic glutamate 2 receptors in the adult offspring: role of maternal immune system. J Neurosci. 2013; 33, 1088–1098.Google Scholar
23. Huttunen, MO, Niskanen, P. Prenatal loss of father and psychiatric disorders. Arch Gen Psychiatry. 1978; 35, 429–431.Google Scholar
24. Myhrman, A, Rantakallio, P, Isohanni, M, Jones, P, Partanen, U. Unwantedness of a pregnancy and schizophrenia in the child. Br J Psychiatry. 1996; 169, 637–640.Google Scholar
25. van Os, J, Selten, JP. Prenatal exposure to maternal stress and subsequent schizophrenia. The May 1940 invasion of The Netherlands. Br J Psychiatry. 1998; 172, 324–326.Google Scholar
26. Khashan, AS, Abel, KM, McNamee, R, et al. Higher risk of offspring schizophrenia following antenatal maternal exposure to severe adverse life events. Arch Gen Psychiatry. 2008; 65, 146–152.Google Scholar
27. Khashan, AS, McNamee, R, Henriksen, TB, et al. Risk of affective disorders following prenatal exposure to severe life events: a Danish population-based cohort study. J Psychiatr Res. 2011; 45, 879–885.Google Scholar
28. Babenko, O, Kovalchuk, I, Metz, GA. Stress-induced perinatal and transgenerational epigenetic programming of brain development and mental health. Neurosci Biobehav Rev. 2015; 48, 70–91.Google Scholar
29. Thorn, SR, Regnault, TR, Brown, LD, et al. Intrauterine growth restriction increases fetal hepatic gluconeogenic capacity and reduces messenger ribonucleic acid translation initiation and nutrient sensing in fetal liver and skeletal muscle. Endocrinology. 2009; 150, 3021–3030.Google Scholar
30. Radford, EJ, Ito, M, Shi, H, et al. In utero effects. In utero undernourishment perturbs the adult sperm methylome and intergenerational metabolism. Science . 2014; 345, 1255903.Google Scholar
31. Barker, DJ. In utero programming of chronic disease. Clin Sci (Lond). 1998; 95, 115–128.Google Scholar
32. Hales, CN, Barker, DJ. Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. 1992. Int J Epidemiol. 2013; 42, 1215–1222.Google Scholar
33. Hughson, M, Farris, AB 3rd, Douglas-Denton, R, Hoy, WE, Bertram, JF. Glomerular number and size in autopsy kidneys: the relationship to birth weight. Kidney Int. 2003; 63, 2113–2122.Google Scholar
34. Hoy, WE, Douglas-Denton, RN, Hughson, MD, et al. A stereological study of glomerular number and volume: preliminary findings in a multiracial study of kidneys at autopsy. Kidney Int Suppl. 2003; 83, S31–S37. https://doi.org/10.1046/j.1523-1755.63.s83.8.x.Google Scholar
35. Mackenzie, HS, Brenner, BM. Fewer nephrons at birth: a missing link in the etiology of essential hypertension? Am J Kidney Dis. 1995; 26, 91–98.Google Scholar
36. Hoy, WE, Hughson, MD, Bertram, JF, Douglas-Denton, R, Amann, K. Nephron number, hypertension, renal disease, and renal failure. J Am Soc Nephrol. 2005; 16, 2557–2564.Google Scholar
37. 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.Google Scholar
38. Painter, RC, Roseboom, TJ, Bleker, OP. Prenatal exposure to the Dutch famine and disease in later life: an overview. Reprod Toxicol. 2005; 20, 345–352.Google Scholar
39. de Rooij, SR, Painter, RC, Phillips, DI, et al. Impaired insulin secretion after prenatal exposure to the Dutch famine. Diabetes Care. 2006; 29, 1897–1901.Google Scholar
40. Ramirez-Velez, R. In utero fetal programming and its impact on health in adulthood. Endocrinol Nutr. 2012; 59, 383–393.Google Scholar
41. Mei-Zahav, M, Korzets, Z, Cohen, I, et al. Ambulatory blood pressure monitoring in children with a solitary kidney—a comparison between unilateral renal agenesis and uninephrectomy. Blood Press Monit. 2001; 6, 263–267.Google Scholar
42. Brenner, BM, Milford, EL. Nephron underdosing: a programmed cause of chronic renal allograft failure. Am J Kidney Dis. 1993; 21(5 Suppl. 2), 66–72.Google Scholar
43. Maccani, MA, Knopik, VS. Cigarette smoke exposure-associated alterations to non-coding RNA. Front Genet. 2012; 3, 53.Google Scholar
44. van Vliet, J, Oates, NA, Whitelaw, E. Epigenetic mechanisms in the context of complex diseases. Cell Mol Life Sci. 2007; 64, 1531–1538.Google Scholar
45. Kaikkonen, MU, Lam, MT, Glass, CK. Non-coding RNAs as regulators of gene expression and epigenetics. Cardiovasc Res. 2011; 90, 430–440.Google Scholar
46. Schmitz, SU, Grote, P, Herrmann, BG. Mechanisms of long noncoding RNA function in development and disease. Cell Mol Life Sci. 2016; 73, 2491–2509.Google Scholar
47. Santos, F, Dean, W. Epigenetic reprogramming during early development in mammals. Reproduction. 2004; 127, 643–651.Google Scholar
48. Ollikainen, M, Smith, KR, Joo, EJ, et al. DNA methylation analysis of multiple tissues from newborn twins reveals both genetic and intrauterine components to variation in the human neonatal epigenome. Hum Mol Genet. 2010; 19, 4176–4188.Google Scholar
49. Heijmans, BT, Tobi, EW, Stein, AD, et al. Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc Natl Acad Sci USA. 2008; 105, 17046–17049.Google Scholar
50. Cui, H, Onyango, P, Brandenburg, S, et al. Loss of imprinting in colorectal cancer linked to hypomethylation of H19 and IGF2. Cancer Res. 2002; 62, 6442–6446.Google Scholar
51. Suter, MA, Anders, AM, Aagaard, KM. Maternal smoking as a model for environmental epigenetic changes affecting birthweight and fetal programming. Mol Hum Reprod. 2013; 19, 1–6.Google Scholar
52. Couturier-Maillard, A, Secher, T, Rehman, A, et al. NOD2-mediated dysbiosis predisposes mice to transmissible colitis and colorectal cancer. J Clin Invest. 2013; 123, 700–711.Google Scholar
53. Russell, SL, Gold, MJ, Willing, BP, et al. Perinatal antibiotic treatment affects murine microbiota, immune responses and allergic asthma. Gut Microbes. 2013; 4, 158–164.Google Scholar
54. Ege, MJ, Bieli, C, Frei, R, et al. Prenatal farm exposure is related to the expression of receptors of the innate immunity and to atopic sensitization in school-age children. J Allergy Clin Immunol. 2006; 117, 817–823.Google Scholar
55. Vuillermin, PJ, Macia, L, Nanan, R, et al. The maternal microbiome during pregnancy and allergic disease in the offspring. Semin Immunopathol. 2017; 39, 669–675.Google Scholar
56. Mulligan, CM, Friedman, JE. Maternal modifiers of the infant gut microbiota: metabolic consequences. J Endocrinol. 2017; 235, R1–R12.Google Scholar
57. Jenmalm, MC. The mother-offspring dyad: microbial transmission, immune interactions and allergy development. J Intern Med. 2017; 282, 484–495.Google Scholar
58. Collado, MC, Rautava, S, Aakko, J, Isolauri, E, Salminen, S. Human gut colonisation may be initiated in utero by distinct microbial communities in the placenta and amniotic fluid. Sci Rep. 2016; 6, 23129.Google Scholar
59. Chen, C, Song, X, Wei, W, et al. The microbiota continuum along the female reproductive tract and its relation to uterine-related diseases. Nat Commun. 2017; 8, 875.Google Scholar
60. Perez, PF, Dore, J, Leclerc, M, et al. Bacterial imprinting of the neonatal immune system: lessons from maternal cells? Pediatrics. 2007; 119, e724–e732.Google Scholar
61. Fridmann-Sirkis, Y, Stern, S, Elgart, M, et al. Delayed development induced by toxicity to the host can be inherited by a bacterial-dependent, transgenerational effect. Front Genet. 2014; 5, 27.Google Scholar
62. Ojha, S, Robinson, L, Symonds, ME, Budge, H. Suboptimal maternal nutrition affects offspring health in adult life. Early Hum Dev. 2013; 89, 909–913.Google Scholar
63. Yoshimura, S, Masuzaki, H, Miura, K, Gotoh, H, Ishimaru, T. Fetal blood flow redistribution in term intrauterine growth retardation (IUGR) and post-natal growth. Int J Gynaecol Obstet. 1998; 60, 3–8.Google Scholar
64. Watkins, AJ, Lucas, ES, Torrens, C, et al. Maternal low-protein diet during mouse pre-implantation development induces vascular dysfunction and altered renin-angiotensin-system homeostasis in the offspring. Br J Nutr. 2010; 103, 1762–1770.Google Scholar
65. Barry, JS, Anthony, RV. The pregnant sheep as a model for human pregnancy. Theriogenology. 2008; 69, 55–67.Google Scholar
66. Borgel, J, Guibert, S, Li, Y, et al. Targets and dynamics of promoter DNA methylation during early mouse development. Nat Genet. 2010; 42, 1093–1100.Google Scholar
67. Smallwood, SA, Tomizawa, S, Krueger, F, et al. Dynamic CpG island methylation landscape in oocytes and preimplantation embryos. Nat Genet. 2011; 43, 811–814.Google Scholar
68. Smith, ZD, Chan, MM, Mikkelsen, TS, et al. A unique regulatory phase of DNA methylation in the early mammalian embryo. Nature. 2012; 484, 339–344.Google Scholar
69. Smith, J, Cianflone, K, Biron, S, et al. Effects of maternal surgical weight loss in mothers on intergenerational transmission of obesity. J Clin Endocrinol Metab. 2009; 94, 4275–4283.Google Scholar
70. Long, NM, Rule, DC, Tuersunjiang, N, Nathanielsz, PW, Ford, SP. Maternal obesity in sheep increases fatty acid synthesis, upregulates nutrient transporters, and increases adiposity in adult male offspring after a feeding challenge. PLoS One. 2015; 10, e0122152.Google Scholar
71. Foster, SR, Blank, K, See Hoe, LE, et al. Bitter taste receptor agonists elicit G-protein-dependent negative inotropy in the murine heart. FASEB J. 2014; 28, 4497–4508.Google Scholar
72. Raipuria, M, Hardy, GO, Bahari, H, Morris, MJ. Maternal obesity regulates gene expression in the hearts of offspring. Nutr Metab Cardiovasc Dis. 2015; 25, 881–888.Google Scholar
73. Marco, A, Kisliouk, T, Tabachnik, T, Weller, A, Meiri, N. DNA CpG methylation (5-methylcytosine) and its derivative (5-hydroxymethylcytosine) alter histone posttranslational modifications at the pomc promoter, affecting the impact of perinatal diet on leanness and obesity of the offspring. Diabetes. 2016; 65, 2258–2267.Google Scholar
74. Savabieasfahani, M, Kannan, K, Astapova, O, Evans, NP, Padmanabhan, V. Developmental programming: differential effects of prenatal exposure to bisphenol-A or methoxychlor on reproductive function. Endocrinology. 2006; 147, 5956–5966.Google Scholar
75. Veiga-Lopez, A, Luense, LJ, Christenson, LK, Padmanabhan, V. Developmental programming: gestational bisphenol-A treatment alters trajectory of fetal ovarian gene expression. Endocrinology. 2013; 154, 1873–1884.Google Scholar
76. Veiga-Lopez, A, Beckett, EM, Abi Salloum, B, Ye, W, Padmanabhan, V. Developmental programming: prenatal BPA treatment disrupts timing of LH surge and ovarian follicular wave dynamics in adult sheep. Toxicol Appl Pharmacol. 2014; 279, 119–128.Google Scholar
77. Liao, C, Kannan, K. A survey of alkylphenols, bisphenols, and triclosan in personal care products from China and the United States. Arch Environ Contam Toxicol. 2014; 67, 50–59.Google Scholar
78. Ziv-Gal, A, Wang, W, Zhou, C, Flaws, JA. The effects of in utero bisphenol A exposure on reproductive capacity in several generations of mice. Toxicol Appl Pharmacol. 2015; 284, 354–362.Google Scholar
79. Ilagan, Y, Mamillapalli, R, Goetz, LG, Kayani, J, Taylor, HS. Bisphenol-A exposure in utero programs a sexually dimorphic estrogenic state of hepatic metabolic gene expression. Reprod Toxicol. 2017; 71, 84–94.Google Scholar
80. van Esterik, JC, Vitins, AP, Hodemaekers, HM, et al. Liver DNA methylation analysis in adult female C57BL/6JxFVB mice following perinatal exposure to bisphenol A. Toxicol Lett. 2015; 232, 293–300.Google Scholar
81. Ma, Y, Xia, W, Wang, DQ, et al. Hepatic DNA methylation modifications in early development of rats resulting from perinatal BPA exposure contribute to insulin resistance in adulthood. Diabetologia. 2013; 56, 2059–2067.Google Scholar
82. Li, G, Chang, H, Xia, W, et al. F0 maternal BPA exposure induced glucose intolerance of F2 generation through DNA methylation change in Gck. Toxicol Lett. 2014; 228, 192–199.Google Scholar
83. Paul, HA, Bomhof, MR, Vogel, HJ, Reimer, RA. Diet-induced changes in maternal gut microbiota and metabolomic profiles influence programming of offspring obesity risk in rats. Sci Rep. 2016; 6, 20683.Google Scholar
84. Rose, KM, Parmar, MS, Cavanaugh, JE. Dietary supplementation with resveratrol protects against striatal dopaminergic deficits produced by in utero LPS exposure. Brain Res. 2014; 1573, 37–43.Google Scholar
85. Adamu, HA, Imam, MU, Ooi, DJ, et al. In utero exposure to germinated brown rice and its oryzanol-rich extract attenuated high fat diet-induced insulin resistance in F1 generation of rats. BMC Complement Altern Med. 2017; 17, 67.Google Scholar
86. Tain, YL, Lin, YJ, Chan, JYH, Lee, CT, Hsu, CN. Maternal melatonin or agomelatine therapy prevents programmed hypertension in male offspring of mother exposed to continuous light. Biol Reprod. 2017; 97, 636–643.Google Scholar
87. Yamashita, T, Freigang, S, Eberle, C, et al. Maternal immunization programs postnatal immune responses and reduces atherosclerosis in offspring. Circ Res. 2006; 99, e51–e64.Google Scholar
88. Eberle, C, Merki, E, Yamashita, T, et al. Maternal immunization affects in utero programming of insulin resistance and type 2 diabetes. PLoS One. 2012; 7, e45361.Google Scholar
89. Maiellaro, M, Correa-Costa, M, Vitoretti, LB, et al. Exposure to low doses of formaldehyde during pregnancy suppresses the development of allergic lung inflammation in offspring. Toxicol Appl Pharmacol. 2014; 278, 266–274.Google Scholar
90. Hu, Y, Jin, P, Peng, J, et al. Different immunological responses to early-life antibiotic exposure affecting autoimmune diabetes development in NOD mice. J Autoimmun. 2016; 72, 47–56.Google Scholar
91. Li, Y, Saldanha, SN, Tollefsbol, TO. Impact of epigenetic dietary compounds on transgenerational prevention of human diseases. AAPS J. 2014; 16, 27–36.Google Scholar
92. Vahid, F, Zand, H, Nosrat-Mirshekarlou, E, Najafi, R, Hekmatdoost, A. The role dietary of bioactive compounds on the regulation of histone acetylases and deacetylases: a review. Gene. 2015; 562, 8–15.Google Scholar
93. Pennington, KL, DeAngelis, MM. Epigenetic mechanisms of the aging human retina. J Exp Neurosci. 2015; 9(Suppl. 2), 51–79.Google Scholar
94. Jensen, CD, Block, G, Buffler, P, et al. Maternal dietary risk factors in childhood acute lymphoblastic leukemia (United States). Cancer Causes Control. 2004; 15, 559–570.Google Scholar
95. Musselman, JR, Jurek, AM, Johnson, KJ, et al. Maternal dietary patterns during early pregnancy and the odds of childhood germ cell tumors: a Children’s Oncology Group study. Am J Epidemiol. 2011; 173, 282–291.Google Scholar
96. Pogoda, JM, Preston-Martin, S, Howe, G, et al. An international case-control study of maternal diet during pregnancy and childhood brain tumor risk: a histology-specific analysis by food group. Ann Epidemiol. 2009; 19, 148–160.Google Scholar
97. Lombardi, C, Ganguly, A, Bunin, GR, et al. Maternal diet during pregnancy and unilateral retinoblastoma. Cancer Causes Control. 2015; 26, 387–397.Google Scholar
98. Hilakivi-Clarke, L, Clarke, R, Onojafe, I, et al. A maternal diet high in n-6 polyunsaturated fats alters mammary gland development, puberty onset, and breast cancer risk among female rat offspring. Proc Natl Acad Sci U S A. 1997; 94, 9372–9377.Google Scholar
99. de Assis, S, Khan, G, Hilakivi-Clarke, L. High birth weight increases mammary tumorigenesis in rats. Int J Cancer. 2006; 119, 1537–1546.Google Scholar
100. Stark, AH, Kossoy, G, Zusman, I, Yarden, G, Madar, Z. Olive oil consumption during pregnancy and lactation in rats influences mammary cancer development in female offspring. Nutr Cancer. 2003; 46, 59–65.Google Scholar
101. Olivo, SE, Hilakivi-Clarke, L. Opposing effects of prepubertal low- and high-fat n-3 polyunsaturated fatty acid diets on rat mammary tumorigenesis. Carcinogenesis. 2005; 26, 1563–1572.Google Scholar
102. Ion, G, Akinsete, JA, Hardman, WE. Maternal consumption of canola oil suppressed mammary gland tumorigenesis in C3(1) TAg mice offspring. BMC Cancer. 2010; 10, 81.Google Scholar
103. de Oliveira Andrade, F, Fontelles, CC, Rosim, MP, et al. Exposure to lard-based high-fat diet during fetal and lactation periods modifies breast cancer susceptibility in adulthood in rats. J Nutr Biochem. 2014; 25, 613–622.Google Scholar
104. Segovia, SA, Vickers, MH, Gray, C, Zhang, XD, Reynolds, CM. Conjugated linoleic acid supplementation improves maternal high fat diet-induced programming of metabolic dysfunction in adult male rat offspring. Sci Rep. 2017; 7, 6663.Google Scholar
105. Arany, E, Strutt, B, Romanus, P, et al. Taurine supplement in early life altered islet morphology, decreased insulitis and delayed the onset of diabetes in non-obese diabetic mice. Diabetologia. 2004; 47, 1831–1837.Google Scholar
106. Mortensen, OH, Olsen, HL, Frandsen, L, et al. A maternal low protein diet has pronounced effects on mitochondrial gene expression in offspring liver and skeletal muscle; protective effect of taurine. J Biomed Sci. 2010; 17(Suppl. 1), S38.Google Scholar
107. Lee, YY, Lee, HJ, Lee, SS, et al. Taurine supplementation restored the changes in pancreatic islet mitochondria in the fetal protein-malnourished rat. Br J Nutr. 2011; 106, 1198–1206.Google Scholar
108. Tang, C, Marchand, K, Lam, L, et al. Maternal taurine supplementation in rats partially prevents the adverse effects of early-life protein deprivation on beta-cell function and insulin sensitivity. Reproduction. 2013; 145, 609–620.Google Scholar
109. Hultman, K, Alexanderson, C, Manneras, L, et al. Maternal taurine supplementation in the late pregnant rat stimulates postnatal growth and induces obesity and insulin resistance in adult offspring. J Physiol. 2007; 579, 823–833.Google Scholar
110. Deliyanti, D, Armani, R, Casely, D, et al. Retinal vasculopathy is reduced by dietary salt restriction: involvement of Glia, ENaCalpha, and the renin-angiotensin-aldosterone system. Arterioscler Thromb Vasc Biol. 2014; 34, 2033–2041.Google Scholar
111. Lyons, A, O’Mahony, D, O’Brien, F, et al. Bacterial strain-specific induction of Foxp3+ T regulatory cells is protective in murine allergy models. Clin Exp Allergy. 2010; 40, 811–819.Google Scholar
112. Hogenkamp, A, Knippels, LM, Garssen, J, van Esch, BC. Supplementation of mice with specific nondigestible oligosaccharides during pregnancy or lactation leads to diminished sensitization and allergy in the female offspring. J Nutr. 2015; 145, 996–1002.Google Scholar
113. Hogenkamp, A, Thijssen, S, van Vlies, N, Garssen, J. Supplementing pregnant mice with a specific mixture of nondigestible oligosaccharides reduces symptoms of allergic asthma in male offspring. J Nutr. 2015; 145, 640–646.Google Scholar
114. Verheijden, KA, Willemsen, LE, Braber, S, et al. Dietary galacto-oligosaccharides prevent airway eosinophilia and hyperresponsiveness in a murine house dust mite-induced asthma model. Respir Res. 2015; 16, 17.Google Scholar
115. Bouchaud, G, Castan, L, Chesne, J, et al. Maternal exposure to GOS/inulin mixture prevents food allergies and promotes tolerance in offspring in mice. Allergy. 2016; 71, 68–76.Google Scholar
116. Vaidya, A, Saville, N, Shrestha, BP, et al. Effects of antenatal multiple micronutrient supplementation on children’s weight and size at 2 years of age in Nepal: follow-up of a double-blind randomised controlled trial. Lancet. 2008; 371, 492–499.Google Scholar
117. Pena-Rosas, JP, De-Regil, LM, Dowswell, T, Viteri, FE. Daily oral iron supplementation during pregnancy. Cochrane Database Syst Rev. 2012; 12, CD004736.Google Scholar
118. Pena-Rosas, JP, De-Regil, LM, Dowswell, T, Viteri, FE. Intermittent oral iron supplementation during pregnancy. Cochrane Database Syst Rev. 2012, CD009997. https://doi.org/10.1002/14651858.CD009997.Google Scholar
119. Imdad, A, Bhutta, ZA. Maternal nutrition and birth outcomes: effect of balanced protein-energy supplementation. Paediatr Perinat Epidemiol. 2012; 26(Suppl. 1), 178–190.Google Scholar
120. Stewart, CP, Christian, P, Schulze, KJ, et al. Antenatal micronutrient supplementation reduces metabolic syndrome in 6- to 8-year-old children in rural Nepal. J Nutr. 2009; 139, 1575–1581.Google Scholar
121. Marcelino, TB, Longoni, A, Kudo, KY, et al. Evidences that maternal swimming exercise improves antioxidant defenses and induces mitochondrial biogenesis in the brain of young Wistar rats. Neuroscience. 2013; 246, 28–39.Google Scholar
122. Solvsten, CAE, de Paoli, F, Christensen, JH, Nielsen, AL. Voluntary physical exercise induces expression and epigenetic remodeling of vegfa in the rat hippocampus. Mol Neurobiol. 2018; 55, 567–582.Google Scholar