Hostname: page-component-7dd5485656-zlgnt Total loading time: 0 Render date: 2025-10-31T18:33:17.092Z Has data issue: false hasContentIssue false
  • English
  • Français

Strength of nonhuman primate studies of developmental programming: review of sample sizes, challenges, and steps for future work

Part of: DOHaD on International Women's Day 2020

Published online by Cambridge University Press:  30 September 2019

Hillary F. Huber Open the ORCID record for Hillary F. Huber [Opens in a new window] ,
Susan L. Jenkins ,
Cun Li  and
Peter W. Nathanielsz
Hillary F. Huber*
Affiliation:
Department of Animal Science, University of Wyoming, Laramie, WY, USA
Susan L. Jenkins
Affiliation:
Department of Animal Science, University of Wyoming, Laramie, WY, USA
Cun Li
Affiliation:
Department of Animal Science, University of Wyoming, Laramie, WY, USA Southwest National Primate Research Center, Texas Biomedical Research Institute, San Antonio, TX, USA
Peter W. Nathanielsz
Affiliation:
Department of Animal Science, University of Wyoming, Laramie, WY, USA Southwest National Primate Research Center, Texas Biomedical Research Institute, San Antonio, TX, USA
*
Address for correspondence: Hillary F. Huber, Texas Pregnancy & Life-Course Health Research Center, Herff Building 13, Texas Biomedical Research Institute, P.O. Box 760549, San Antonio, TX 78245-0549, USA. Email: hhuber4@uwyo.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

Nonhuman primate (NHP) studies are crucial to biomedical research. NHPs are the species most similar to humans in lifespan, body size, and hormonal profiles. Planning research requires statistical power evaluation, which is difficult to perform when lacking directly relevant preliminary data. This is especially true for NHP developmental programming studies, which are scarce. We review the sample sizes reported, challenges, areas needing further work, and goals of NHP maternal nutritional programming studies. The literature search included 27 keywords, for example, maternal obesity, intrauterine growth restriction, maternal high-fat diet, and maternal nutrient reduction. Only fetal and postnatal offspring studies involving tissue collection or imaging were included. Twenty-eight studies investigated maternal over-nutrition and 33 under-nutrition; 23 involved macaques and 38 baboons. Analysis by sex was performed in 19; minimum group size ranged from 1 to 8 (mean 4.7 ± 0.52, median 4, mode 3) and maximum group size from 3 to 16 (8.3 ± 0.93, 8, 8). Sexes were pooled in 42 studies; minimum group size ranged from 2 to 16 (mean 5.3 ± 0.35, median 6, mode 6) and maximum group size from 4 to 26 (10.2 ± 0.92, 8, 8). A typical study with sex-based analyses had group size minimum 4 and maximum 8 per sex. Among studies with sexes pooled, minimum group size averaged 6 and maximum 8. All studies reported some significant differences between groups. Therefore, studies with group sizes 3–8 can detect significance between groups. To address deficiencies in the literature, goals include increasing age range, more frequently considering sex as a biological variable, expanding topics, replicating studies, exploring intergenerational effects, and examining interventions.

Keywords

Maternal obesityintrauterine growth restrictionmaternal nutritionmaternal nutrient reductionmaternal western style diet

Information

Type
Review
Information
Journal of Developmental Origins of Health and Disease , Volume 11 , Issue 3 , June 2020 , pp. 297 - 306
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2019

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.)

Article purchase

Temporarily unavailable

Footnotes

Institution at which work was performed: Southwest National Primate Research Center, San Antonio, TX, USA.

References

Sullivan, EL, Rivera, HM, True, CA, et al. Maternal and postnatal high-fat diet consumption programs energy balance and hypothalamic melanocortin signaling in nonhuman primate offspring. Am J Physiol Regul Integr Comp Physiol. 2017; 313(2), R169–R179.CrossRefGoogle ScholarPubMed
Cox, LA, Li, C, Glenn, JP, et al. Expression of the placental transcriptome in maternal nutrient reduction in baboons is dependent on fetal sex. J Nutr. 2013; 143(11), 1698–1708.CrossRefGoogle ScholarPubMed
Gandhi, K, Li, C, German, N, et al. Effect of maternal high-fat diet on key components of the placental and hepatic endocannabinoid system. Am J Physiol Endocrinol Metab. 2017; 314(4), E322–E333.CrossRefGoogle ScholarPubMed
Guo, C, Li, C, Myatt, L, Nathanielsz, PW, Sun, K.Sexually dimorphic effects of maternal nutrient reduction on expression of genes regulating cortisol metabolism in fetal baboon adipose and liver tissues. Diabetes. 2013; 62(4), 1175–1185.CrossRefGoogle ScholarPubMed
McCurdy, CE, Schenk, S, Hetrick, B, et al. Maternal obesity reduces oxidative capacity in fetal skeletal muscle of Japanese macaques. JCI Insight. 2016; 1(16), e86612.CrossRefGoogle ScholarPubMed
Muralimanoharan, S, Li, C, Nakayasu, ES, et al. Sexual dimorphism in the fetal cardiac response to maternal nutrient restriction. J Mol Cell Cardiol. 2017; 108, 181–193.CrossRefGoogle ScholarPubMed
Pereira, SP, Oliveira, PJ, Tavares, LC, et al. Effects of moderate global maternal nutrient reduction on fetal baboon renal mitochondrial gene expression at 0.9 gestation. Am J Physiol Renal Physiol. 2015; 308(11), F1217–F1228.CrossRefGoogle ScholarPubMed
Tchoukalova, YD, Krishnapuram, R, White, UA, et al. Fetal baboon sex-specific outcomes in adipocyte differentiation at 0.9 gestation in response to moderate maternal nutrient reduction. Int J Obes (Lond). 2014; 38(2), 224–230.CrossRefGoogle ScholarPubMed
Franke, K, Clarke, GD, Dahnke, R, et al. Premature brain aging in baboons resulting from moderate fetal undernutrition. Front Aging Neurosci. 2017; 9, 92.CrossRefGoogle ScholarPubMed
Huber, HF, Considine, MM, Jenkins, S, Li, C, Nathanielsz, PW.Reproductive cycling in adult baboons (Papio species) that were intrauterine growth restricted at birth implies normal fertility but increased psychosocial stress. J Med Primatol. 2018; 47(6), 427–429.CrossRefGoogle ScholarPubMed
Kuo, AH, Li, C, Li, J, Huber, HF, Nathanielsz, PW, Clarke, GD.Cardiac remodelling in a baboon model of intrauterine growth restriction mimics accelerated ageing. J Physiol (Lond). 2017; 595(4), 1093–1110.CrossRefGoogle Scholar
Kuo, AH, Li, C, Huber, HF, Schwab, M, Nathanielsz, PW, Clarke, GD.Maternal nutrient restriction during pregnancy and lactation leads to impaired right ventricular function in young adult baboons. J Physiol. 2017; 595(13), 4245–4260.CrossRefGoogle ScholarPubMed
Kuo, AH, Li, C, Huber, HF, Clarke, GD, Nathanielsz, PW.Intrauterine growth restriction results in persistent vascular mismatch in adulthood. J Physiol (Lond). 2018; 596(23), 5777–5790.CrossRefGoogle ScholarPubMed
Kuo, AH, Li, J, Li, C, Huber, HF, Nathanielsz, PW, Clarke, GD.Poor perinatal growth impairs baboon aortic windkessel function. J Dev Orig Health Dis. 2018; 9(2), 137–142.CrossRefGoogle ScholarPubMed
Kuo, AH, Li, C, Mattern, V, et al. Sex-dimorphic acceleration of pericardial, subcutaneous, and plasma lipid increase in offspring of poorly nourished baboons. Int J Obes. 2018; 42(5), 1092–1096.CrossRefGoogle ScholarPubMed
Salmon, AB, Dorigatti, J, Huber, HF, Li, C, Nathanielsz, PW.Maternal nutrient restriction in baboon programs later-life cellular growth and respiration of cultured skin fibroblasts: a potential model for the study of aging-programming interactions. Geroscience. 2018; 40(3), 269–278.CrossRefGoogle Scholar
Thompson, JR, Valleau, JC, Barling, AN, et al. Exposure to a high-fat diet during early development programs behavior and impairs the central serotonergic system in juvenile non-human primates. Front Endocrinol (Lausanne). 2017; 8, 164.CrossRefGoogle ScholarPubMed
Grant, WF, Nicol, LE, Thorn, SR, Grove, KL, Friedman, JE, Marks, DL.Perinatal exposure to a high-fat diet is associated with reduced hepatic sympathetic innervation in one-year old male Japanese macaques. PLoS One. 2012; 7(10), e48119.CrossRefGoogle ScholarPubMed
Sullivan, EL, Grayson, B, Takahashi, D, et al. Chronic consumption of a high-fat diet during pregnancy causes perturbations in the serotonergic system and increased anxiety-like behavior in nonhuman primate offspring. J Neurosci. 2010; 30(10), 3826–3830.CrossRefGoogle ScholarPubMed
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(2), 91–102.CrossRefGoogle ScholarPubMed
Abu Shehab, M, Damerill, I, Shen, T, et al. Liver mTOR controls IGF-I bioavailability by regulation of protein kinase CK2 and IGFBP-1 phosphorylation in fetal growth restriction. Endocrinology. 2014; 155(4), 1327–1339.CrossRefGoogle ScholarPubMed
Antonow-Schlorke, I, Schwab, M, Cox, LA, et al. Vulnerability of the fetal primate brain to moderate reduction in maternal global nutrient availability. PNAS. 2011; 108(7), 3011–3016.CrossRefGoogle ScholarPubMed
Cox, LA, Nijland, MJ, Gilbert, JS, et al. Effect of 30 per cent maternal nutrient restriction from 0.16 to 0.5 gestation on fetal baboon kidney gene expression. J Physiol. 2006; 572(1), 67–85.CrossRefGoogle ScholarPubMed
Cox, J, Williams, S, Grove, K, Lane, RH, Aagaard-Tillery, KM.A maternal high-fat diet is accompanied by alterations in the fetal primate metabolome. Am J Obstet Gynecol. 2009; 201(3), 281.e1–9.CrossRefGoogle ScholarPubMed
DuBois, BN, O’Tierney-Ginn, P, Pearson, J, Friedman, JE, Thornburg, K, Cherala, G.Maternal obesity alters feto-placental cytochrome P4501A1 activity. Placenta. 2012; 33(12), 1045–1051.CrossRefGoogle ScholarPubMed
Farley, D, Tejero, ME, Comuzzie, AG, et al. Feto-placental adaptations to maternal obesity in the baboon. Placenta. 2009; 30(9), 752–760.CrossRefGoogle ScholarPubMed
Frias, AE, Morgan, TK, Evans, AE, et al. Maternal high-fat diet disturbs uteroplacental hemodynamics and increases the frequency of stillbirth in a nonhuman primate model of excess nutrition. Endocrinology. 2011; 152(6), 2456–2464.CrossRefGoogle Scholar
Grant, WF, Gillingham, MB, Batra, AK, et al. Maternal high fat diet is associated with decreased plasma n-3 fatty acids and fetal hepatic apoptosis in nonhuman primates. PLoS One. 2011; 6(2), e17261.CrossRefGoogle ScholarPubMed
Grayson, BE, Levasseur, PR, Williams, SM, Smith, MS, Marks, DL, Grove, KL.Changes in melanocortin expression and inflammatory pathways in fetal offspring of nonhuman primates fed a high-fat diet. Endocrinology. 2010; 151(4), 1622–1632.CrossRefGoogle ScholarPubMed
Hellmuth, C, Uhl, O, Kirchberg, FF, et al. Influence of moderate maternal nutrition restriction on the fetal baboon metabolome at 0.5 and 0.9 gestation. Nutr Metab Cardiovasc Dis. 2016; 26(9), 786–796.CrossRefGoogle ScholarPubMed
Kamat, A, Nijland, MJ, McDonald, TJ, Cox, LA, Nathanielsz, PW, Li, C.Moderate global reduction in maternal nutrition has differential stage of gestation specific effects on β1- and β2-adrenergic receptors in the fetal baboon liver. Reprod Sci. 2011; 18(4), 398–405.CrossRefGoogle Scholar
Kavitha, JV, Rosario, FJ, Nijland, MJ, et al. Down-regulation of placental mTOR, insulin/IGF-I signaling, and nutrient transporters in response to maternal nutrient restriction in the baboon. FASEB J. 2014; 28(3), 1294–1305.CrossRefGoogle ScholarPubMed
Li, C, Levitz, M, Hubbard, GB, et al. The IGF axis in baboon pregnancy: placental and systemic responses to feeding 70% global ad libitum diet. Placenta. 2007; 28(11–12), 1200–1210.CrossRefGoogle ScholarPubMed
Li, C, Schlabritz-Loutsevitch, NE, Hubbard, GB, et al. Effects of maternal global nutrient restriction on fetal baboon hepatic insulin-like growth factor system genes and gene products. Endocrinology. 2009; 150(10), 4634–4642.CrossRefGoogle ScholarPubMed
Li, C, Ramahi, E, Nijland, MJ, et al. Up-regulation of the fetal baboon hypothalamo-pituitary-adrenal axis in intrauterine growth restriction: coincidence with hypothalamic glucocorticoid receptor insensitivity and leptin receptor down-regulation. Endocrinology. 2013; 154(7), 2365–2373.CrossRefGoogle ScholarPubMed
Li, C, McDonald, TJ, Wu, G, Nijland, MJ, Nathanielsz, PW.Intrauterine growth restriction alters term fetal baboon hypothalamic appetitive peptide balance. J Endocrinol. 2013; 217(3), 275–282.CrossRefGoogle ScholarPubMed
Maloyan, A, Muralimanoharan, S, Huffman, S, et al. Identification and comparative analyses of myocardial miRNAs involved in the fetal response to maternal obesity. Physiol Genomics. 2013; 45(19), 889–900.CrossRefGoogle ScholarPubMed
McDonald, TJ, Wu, G, Nijland, MJ, Jenkins, SL, Nathanielsz, PW, Jansson, T.Effect of 30 % nutrient restriction in the first half of gestation on maternal and fetal baboon serum amino acid concentrations. Br J Nutr. 2013; 109(08), 1382–1388.CrossRefGoogle ScholarPubMed
Nathanielsz, PW, Yan, J, Green, R, et al. Maternal obesity disrupts the methionine cycle in baboon pregnancy. Physiol Rep. 2015; 3(11), e12564.CrossRefGoogle ScholarPubMed
Nijland, MJ, Schlabritz-Loutsevitch, NE, Hubbard, GB, Nathanielsz, PW, Cox, LA.Non-human primate fetal kidney transcriptome analysis indicates mammalian target of rapamycin (mTOR) is a central nutrient-responsive pathway. J Physiol. 2007; 579(3), 643–656.CrossRefGoogle ScholarPubMed
Roberts, VHJ, Pound, LD, Thorn, SR, et al. Beneficial and cautionary outcomes of resveratrol supplementation in pregnant nonhuman primates. FASEB J. 2014; 28(6), 2466–2477.CrossRefGoogle ScholarPubMed
Suter, MA, Sangi-Haghpeykar, H, Showalter, L, et al. Maternal high-fat diet modulates the fetal thyroid axis and thyroid gene expression in a nonhuman primate model. Mol Endocrinol. 2012; 26(12), 2071–2080.CrossRefGoogle Scholar
Suter, MA, Chen, A, Burdine, MS, et al. A maternal high-fat diet modulates fetal SIRT1 histone and protein deacetylase activity in nonhuman primates. FASEB J. 2012; 26(12), 5106–5114.CrossRefGoogle ScholarPubMed
Li, C, Shu, Z-J, Lee, S, et al. Effects of maternal nutrient restriction, intrauterine growth restriction, and glucocorticoid exposure on phosphoenolpyruvate carboxykinase-1 expression in fetal baboon hepatocytes in vitro. J Med Primatol. 2013; 42(4), 211–219.CrossRefGoogle ScholarPubMed
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(2), 323–335.Google ScholarPubMed
Unterberger, A, Szyf, M, Nathanielsz, PW, Cox, LA.Organ and gestational age effects of maternal nutrient restriction on global methylation in fetal baboons. J Med Primatol. 2009; 38(4), 219–227.CrossRefGoogle ScholarPubMed
Ye, W, Xie, L, Li, C, Nathanielsz, PW, Thompson, BJ.Impaired development of fetal serotonergic neurons in intrauterine growth restricted baboons. J Med Primatol. 2014; 43(4), 284–287.CrossRefGoogle ScholarPubMed
Pantham, P, Rosario, FJ, Weintraub, ST, et al. Down-regulation of placental transport of amino acids precedes the development of intrauterine growth restriction in maternal nutrient restricted baboons. Biol Reprod. 2016; 95(5), 98.CrossRefGoogle ScholarPubMed
Puppala, S, Li, C, Glenn, JP, et al. Primate fetal hepatic responses to maternal obesity: epigenetic signalling pathways and lipid accumulation. J Physiol (Lond). 2018; 596(23), 5823–5837.CrossRefGoogle ScholarPubMed
Nijland, MJ, Mitsuya, K, Li, C, et al. Epigenetic modification of fetal baboon hepatic phosphoenolpyruvate carboxykinase following exposure to moderately reduced nutrient availability. J Physiol. 2010; 588(8), 1349–1359.CrossRefGoogle ScholarPubMed
Xie, L, Antonow-Schlorke, I, Schwab, M, McDonald, TJ, Nathanielsz, PW, Li, C.The frontal cortex IGF system is down regulated in the term, intrauterine growth restricted fetal baboon. Growth Horm IGF Res. 2013; 23(5), 187–192.CrossRefGoogle ScholarPubMed
Fan, L, Lindsley, SR, Comstock, SM, et al. Maternal high-fat diet impacts endothelial function in nonhuman primate offspring. Int J Obes (Lond). 2013; 37(2), 254.CrossRefGoogle ScholarPubMed
Ma, J, Prince, AL, Bader, D, et al. High-fat maternal diet during pregnancy persistently alters the offspring microbiome in a primate model. Nat Commun. 2014; 5, 3889.CrossRefGoogle Scholar
Suter, MA, Takahashi, D, Grove, KL, Aagaard, KM.Postweaning exposure to a high-fat diet is associated with alterations to the hepatic histone code in Japanese macaques. Pediatr Res. 2013; 74(3), 252–258.CrossRefGoogle ScholarPubMed
Pace, RM, Prince, AL, Ma, J, et al. Modulations in the offspring gut microbiome are refractory to postnatal synbiotic supplementation among juvenile primates. BMC Microbiol. 2018; 18(1), 28.CrossRefGoogle ScholarPubMed
Rivera, HM, Kievit, P, Kirigiti, MA, et al. Maternal high-fat diet and obesity impact palatable food intake and dopamine signaling in nonhuman primate offspring. Obesity. 2015; 23(11), 2157–2164.CrossRefGoogle ScholarPubMed
Choi, J, Li, C, McDonald, TJ, Comuzzie, A, Mattern, V, Nathanielsz, PW.Emergence of insulin resistance in juvenile baboon offspring of mothers exposed to moderate maternal nutrient reduction. Am J Physiol Regul Integr Comp Physiol. 2011; 301(3), R757–R762.CrossRefGoogle ScholarPubMed
Comstock, SM, Pound, LD, Bishop, JM, et al. High-fat diet consumption during pregnancy and the early post-natal period leads to decreased α cell plasticity in the nonhuman primate. Mol Metab. 2012; 2(1), 10–22.CrossRefGoogle ScholarPubMed
Suter, M, Bocock, P, Showalter, L, et al. Epigenomics: maternal high-fat diet exposure in utero disrupts peripheral circadian gene expression in nonhuman primates. FASEB J. 2011; 25(2), 714–726.CrossRefGoogle ScholarPubMed
Li, C, Jenkins, SL, Mattern, V, et al. Effect of moderate, 30 percent global maternal nutrient reduction on fetal and postnatal baboon phenotype. J Med Primatol. 2017; 46(6), 293–303.CrossRefGoogle ScholarPubMed
Pound, LD, Comstock, SM, Grove, KL.Consumption of a Western-style diet during pregnancy impairs offspring islet vascularization in a Japanese macaque model. Am J Physiol Endocrinol Metab. 2014; 307(1), E115–E123.CrossRefGoogle Scholar
Dwan, K, Gamble, C, Williamson, PR, Kirkham, JJ, Reporting Bias Group. Systematic review of the empirical evidence of study publication bias and outcome reporting bias – an updated review. PLoS ONE. 2013; 8(7), e66844.CrossRefGoogle ScholarPubMed
Paterson, JD.Coming to America: acclimation in macaque body structures and Bergmann’s rule. Int J Primatol. 1996; 17(4), 585–611.CrossRefGoogle Scholar
Coelho, AM.Baboon dimorphism: growth in weight, length and adiposity from birth to 8 years of age. In Nonhuman Primate Models for Human Growth and Development (ed. Watts, ES), 1985; pp. 125–159. Alan R. Liss, New York.Google Scholar
Bronikowski, AM, Alberts, SC, Altmann, J, Packer, C, Carey, KD, Tatar, M.The aging baboon: comparative demography in a non-human primate. PNAS. 2002; 99(14), 9591–9595.CrossRefGoogle Scholar
Pavelka, MS, Fedigan, LM.Reproductive termination in female Japanese monkeys: a comparative life history perspective. Am J Phys Anthropol. 1999; 109(4), 455–464.3.0.CO;2-Z>CrossRefGoogle ScholarPubMed
Harvey, PH, Clutton-Brock, TH.Life history variation in primates. Evolution. 1985; 39(3), 559–581.CrossRefGoogle ScholarPubMed
Schlabritz-Loutsevitch, NE, Howell, K, Rice, K, et al. Development of a system for individual feeding of baboons maintained in an outdoor group social environment. J Med Primatol. 2004; 33(3), 117–126.CrossRefGoogle Scholar
Huber, HF, Kuo, AH, Li, C, et al. Antenatal synthetic glucocorticoid exposure at human therapeutic equivalent doses predisposes middle-age male offspring baboons to an obese phenotype that emerges with aging. Reprod Sci. 2019; 26(5), 591–599.CrossRefGoogle Scholar
Kuo, AH, Huber, HF, Li, C, Li, J, Nathanielsz, PW, Clarke, GD.Accelerated right heart aging in IUGR offspring of undernourished pregnant baboons. Reprod Sci. 2016; 23(Suppl. 1), 147A.Google Scholar
Bertram, C, Khan, O, Ohri, S, Phillips, DI, Matthews, SG, Hanson, MA.Transgenerational effects of prenatal nutrient restriction on cardiovascular and hypothalamic-pituitary-adrenal function. J Physiol (Lond). 2008; 586(8), 2217–2229.CrossRefGoogle ScholarPubMed
Aiken, CE, Ozanne, SE.Transgenerational developmental programming. Hum Reprod Update. 2014; 20(1), 63–75.CrossRefGoogle ScholarPubMed
Radford, EJ, Ito, M, Shi, H, et al. In utero undernourishment perturbs the adult sperm methylome and intergenerational metabolism. Science. 2014; 345(6198), 1255903.CrossRefGoogle ScholarPubMed
Reyes-Castro, LA, Rodríguez-González, GL, Chavira, R, et al. Paternal line multigenerational passage of altered risk assessment behavior in female but not male rat offspring of mothers fed a low protein diet. Physiol Behav. 2015; 140, 89–95.CrossRefGoogle Scholar
Burdge, GC, Slater-Jefferies, J, Torrens, C, Phillips, ES, Hanson, MA, Lillycrop, KA.Dietary protein restriction of pregnant rats in the F0 generation induces altered methylation of hepatic gene promoters in the adult male offspring in the F1 and F2 generations. Br J Nutr. 2007; 97(3), 435–439.CrossRefGoogle ScholarPubMed
Pankey, CL, Walton, MW, Odhiambo, JF, et al. Intergenerational impact of maternal overnutrition and obesity throughout pregnancy in sheep on metabolic syndrome in grandsons and granddaughters. Domest Anim Endocrinol. 2017; 60, 67–74.CrossRefGoogle ScholarPubMed
Shasa, DR, Odhiambo, JF, Long, NM, Tuersunjiang, N, Nathanielsz, PW, Ford, SP.Multigenerational impact of maternal overnutrition/obesity in the sheep on the neonatal leptin surge in granddaughters. Int J Obes (Lond). 2015; 39(4), 695–701.CrossRefGoogle ScholarPubMed
Zambrano, E, Nathanielsz, PW.Mechanisms by which maternal obesity programs offspring for obesity: evidence from animal studies. Nutr Rev. 2013; 71(Suppl. 1), S42–S54.CrossRefGoogle ScholarPubMed
Aiken, CE, Ozanne, SE.Sex differences in developmental programming models. Reproduction. 2013; 145(1), R1–R13.CrossRefGoogle ScholarPubMed
Sandman, CA, Glynn, LM, Davis, EP.Is there a viability-vulnerability tradeoff? Sex differences in fetal programming. J Psychosom Res. 2013; 75(4), 327–335.CrossRefGoogle Scholar
Dasinger, JH, Alexander, BT.Gender differences in developmental programming of cardiovascular diseases. Clin Sci. 2016; 130(5), 337–348.CrossRefGoogle ScholarPubMed
Gilbert, JS, Nijland, MJ.Sex differences in the developmental origins of hypertension and cardiorenal disease. Am J Physiol Regul Integr Comp Physiol. 2008; 295(6), R1941–R1952.CrossRefGoogle ScholarPubMed
Ojeda, NB, Intapad, S, Alexander, BT.Sex differences in the developmental programming of hypertension. Acta Physiol (Oxf). 2014; 210(2), 307–316.CrossRefGoogle ScholarPubMed
Dearden, L, Bouret, SG, Ozanne, SE.Sex and gender differences in developmental programming of metabolism. Mol Metab. 2018; 15, 8–19.CrossRefGoogle Scholar
Huber, HF, Bartlett, TQ, Smith, BK, Li, C, Jenkins, SL, Nathanielsz, PW.Birth sex ratio in baboon mothers fed ad lib, reduced or obesogenic diet. Reprod Sci. 2016; 23(1 Suppl), 236A.Google Scholar
Clutton-Brock, TH, Albon, SD, Guinness, FE.Parental investment and sex differences in juvenile mortality in birds and mammals. Nature. 1985; 313(5998), 131–133.CrossRefGoogle Scholar
van Schaik, CP, Hrdy, SB.Intensity of local resource competition shapes the relationship between maternal rank and sex ratios at birth in cercopithecine primates. Am Nat. 1991; 138(6), 1555–1562.CrossRefGoogle Scholar
Silk, JB, Brown, GR.Local resource competition and local resource enhancement shape primate birth sex ratios. Proc R Soc B. 2008; 275(1644), 1761–1765.CrossRefGoogle ScholarPubMed
Vega, CC, Reyes-Castro, LA, Rodríguez-González, GL, et al. Resveratrol partially prevents oxidative stress and metabolic dysfunction in pregnant rats fed a low protein diet and their offspring. J Physiol (Lond). 2016; 594(5), 1483–1499.CrossRefGoogle ScholarPubMed
Zou, T, Chen, D, Yang, Q, et al. Resveratrol supplementation of high-fat diet-fed pregnant mice promotes brown and beige adipocyte development and prevents obesity in male offspring. J Physiol (Lond). 2016; 595(5), 1547–1562.CrossRefGoogle Scholar
Vega, CC, Reyes-Castro, LA, Bautista, CJ, Larrea, F, Nathanielsz, PW, Zambrano, E.Exercise in obese female rats has beneficial effects on maternal and male and female offspring metabolism. Int J Obes (Lond). 2015; 39(4), 712–719.CrossRefGoogle ScholarPubMed
Santos, M, Rodríguez-González, GL, Ibáñez, C, Vega, CC, Nathanielsz, PW, Zambrano, E.Adult exercise effects on oxidative stress and reproductive programming in male offspring of obese rats. Am J Physiol Regul Integr Comp Physiol. 2015; 308(3), R219–R225.CrossRefGoogle ScholarPubMed
Tarry-Adkins, JL, Fernandez-Twinn, DS, Madsen, R, et al. Coenzyme Q10 prevents insulin signaling dysregulation and inflammation prior to development of insulin resistance in male offspring of a rat model of poor maternal nutrition and accelerated postnatal growth. Endocrinology. 2015; 156(10), 3528–3537.CrossRefGoogle ScholarPubMed
Tarry-Adkins, JL, Fernandez-Twinn, DS, Hargreaves, IP, et al. Coenzyme Q10 prevents hepatic fibrosis, inflammation, and oxidative stress in a male rat model of poor maternal nutrition and accelerated postnatal growth. Am J Clin Nutr. 2016; 103(2), 579–588.CrossRefGoogle Scholar
Rabadán-Diehl, C, Nathanielsz, P.From mice to men: research models of developmental programming. J Dev Orig Health Dis. 2013; 4(01), 3–9.CrossRefGoogle ScholarPubMed