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Developmental programming of reproduction and fertility: what is the evidence?*

Published online by Cambridge University Press:  01 August 2008

D. S. Gardner ,
R. G. Lea  and
K. D. Sinclair
D. S. Gardner*
Affiliation:
School of Veterinary Medicine and Science, Sutton Bonington Campus, University of Nottingham, Loughborough LE12 5RA, UK
R. G. Lea
Affiliation:
School of Veterinary Medicine and Science, Sutton Bonington Campus, University of Nottingham, Loughborough LE12 5RA, UK
K. D. Sinclair
Affiliation:
School of Biosciences, Sutton Bonington Campus, University of Nottingham, Loughborough LE12 5RA, UK
*
E-mail: david.gardner@nottingham.ac.uk or kevin.sinclair@nottingham.ac.uk
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Abstract

The concept of the foetal/developmental origins of adult disease has been around for ~20 years and from the original epidemiological studies in human populations much more evidence has accumulated from the many studies in animal models. The majority of these have focused upon the role of early dietary intake before conception, through gestation and/or lactation and subsequent interactions with the postnatal environment, e.g. dietary and physical activity exposures. Whilst a number of theoretical models have been proposed to place the experimental data into a biological context, the underlying phenomena remain the same; developmental deficits (of single (micro) nutrients) during critical or sensitive periods of tissue growth alter the developmental pathway to ultimately constrain later functional capacity when the individual is adult. Ageing, without exception, exacerbates any programmed sequelae. Thus, adult phenotypes that have been relatively easy to characterise (e.g. blood pressure, insulin sensitivity, body fat mass) have received most attention in the literature. To date, relatively few studies have considered the effect of differential early environmental exposures on reproductive function and fecundity in predominantly mono-ovular species such as the sheep, cow and human. The available evidence suggests that prenatal insults, undernutrition for example, have little effect on lifetime reproductive capacity despite subtle effects on the hypothalamic–pituitary–gonadal axis and gonadal progenitor cell complement. The postnatal environment is clearly important, however, since neonatal/adolescent growth acceleration (itself not independent from prenatal experience) has been shown to significantly influence fecundity in farm animals. The present paper will expand these interesting areas of investigation and review the available evidence regarding developmental programming of reproduction and fertility. However, it appears there is little strong evidence to indicate that offspring fertility and reproductive senescence in the human and in farm animal species are overtly affected by prenatal nutrient exposure. Nevertheless, it is clear that the developing gonad is sensitive to its immediate environment but more detailed investigation is required to specifically test the long-term consequences of nutritional perturbations during pregnancy on adult reproductive well-being.

Keywords

nutritionprogrammingreproductionfertilityfarm animals
Type
Full Paper
Information
animal , Volume 2 , Issue 8 , August 2008 , pp. 1128 - 1134
Copyright
Copyright © The Animal Consortium 2008

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Footnotes

*

This invited paper was presented at BSAS meeting ‘Fertility in Dairy Cows – bridging the gaps’, 30–31 August 2007, Liverpool Hope University.

References

Allden, WG 1979. Undernutrition of the Merion sheep and its sequelae. V. The influence of severe growth restriction during early post-natal life on reproduction and growth in later life. Australian Journal of Agricultural Research 30, 939–948.CrossRefGoogle Scholar
Armitage, JA, Khan, IY, Taylor, PD, Nathanielsz, PW, Poston, L 2004. Developmental programming of metabolic syndrome by maternal nutritional imbalance; how strong is the evidence from experimental models in mammals? Journal of Physiology 561, 355–377.CrossRefGoogle ScholarPubMed
Barker, DJ, Osmond, C 1986. Infant mortality, childhood nutrition, and ischaemic heart disease in England and Wales. Lancet 327, 1077–1081.CrossRefGoogle Scholar
Barker, DJ, Osmond, C 1988. Low birth weight and hypertension. British Medical Journal 297, 134–135.CrossRefGoogle ScholarPubMed
Barker, DJ, Osmond, C, Forsen, TJ, Kajantie, E, Eriksson, JG 2005. Trajectories of growth among children who have coronary events as adults. New England Journal of Medicine 353, 1802–1809.CrossRefGoogle ScholarPubMed
Cameron, N, Preece, MA, Cole, TJ 2005. Catch-up growth or regression to the mean? Recovery from stunting revisited. American Journal of Human Biology 17, 412–417.CrossRefGoogle ScholarPubMed
Catalano, PM, Kirwan, JP, Haugel-de Mouzon, S, King, J 2003. Gestational diabetes and insulin resistance: role in short- and long-term implications for mother and fetus. Journal of Nutrition 133 (suppl. 2), 1674S–1683S.CrossRefGoogle Scholar
Cresswell, JL, Egger, P, Fall, CH, Osmond, C, Fraser, RB, Barker, DJ 1997. Is the age of menopause determined in-utero? Early Human Development 49, 143–148.CrossRefGoogle ScholarPubMed
Da Silva, P, Aitken, RP, Rhind, SM, Racey, PA, Wallace, JM 2001. Influence of placentally mediated fetal growth restriction on the onset of puberty in male and female lambs. Reproduction 122, 375–383.CrossRefGoogle ScholarPubMed
Da Silva, P, Aitken, RP, Rhind, SM, Racey, PA, Wallace, JM 2002. Impact of maternal nutrition during pregnancy on pituitary gonadotrophin gene expression and ovarian development in growth-restricted and normally grown late gestation sheep fetuses. Reproduction 123, 769–777.CrossRefGoogle ScholarPubMed
Da Silva, P, Aitken, RP, Rhind, SM, Racey, PA, Wallace, JM 2003. Effect of maternal overnutrition during pregnancy on pituitary gonadotrophin gene expression and gonadal morphology in female and male foetal sheep at day 103 of gestation. Placenta 24, 248–257.CrossRefGoogle ScholarPubMed
Despres, JP, Lemieux, I 2006. Abdominal obesity and metabolic syndrome. Nature 444, 881–887.CrossRefGoogle ScholarPubMed
Elias, SG, van Noord, PAH, Peeters, PHM, den Tonkelaar, I, Grobbee, DE 2005. Childhood exposure to the 1944–1945 Dutch famine and subsequent female reproductive function. Human Reproduction 20, 2483–2488.CrossRefGoogle Scholar
Eriksson, J, Forsen, T, Tuomilehto, J, Osmond, C, Barker, D 2000. Fetal and childhood growth and hypertension in adult life. Hypertension 36, 790–794.CrossRefGoogle ScholarPubMed
Gardner, DS, Bell, RC, Symonds, ME 2007. Fetal mechanisms that lead to later hypertension. Current Drug Targets 8, 894–905.CrossRefGoogle ScholarPubMed
Gluckman, PD, Hanson, MA 2004. Living with the past: evolution, development, and patterns of disease. Science 305, 1733–1736.CrossRefGoogle ScholarPubMed
Gunn, RG 1983. The influence of nutrition on the reproductive perfomance of ewes. In Sheep production (ed. W Haresign), pp. 99–110. Butterworths, London.Google Scholar
Gunn, RG, Sim, DA, Hunter, EA 1995. Effects of nutrition in utero and in early life on the subsequent lifetime reproductive performance of Scottish Blackface ewes in two management systems. Animal Science 60, 223–230.CrossRefGoogle Scholar
Hales, CN, Barker, DJ 2001. The thrifty phenotype hypothesis. British Medical Bulletin 60, 5–20.CrossRefGoogle ScholarPubMed
Hardy, R, Kuh, D 2002. Does early growth influence timing of the menopause? Evidence from a British birth cohort. Human Reproduction 17, 2474–2479.CrossRefGoogle ScholarPubMed
Huxley, R, Neil, A, Collins, R 2002. Unravelling the fetal origins hypothesis: is there really an inverse association between birthweight and subsequent blood pressure? Lancet 360, 659–665.CrossRefGoogle ScholarPubMed
Ibanez, L, Potau, N, Ferrer, A, Rodriguez-Hierro, F, Marcos, MV, de Zegher, F 2002a. Anovulation in eumenorrheic, nonobese adolescent girls born small for gestational age: insulin sensitization induces ovulation, increases lean body mass, and reduces abdominal fat excess, dyslipidemia, and subclinical hyperandrogenism. Journal of Clinical Endocrinology and Metabolism 87, 5702–5705.CrossRefGoogle ScholarPubMed
Ibanez, L, Potau, N, Ferrer, A, Rodriguez-Hierro, F, Marcos, MV, de Zegher, F 2002b. Reduced ovulation rate in adolescent girls born small for gestational age. Journal of Clinical Endocrinology and Metabolism 87, 3391–3393.CrossRefGoogle ScholarPubMed
Jackson, AA 1996. Perinatal nutrition: the impact on postnatal growth and development. In Pediatrics and perinataology. The scientific basis (ed. PD Gluckman, MA Heymann, K Goldstone and PD Sugan), pp. 298–303. Arnold, London.Google Scholar
Kuzawa, CW 2005. Fetal origins of developmental plasticity: are fetal cues reliable predictors of future nutritional environments? American Journal of Human Biology 17, 5–21.CrossRefGoogle ScholarPubMed
Langley-Evans, SC 2004. Experimental models of hypertension and cardiovascular disease. In Fetal nutrition and adult disease: programming of chronic disease through fetal exposure to undernutrition (ed. SC Langley-Evans), pp. 129–156. CAB International, Wallingford.CrossRefGoogle Scholar
Lea, RG, Andrade, LP, Rae, MT, Hannah, LT, Kyle, CE, Murray, JF, Rhind, SM, Miller, DW 2006. Effects of maternal undernutrition during early pregnancy on apoptosis regulators in the ovine fetal ovary. Reproduction 131, 113–124.CrossRefGoogle ScholarPubMed
Lucas, A, Fewtrell, MS, Cole, TJ 1999. Fetal origins of adult disease – the hypothesis revisited. British Medical Journal 319, 245–249.CrossRefGoogle ScholarPubMed
Lumey, LH 1998. Reproductive outcomes in women prenatally exposed to undernutrition: a review of findings from the Dutch famine birth cohort. Proceedings of the Nutrition Society 57, 129–135.CrossRefGoogle ScholarPubMed
Lumey, LH, Stein, AD 1997. In utero exposure to famine and subsequent fertility: the Dutch Famine Birth Cohort Study. American Journal Public Health 87, 1962–1966.CrossRefGoogle ScholarPubMed
Martin, JL, Vonnahme, KA, Adams, DC, Lardy, GP, Funston, RN 2007. Effects of dam nutrition on growth and reproductive performance of heifer calves. Journal of Animal Science 85, 841–847.CrossRefGoogle ScholarPubMed
McMillen, IC, Robinson, JS 2005. Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Physiological Reviews 85, 571–633.CrossRefGoogle ScholarPubMed
Murdoch, WJ, Van Kirk, EA, Vonnahme, KA, Ford, SP 2003. Ovarian responses to undernutrition in pregnant ewes, USA. Reproductive Biology Endocrinology 1, 6.CrossRefGoogle ScholarPubMed
Ozanne, SE, Hales, CN 2004. Lifespan: catch-up growth and obesity in male mice. Nature 427, 411–412.CrossRefGoogle ScholarPubMed
Painter, RC, Roseboom, TJ, Bleker, OP 2005. Prenatal exposure to the Dutch famine and disease in later life: an overview. Reproductive Toxicology 20, 345–352.CrossRefGoogle Scholar
Phelan, JP, Rose, MR 2005. Why dietary restriction substantially increases longevity in animal models but won’t in humans. Ageing Research Reviews 4, 339–350.CrossRefGoogle ScholarPubMed
Popkin, BM 2006. Global nutrition dynamics: the world is shifting rapidly toward a diet linked with noncommunicable diseases. American Journal of Clinical Nutrition 84, 289–298.CrossRefGoogle Scholar
Pryce, JE, Simm, G, Robinson, JJ 2002. Effects of selection for production and maternal diet on maiden daity heifer fertility. Animal Science 74, 415–421.CrossRefGoogle Scholar
Rae, MT, Palassio, S, Kyle, CE, Brooks, AN, Lea, RG, Miller, DW, Rhind, SM 2001. Effect of maternal undernutrition during pregnancy on early ovarian development and subsequent follicular development in sheep fetuses. Reproduction 122, 915–922.CrossRefGoogle ScholarPubMed
Rae, MT, Kyle, CE, Miller, DW, Hammond, AJ, Brooks, AN, Rhind, SM 2002. The effects of undernutrition, in utero, on reproductive function in adult male and female sheep. Animal Reproduction Science 72, 63–71.CrossRefGoogle ScholarPubMed
Rhind, SM, Elston, DA, Jones, JR, Rees, ME, McMillen, SR, Gunn, RG 1998. Effects of restriction of growth and development of Brecon Cheviot ewe lambs on subsequent lifetime reproductive performance. Small Ruminant Research 30, 121–126.CrossRefGoogle Scholar
Rich-Edwards, J 2004. Epidemiology of the fetal origins of adult disease: cohort studies of birthweight and cardiovascular disease. In Fetal nutrition and adult disease: programming of chronic disease through fetal exposure to undernutrition (ed. SC Langley-Evans), pp. 87–104. CAB International, Wallingford.CrossRefGoogle Scholar
Rodrigues, S, Robinson, E, Gray-Donald, K 1999. Prevalence of gestational diabetes mellitus among James Bay Cree women in northern Quebec. Canadian Medical Association Journal 160, 1293–1297.Google ScholarPubMed
Sinclair, KD, Lea, RG, Rees, WD, Young, LE 2007. The developmental origins of health and disease: current theories and epigenetic mechanisms. Society of Reproduction and Fertility, Supplement 64, 425–443.Google ScholarPubMed
Singhal, A, Lucas, A 2004. Early origins of cardiovascular disease: is there a unifying hypothesis? Lancet 363, 1642–1645.CrossRefGoogle Scholar
Swali, A, Wathes, DC 2006. Influence of the dam and sire on size at birth and subsequent growth, milk production and fertility in dairy heifers. Theriogenology 66, 1173–1184.CrossRefGoogle ScholarPubMed
Treloar, SA, Sadrzadeh, S, Do, KA, Martin, NG, Lambalk, CB 2000. Birth weight and age at menopause in Australian female twin pairs: exploration of the fetal origin hypothesis. Human Reproduction 15, 55–59.CrossRefGoogle ScholarPubMed
Wallace, JM, Aitken, RP, Cheyne, MA 1996. Nutrient partitioning and fetal growth in rapidly growing adolescent ewes. Journal of Reproduction and Fertility 107, 183–190.CrossRefGoogle ScholarPubMed
Wells, JC 2007. The programming effects of early growth. Early Human Development 83, 743–748.CrossRefGoogle ScholarPubMed
Yajnik, CS 2004. Early life origins of insulin resistance and type 2 diabetes in India and other Asian countries. Journal of Nutrition 134, 205–210.CrossRefGoogle ScholarPubMed