Skip to main content Accessibility help
×
Home

A conceptual framework for the developmental origins of health and disease

  • P. D. Gluckman (a1) (a2), M. A. Hanson (a3) and T. Buklijas (a1)

Abstract

In the last decades, the developmental origins of health and disease (DOHaD) have emerged as a vigorous field combining experimental, clinical, epidemiological and public health research. Its goal is to understand how events in early life shape later morbidity risk, especially of non-communicable chronic diseases. As these diseases become the major cause of morbidity and mortality worldwide, research arising from DOHaD is likely to gain significance to public health and economic development. But action may be hindered by the lack of a firm mechanistic explanation and of a conceptual basis, especially regarding the evolutionary significance of the DOHaD phenomenon. In this article, we provide a succinct historical review of the research into the relationship between development and later disease, consider the evolutionary and developmental significance and discuss the underlying mechanisms of the DOHaD phenomenon. DOHaD should be viewed as a part of a broader biological mechanism of plasticity by which organisms, in response to cues such as nutrition or hormones, adapt their phenotype to environment. These responses may be divided into those for immediate benefit and those aimed at prediction of a future environment: disease occurs in the mismatch between predicted and realized future. The likely mechanisms that enable plasticity involve epigenetic processes, affecting the expression of genes associated with regulatory pathways. There is now evidence that epigenetic marks may be inherited and so contribute to non-genomic heritable disease risk. We end by discussing the global significance of the DOHaD phenomenon and its potential applications for public health purposes.

  • View HTML
    • Send article to Kindle

      To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

      Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      A conceptual framework for the developmental origins of health and disease
      Available formats
      ×

      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

      A conceptual framework for the developmental origins of health and disease
      Available formats
      ×

      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

      A conceptual framework for the developmental origins of health and disease
      Available formats
      ×

Copyright

Corresponding author

Address for correspondence: P. D. Gluckman, Liggins Institute, The University of Auckland, Private Bag 92019, Auckland 1023, New Zealand. (Email pd.gluckman@auckland.ac.nz)

References

Hide All
1.Goldstein, DB. Common genetic variation and human traits. N Engl J Med. 2009; 360, 16961698.
2.Hirschhorn, JN. Genome-wide association studies – illuminating biologic pathways. N Engl J Med. 2009; 360, 16991701.
3.Chi, KR. Human genetics: hit or miss? Nature. 2009; 461, 712714.
4.The Wellcome Trust Case Control Consortium. Genome-wide association study of 14,000 cases of seven common diseases and 3,000 shared controls. Nature. 2007; 447, 661678.
5.Maher, B. Personal genomes: the case of the missing heritability. Nature. 2008; 456, 1821.
6.Hayden Check, E. Genomics shifts focus to rare diseases. Nature. 2009; 461, 458459.
7.Allis, CD, Jenuwein, T, Reinberg, D (eds) Epigenetics, 2007. Cold Spring Harbor Laboratory Press: Cold Spring Harbor: NY.
8.Amundsen, R. The Changing Role of the Embryo in Evolutionary Thought: Roots of Evo-Devo, 2005. Cambridge University Press: Cambridge.
9.Gilbert, SF. Ecological developmental biology: developmental biology meets the real world. Dev Biol. 2001; 233, 112.
10.Oyama, S. The Ontogeny of Information: Developmental Systems and Evolution, 1985. Cambridge University Press: Cambridge.
11.Kramer, MS, Joseph, KS. Enigma of fetal/infant-origins hypothesis. Lancet. 1996; 348, 12541255.
12.Huxley, R, Neil, A, Collins, R. Unravelling the fetal origins hypothesis: is there really an inverse association between birthweight and subsequent blood pressure? Lancet. 2002; 360, 659665.
13.Hopwood, N. Embryology. In The Cambridge History of Science, vol 6: the Modern Biological and Earth Sciences (eds. Bowler PJ, Pickstone JV), 2009; pp. 285315. Cambridge University Press, Cambridge.
14.Richards, E. A political anatomy of monsters, hopeful and otherwise: teratogeny, transcendentalism, and evolutionary theorizing. Isis. 1994; 85, 377411.
15.Oppenheimer, JM. Some historical relationships between teratology and experimental embryology. Bull Hist Med. 1968; 42, 145159.
16.Gliboff, S. “Protoplasm…is soft wax in our hands”: Paul Kammerer and the art of biological transformation. Endeavour. 2005; 29, 162167.
17.Vargas, AO. Did Paul Kammerer discover epigenetic inheritance? a modern look at the controversial midwife toad experiments. J Exp Zool (Mol Dev Evo). 2009; 312B, 667678.
18.Roll-Hansen, N. The Lysenko Effect: The Politics of Science, 2005. Humanity Books: Amherst, NJ.
19.Kermack, W, McKendrick, A, McKinlay, P. Death rates in Great Britain and Sweden: some general regularities and their significance. Lancet. 1934; 223, 698703.
20.Dörner, G. Die mögliche Bedeutung der prä- und/oder perinatalen Ernährung für die Pathogenese der Obesitas. Acta Biol Med Ger. 1973; 30, 1922.
21.Dörner, G, Götz, F. Hyperglikämie und Übergewicht in neonatal insulinbehandelten erwachsenen Rättenmänchen. Acta Biol Med Ger. 1972; 29, 467470.
22.Dörner, G, Haller, K, Leonhardt, M. Zur möglichen Bedeutung der prä- und/oder früh postnatalen Ernährung für die Pathogenese der Arterioskleroze. Acta Biol Med Ger. 1973; 31, 3135.
23.Dörner, G, Mohnike, A. Zur möglichen Bedeutung der prä- und/oder frühpostnatalen Ernährung für die Pathogenese der Diabetes Mellitus. Acta Biol Med Ger. 1973; 31, 710.
24.Dörner, G, Rodekamp, E, Plagemann, A. Maternal deprivation and overnutrition in early postnatal life and their primary prevention: historical reminiscence of an “ecological” experiment in Germany. Hum ontogenet. 2008; 2, 5159.
25.Lucas, A. Programming by early nutrition in man. (discussion 50-55) Ciba Found Symp. 1991; 156, 3850.
26.Dörner, G. Günter Dörner, endocrinologist. Hum Ontogenet. 2008; 2, 59.
27.Freinkel, N. Banting lecture 1980. Of pregnancy and progeny. Diabetes. 1980; 29, 10231035.
28.De Prins, FA, Van Assche, FA. Intrauterine growth retardation and development of endocrine pancreas in the experimental rat. Biologia Neonatorum. 1982; 41, 1621.
29.Aerts, L, Van Assche, FA. Is gestational diabetes an acquired condition? J Dev Physiol. 1979; 1, 219225.
30.Forsdahl, A. Are poor living conditions in childhood and adolescence an important risk factor for arteriosclerotic heart disease? Br J Prevent Soc Med. 1977; 31, 9195.
31.Wadsworth, ME, Cripps, HA, Midwinter, RE, Colley, JR. Blood pressure in a national birth cohort at the age of 36 related to social and familial factors, smoking, and body mass. Br Med J (Clin Res Ed). 1985; 291, 15341538.
32.Notkola, V, Punsar, S, Karvonen, MJ, Haapakoski, J. Socio-economic conditions in childhood and mortality and morbidity caused by coronary heart disease in adulthood in rural Finland. Soc Sci Med. 1985; 21, 517523.
33.Barker, DJ, Osmond, C. Infant mortality, childhood nutrition, and ischaemic heart disease in England and Wales. Lancet. 1986; 1, 10771081.
34.Gennser, G, Rymark, P, Isberg, PE. Low birth weight and risk of high blood pressure in adulthood. Br Med J (Clin Res Ed). 1988; 296, 14981500.
35.Pettitt, DJ, Aleck, KA, Baird, HR, Carraher, MJ, Bennett, PH, Knowler, WC. Congenital susceptibility to NIDDM. Role of intrauterine environment. Diabetes. 1988; 37, 622628.
36.Godfrey, K. The ‘developmental origins’ hypothesis: epidemiology. In Developmental Origins of Health and Disease (eds. Gluckman PD, Hanson MA), 2006; pp. 632. Cambridge University Press, Cambridge.
37.Cooper, C, Walker-Bone, K, Arden, N, Dennison, E. Novel insights into the pathogenesis of osteoporosis: the role of intrauterine programming. Rheumatology. 2000; 39, 13121315.
38.Gale, CR, Martyn, CN. Birth weight and later risk of depression in a national birth cohort. Br J Psychiatry. 2004; 184, 2833.
39.Wahlbeck, K, Forsen, T, Osmond, C, Barker, DJP, Eriksson, JG. Association of schizophrenia with low maternal body mass index, small size at birth, and thinness during childhood. Arch Gen Psych. 2001; 58, 4852.
40.Barker, DJ, Godfrey, KM, Fall, C, et al. Relation of birth weight and childhood respiratory infection to adult lung function and death from chronic obstructive airways disease. Br Med J. 1991; 303, 671675.
41.Ahlgren, M, Melbye, M, Wohlfahrt, J, Sorensen, TIA. Growth patterns and the risk of breast cancer in women. New Engl J Med. 2004; 351, 16191626.
42.Jefferis, BJMH, Power, C, Hertzman, C. Birth weight, childhood socioeconomic environment, and cognitive development in the 1958 British birth cohort study. Br Med J. 2002; 325, 305311.
43.Harding, JE. The nutritional basis of the fetal origins of adult disease. Int J Epidemiol. 2001; 30, 1523.
44.McMullen, S, Mostyn, A. Animal models for the study of the developmental origins of health and disease. Proc Nutr Soc. 2009; 68, 306320.
45.Mayr, E. Cause and effect in biology. Science. 1961; 134, 15011506.
46.Cohen, MN, Armelagos, GJ (eds) Paleopathology at the Origins of Agriculture. Academic Press: Orlando, 1984.
47.Neel, JV. Diabetes mellitus: a “thrifty” genotype rendered detrimental by “progress”? Am J Hum Genet. 1962; 14, 353362.
48.Kuzawa, CW, Gluckman, PD, Hanson, MA, Fantuzzi, G, Mazzone, T. Developmental perspectives on the origin of obesity. In Adipose Tissue and Adipokines in Health and Disease (eds. Fantuzzi G, Mazzone T), 2007; pp. 207219. Humana Press: Totowa, NJ.
49.Hales, CN, Barker, DJ. Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia. 1992; 35, 595601.
50.Denver, R, Mirhadi, N, Phillips, M. Adaptive plasticity in amphibian metamorphosis: response of Scaphiopus hammondii tadpoles to habitat desiccation. Ecology. 1998; 79, 18591872.
51.Reusens, B, Remacle, C. Programming of impaired insulin secretion versus sensitivity: cause or effect?. In Early Nutrition Programming and Health Outcomes in Later Life: Obesity and Beyond (eds. Koletzko B, Decsi T, Molnar D, de La Hunty A), 2009; pp. 125131. Springer, Netherlands, Dordrecht.
52.Dawes, GS, Borruto, F, Zacutti, A (eds) Fetal Autonomy and Adaptation, 1990. Wiley: Chichester.
53.Bateson, P. Fetal experience and good adult design. Int J Epidemiol. 2001; 30, 928934.
54.Gluckman, PD, Hanson, MA. Living with the past: evolution, development, and patterns of disease. Science. 2004; 305, 17331736.
55.Bateson, P, Barker, D, Clutton-Brock, T, et al. Developmental plasticity and human health. Nature. 2004; 430, 419421.
56.Gluckman, PD, Hanson, MA, Spencer, HG, Bateson, P. Environmental influences during development and their later consequences for health and disease: implications for the interpretation of empirical studies. Proc Royal Soc Lond B. 2005; 272, 671677.
57.Gluckman, PD, Hanson, MA, Spencer, HG. Predictive adaptive responses and human evolution. Trends Ecol Evol. 2005; 20, 527533.
58.Gluckman, PD, Hanson, MA, Beedle, AS. Early life events and their consequences for later disease: a life history and evolutionary perspective. Am J Hum Biol. 2007; 19, 119.
59.Applebaum, SW, Heifetz, Y. Density-dependent physiological phase in insects. Annu Rev Entomol. 1999; 44, 317341.
60.Desai, M, Gayle, D, Babu, J, Ross, MG. Programmed obesity in intrauterine growth restricted newborns: modulation by newborn nutrition. Am J Physiol. 2005; 288, R91R96.
61.Sloboda, DM, Howie, GJ, Vickers, MH. Early-onset puberty in offspring after maternal undernutrition is exaggerated by a post-weaning high fat diet: sex specific evidence of nutritional mismatch. Early Hum Dev. 2007; 83(Suppl 1), S65S66.
62.Mitchell, A, Romano, GH, Groisman, B, et al. Adaptive prediction of environmental changes by microorganisms. Nature. 2009; 460, 220224.
63.Jablonka, E, Oborny, B, Molnar, I, et al. The adaptive advantage of phenotypic memory in changing environments. Philos Trans R Soc Lond B Biol Sci. 1995; 350, 133141.
64.Moran, NA. The evolutionary maintenance of alternative phenotypes. Am Nat. 1992; 139, 971989.
65.Gluckman, PD, Hanson, MA. The Fetal Matrix: Evolution, Development, and Disease, 2005. Cambridge University Press: Cambridge.
66.Kuzawa, CW. Fetal origins of developmental plasticity: are fetal cues reliable predictors of future nutritional environments? Am J Hum Biol. 2005; 17, 521.
67.Bloomfield, FH, Oliver, MH, Hawkins, P, et al. A periconceptional nutritional origin for non-infectious preterm birth. Science. 2003; 300, 606.
68.Ronnenberg, AG, Wang, X, Xing, H, et al. Low preconception body mass index is associated with birth outcome in a prospective cohort of Chinese women. J Nutr. 2003; 133, 34493455.
69.Boyne, MS, Thame, M, Bennett, FI, et al. The relationship among circulating insulin-like growth factor (IGF-1), IGF-binding proteins-1 and -2, and birth anthropometry: a prospective study. J Clin Endocrinol Metab. 2003; 88, 16871691.
70.Wells, JCK. The thrifty phenotype as an adaptive maternal effect. Biol Rev Camb Philos Soc. 2007; 82, 143172.
71.Smith, CA. Effects of maternal undernutrition upon the newborn infant in Holland (1944–45). J Pediatr. 1947; 30, 229243.
72.Painter, RC, Roseboom, TJ, Bleker, OP. Prenatal exposure to the Dutch famine and disease in later life: an overview. Reprod Toxicol. 2005; 20, 345352.
73.MacLaughlin, SM, Walker, SK, Roberts, CT, Kleemann, DO, McMillen, IC. Periconceptional nutrition and the relationship between maternal body weight changes in the periconceptional period and feto-placental growth in the sheep. J Physiol. 2005; 565, 111124.
74.Sloboda, DM, Hart, R, Doherty, DA, Pennell, CE, Hickey, M. Age at menarche: influences of prenatal and postnatal growth. J Clin Endocrinol Metab. 2007; 92, 4650.
75.Gale, CR, Jiang, B, Robinson, SM, et al. Maternal diet during pregnancy and carotid intima-media thickness in children. Arterioscler Thromb Vasc Biol. 2006; 26, 18771882.
76.Gluckman, PD, Hanson, MA. Mismatch: Why our World no Longer fits our Bodies, 2006. Oxford University Press: Oxford.
77.Gluckman, PD, Hanson, MA. Maternal constraint of fetal growth and its consequences. Semin Fetal Neonatal Med. 2004; 9, 419425.
78.Sultan, SE, Spencer, HG. Metapopulation structure favors plasticity over local adaptation. Am Nat. 2002; 160, 271283.
79.Cordain, L, Eaton, SB, Sebastian, A, et al. Origins and evolution of the Western diet: health implications for the 21st century. Am J Clin Nutr. 2005; 81, 341354.
80.Norman, JF, LeVeen, RF. Maternal atherogenic diet in swine is protective against early atherosclerosis development in offspring consuming an atherogeneic diet post-natally. Atherosclerosis. 2001; 157, 4147.
81.Forsen, T, Eriksson, J, Tuomilehto, J, et al. The fetal and childhood growth of persons who develop type 2 diabetes. Ann Intern Med. 2000; 133, 176182.
82.Gluckman, PD, Hanson, MA, Beedle, AS, Raubenheimer, D. Fetal and neonatal pathways to obesity. Front Horm Res. 2008; 36, 6172.
83.Pettitt, DJ, Lawrence, JM, Beyer, J, et al. Association between maternal diabetes in utero and age at offspring’s diagnosis of type 2 diabetes. Diabetes Care. 2008; 31, 21262130.
84.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, 323335.
85.Stettler, N, Tershakovec, AM, Zemel, BS, et al. Early risk factors for increased adiposity: a cohort study of African American subjects followed from birth to young adulthood. Am J Clin Nutr. 2000; 72, 378383.
86.Lawlor, DA, Timpson, NJ, Harbord, RM, et al. Exploring the developmental overnutrition hypothesis using parental-offspring associations and FTO as an instrumental variable. PLoS Med. 2008; 5, 04840493.
87.Sloboda, DM, Howie, GJ, Pleasants, A, Gluckman, PD, Vickers, MH. Pre- and postnatal nutritional histories influence reproductive maturation and ovarian function in the rat. PLoS One. 2009; 4, 18.
88.Hanson, M, Fall, C, Robinson, S, Baird, J. Early Life Nutrition and Lifelong Health, 2009. British Medical Association: London.
89.Meaney, MJ. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu Rev Neurosci. 2001; 24, 11611192.
90.Ross, MG, Desai, M, Guerra, C, Wang, S. Prenatal programming of hypernatremia and hypertension in neonatal lambs. Am J Physiol. 2005; 288, R25R33.
91.Diamond, J. Pearl Harbor and the Emperor’s physiologists. Nat Hist. 1991, 27.
92.Gluckman, PD, Hanson, MA, Cooper, C, Thornburg, KL. Effect of in utero and early-life conditions on adult health and disease. New Engl J Med. 2008; 359, 6173.
93.Bertram, C, Trowern, AR, Copin, N, Jackson, AA, Whorwood, CB. The maternal diet during pregnancy programs altered expression of the glucocorticoid receptor and type 2 11beta-hydroxysteroid dehydrogenase: potential molecular mechanisms underlying the programming of hypertension in utero. Endocrinology. 2001; 142, 28412853.
94.Reik, W. Stability and flexibility of epigenetic gene regulation in mammalian development. Nature. 2007; 447, 425432.
95.Lillycrop, KA, Phillips, ES, Jackson, AA, Hanson, MA, Burdge, GC. Dietary protein restriction of pregnant rats induces and folic acid supplementation prevents epigenetic modification of hepatic gene expression in the offspring. J Nutr. 2005; 135, 13821386.
96.Lillycrop, KA, Slater-Jefferies, JL, Hanson, MA, et al. Induction of altered epigenetic regulation of the hepatic glucocorticoid receptor in the offspring of rats fed a protein-restricted diet during pregnancy suggests that reduced DNA methyltransferase-1 expression is involved in impaired DNA methylation and changes in histone modifications. Br J Nutr. 2007; 97, 10641073.
97.Park, JH, Stoffers, DA, Nicholls, RD, Simmons, RA. Development of type 2 diabetes following intrauterine growth retardation in rats is associated with progressive epigenetic silencing of Pdx1. J Clin Invest. 2008; 118, 23162324.
98.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, 91102.
99.Sinclair, KD, Allegrucci, C, Singh, R, et al. DNA methylation, insulin resistance, and blood pressure in offspring determined by maternal periconceptional B vitamin and methionine status. Proc Natl Acad Sci USA. 2007; 104, 1935119356.
100.Tobi, EW, Lumey, LH, Talens, RP, et al. DNA Methylation differences after exposure to prenatal famine are common and timing- and sex-specific. Hum Mol Genet. 2009; 18, 40464053.
101.Amaral, PP, Dinger, ME, Mercer, TR, Mattick, JS. The eukaryotic genome as an RNA machine. Science. 2008; 319, 17871789.
102.Vickers, MH, Gluckman, PD, Coveny, AH, et al. Neonatal leptin treatment reverses developmental programming. Endocrinology. 2005; 146, 42114216.
103.Gluckman, PD, Lillycrop, KA, Vickers, MH, et al. Metabolic plasticity during mammalian development is directionally dependent on early nutritional status. Proc Natl Acad Sci USA. 2007; 104, 1279612800.
104.Bouret, SG, Simerly, RB. Leptin and development of hypothalamic feeding circuits. Endocrinology. 2004; 145, 26212626.
105.Delahaye, F, Breton, C, Risold, PY, et al. Maternal perinatal undernutrition drastically reduces postnatal leptin surge and affects the development of arcuate nucleus proopiomelanocortin neurons in neonatal male rat pups. Endocrinology. 2008; 149, 470475.
106.Morioka, T, Asilmaz, E, Hu, J, et al. Disruption of leptin receptor expression in the pancreas directly affects beta cell growth and function in mice. J Clin Invest. 2007; 117, 28602868.
107.Elinav, E, Niv-Spector, L, Price, TO, et al. Pegylated leptin antagonist is a potent orexigenic agent: preparation and mechanism of activity. Endocrinology. 2009; 150, 30833091.
108.Stoffers, DA, Desai, BM, DeLeon, DD, Simmons, RA. Neonatal exendin-4 prevents the development of diabetes in the intrauterine growth retarded rat. Diabetes. 2003; 52, 734740.
109.Wyrwoll, CS, Mark, PJ, Mori, TA, Puddey, IB, Waddell, BJ. Prevention of programmed hyperleptinemia and hypertension by postnatal dietary omega-3 fatty acids. Endocrinology. 2006; 147, 599606.
110.Whincup, PH, Gilg, JA, Papacosta, O, et al. Early evidence of ethnic differences in cardiovascular risk: cross sectional comparison of British South Asian and white children. Br Med J. 2002; 324, 16.
111.Yajnik, CS, Fall, CHD, Coyaji, KJ, et al. Neonatal anthropometry: the thin-fat Indian baby. The Pune maternal nutrition study. Int J Obes. 2003; 27, 173180.
112.Jahoor, F, Badaloo, A, Reid, M, et al. Unique metabolic characteristics of the major syndromes of severe childhood malnutrition. In The Tropical Metabolism Research Unit, The University of the West Indies, Jamaica 1956–2006: The House that John Built (eds. Forrester T, Picou D, Walker S), 2007; pp. 2360. Ian Randle Publishers, Kingston.
113.Godfrey, KM, Gluckman, PD, Lillycrop, KA, et al. Epigenetic marks at birth predict childhood body composition at age 9 years. Abstract O-8A-72 presented at the 6th World Congress of Developmental Origins of Health and Disease, Santiago de Chile, November 2009. J DOHaD. 2009; 1(Suppl. 1), S44.
114.Jablonka, E, Raz, G. Transgenerational epigenetic inheritance: prevalence, mechanisms, and implications for the study of heredity and evolution. Q Rev Biol. 2009; 84, 131176.
115.Burdge, GC, Hanson, MA, Slater-Jeffries, JL, Lillycrop, KA. Epigenetic regulation of transcription: a mechanism for inducing variations in phenotype (fetal programming) by differences in nutrition during early life? Br J Nutr. 2007; 97, 10361046.
116.Gluckman, PD, Hanson, MA, Beedle, AS. Non-genomic transgenerational inheritance of disease risk. Bioessays. 2007; 29, 149154.
117.Waterland, RA, Travisano, M, Tahiliani, KG, Rached, MT, Mirza, S. Methyl donor supplementation prevents transgenerational amplification of obesity. Int J Obes. 2008; 32, 13731379.
118.Arpanahi, A, Brinkworth, M, Iles, D, et al. Endonuclease-sensitive regions of human spermatozoal chromatin are highly enriched in promoter and CTCF binding sequences. Gen Res. 2009; 19, 13381349.
119.Anway, MD, Cupp, AS, Uzumcu, M, Skinner, MK. Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science. 2005; 308, 14661469.
120.Rassoulzadegan, M, Grandjean, V, Gounon, P, et al. RNA-mediated non-Mendelian inheritance of an epigenetic change in the mouse. Nature. 2006; 441, 469474.
121.Ibáñez, L, Potau, N, Enriquez, G, Marcos, MV, DeZegher, F. Hypergonadotrophinaemia with reduced uterine and ovarian size in women born small-for-gestational-age. Hum Reprod. 2003; 18, 15651569.
122.Bossdorf, O, Richards, CL, Pigliucci, M. Epigenetics for ecologists. Ecol Lett. 2008; 11, 106115.
123.O’Flaherty, M, Ford, E, Allender, S, Scarborough, P, Capewell, S. Coronary heart disease trends in England and Wales from 1984 to 2004: concealed levelling of mortality rates among young adults. Heart. 2008; 94, 178181.
124.WHO. Preventing Chronic Diseases: a Vital Investment. 2005. World Health Organization: Geneva.
125.Zhang, XL, Shu, XO, Yang, G, et al. Abdominal adiposity and mortality in Chinese women. Arch Int Med. 2007; 167, 886892.
126.Gluckman, PD, Beedle, AS, Hanson, MA, Yap, EP. Developmental perspectives on individual variation: implications for understanding nutritional needs. In Personalized Nutrition for the Diverse Needs of Infants and Children (eds. Bier DM, German JB, Lonnerdal B), 2008; pp. 112. Karger, Basel.
127.Fall, CH, Stein, CE, Kumaran, K, et al. Size at birth, maternal weight, and type 2 diabetes in South India. Diabet Med. 1998; 15, 220227.
128.Wong, L, Tan, ASA. The glucose challenge test for screening gestational diabetes in pregnant women with no risk factors. Singapore Med J. 2001; 42, 517521.
129.Seshiah, V, Balaji, V, Balaji, MS, Sanjeevi, CB, Green, A. Gestational diabetes mellitus in India. J Assoc Physicians India. 2004; 52, 707711.
130.Moore, SE, Cole, TJ, Collinson, AC, et al. Prenatal or early postnatal events predict infectious deaths in young adulthood in rural Africa. Int J Epidemiol. 1999; 28, 10881095.
131.Gluckman, PD, Hanson, MA, Bateson, P, et al. Towards a new developmental synthesis: adaptive developmental plasticity and human disease. Lancet. 2009; 373, 16541657.
132.Alderman, H, Behrman, JR. Estimated Economic Benefits of Reducing low Birth Weight in low-income Countries. Health, Nutrition and Population (HNP) Discussion Paper of the World Bank’s Human Development Network. 2004. World Bank: Washington, DC.
133.O’Connor, KC, Morton, SMB, Gluckman, PD. Modelling the economic antecedents and costs of low birth weight: multidimensional challenges in the international poor start to life project. Early Hum Dev. 2007; 83(Suppl 1), S39.
134.Butland, B, Jebb, S, Kopelman, P, et al. Tackling Obesities: Future Choices (Foresight Project Report), 2008. Government Office for Science: London.

Keywords

Related content

Powered by UNSILO

A conceptual framework for the developmental origins of health and disease

  • P. D. Gluckman (a1) (a2), M. A. Hanson (a3) and T. Buklijas (a1)

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed.