Skip to main content

Prenatal Undernutrition and Ageing and Longevity

  • Chapter
  • First Online:
Early Life Origins of Ageing and Longevity

Part of the book series: Healthy Ageing and Longevity ((HAL,volume 9))

  • 635 Accesses

Abstract

Dietary restriction is one of the most extensively studied ways to elongate lifespan, but when species are undernourished before birth, effects are completely opposite. In the present chapter, evidence from animal experimental as well as from human studies is presented demonstrating that prenatal undernutrition increases the risk for ageing-associated diseases of the brain and the body, seems to accelerate the ageing process and decrease lifespan. The findings presented here are of importance from a public health perspective as prenatal nutrition may be a modifiable factor affecting healthy ageing. Also, understanding the processes by which prenatal undernutrition leads to accelerated ageing may provide clues on how we can detect early ageing and implement interventional approaches when conditions are still reversible.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 159.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Amer MG, Mohamed NM, Shaalan AAM (2017) Gestational protein restriction: study of the probable effects on cardiac muscle structure and function in adult rats. Histol Histopathol 32(12):1293–1303

    CAS  PubMed  Google Scholar 

  • Antonow-Schlorke I, Schwab M, Cox LA, Li C, Stuchlik K, Witte OW, Nathanielsz PW, McDonald TJ (2011) Vulnerability of the fetal primate brain to moderate reduction in maternal global nutrient availability. Proc Natl Acad Sci USA 108(7):3011–3016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Balota DA, Tse CS, Hutchison KA, Spieler DH, Duchek JM, Morris JC (2010) Predicting conversion to dementia of the Alzheimer’s type in a healthy control sample: the power of errors in Stroop color naming. Psychol Aging 25(1):208–218

    Article  PubMed  PubMed Central  Google Scholar 

  • Barreto RR, Franco Ede S, Brasileiro CF, de Oliveira AP, Dimech GS, Malta DJ, Cazuzu JS, Leite AC, da Silva TG, Maia MB (2012) Early undernutrition is associated with attenuated inflammatory response and alteration in pharmacological efficacy of indomethacin in rats. Eur J Pharm Sci Off J Eur Fed Pharm Sci 46(1–2):56–63

    Article  CAS  PubMed  Google Scholar 

  • Beauchamp B, Thrush AB, Quizi J, Antoun G, McIntosh N, Al-Dirbashi OY, Patti ME, Harper ME (2015) Undernutrition during pregnancy in mice leads to dysfunctional cardiac muscle respiration in adult offspring. Biosci Rep 35(3)

    Google Scholar 

  • Berney DM, Desai M, Palmer DJ, Greenwald S, Brown A, Hales CN, Berry CL (1997) The effects of maternal protein deprivation on the fetal rat pancreas: major structural changes and their recuperation. J Pathol 183(1):109–115

    Article  CAS  PubMed  Google Scholar 

  • Bhat NR (2010) Linking cardiometabolic disorders to sporadic Alzheimer’s disease: a perspective on potential mechanisms and mediators. J Neurochem 115(3):551–562

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bleker LS, de Rooij SR, Painter RC, van der Velde N, Roseboom TJ (2016) Prenatal undernutrition and physical function and frailty at the age of 68 years: the Dutch Famine Birth Cohort Study. J Gerontol Ser A Biol Sci Med Sci 71(10):1306–1314

    Article  Google Scholar 

  • Bots ML, Hoes AW, Koudstaal PJ, Hofman A, Grobbee DE (1997) Common carotid intima-media thickness and risk of stroke and myocardial infarction: the Rotterdam Study. Circulation 96(5):1432–1437

    Article  CAS  PubMed  Google Scholar 

  • Calado RT, Young NS (2009) Telomere diseases. N Engl J Med 361(24):2353–2365

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen H, Nembhard WN, Stockwell HG (2014) Sex-specific effects of fetal exposure to the 1959–1961 Chinese famine on risk of adult hypertension. Matern Child Health J 18(3):527–533

    Article  PubMed  Google Scholar 

  • Chung HY, Cesari M, Anton S, Marzetti E, Giovannini S, Seo AY, Carter C, Yu BP, Leeuwenburgh C (2009) Molecular inflammation: underpinnings of aging and age-related diseases. Ageing Res Rev 8(1):18–30

    Article  CAS  PubMed  Google Scholar 

  • Cooper R, Kuh D, Hardy R (2010) Objectively measured physical capability levels and mortality: systematic review and meta-analysis. BMJ (Clinical Research ed) 341:c4467

    Article  Google Scholar 

  • Cooper R, Kuh D, Cooper C, Gale CR, Lawlor DA, Matthews F, Hardy R (2011) Objective measures of physical capability and subsequent health: a systematic review. Age Ageing 40(1):14–23

    Article  PubMed  Google Scholar 

  • de Groot RH, Stein AD, Jolles J, van Boxtel MP, Blauw GJ, van de Bor M, Lumey L (2011) Prenatal famine exposure and cognition at age 59 years. Int J Epidemiol 40(2):327–337

    Article  PubMed  PubMed Central  Google Scholar 

  • de Oliveira Assis T, da Silva TG, de Souza Franco E, Rezende Leite AC, de Moraes SR, de Sousa Maia MB (2011) Impact of early malnourishment on the chronic inflammatory response and its implications for the effect of indomethacin on Wistar rats. Br J Nutr 106(6):845–851

    Article  CAS  Google Scholar 

  • de Rooij SR (2018) Invited commentary: a matter of survival-the detrimental consequences of adverse early-life conditions. Am J Epidemiol 187(10):2093–2094

    Article  PubMed  Google Scholar 

  • de Rooij SR, Painter RC, Phillips DI, Osmond C, Michels RP, Godsland IF, Bossuyt PM, Bleker OP, Roseboom TJ (2006) Impaired insulin secretion after prenatal exposure to the Dutch famine. Diabetes Care 29(8):1897–1901

    Article  PubMed  Google Scholar 

  • de Rooij SR, Wouters H, Yonker JE, Painter RC, Roseboom TJ (2010) Prenatal undernutrition and cognitive function in late adulthood. Proc Natl Acad Sci USA 107(39):16881–16886

    Article  PubMed  PubMed Central  Google Scholar 

  • de Rooij SR, Roseboom TJ, Painter RC (2014) Famines in the last 100 years: implications for diabetes. Curr DiabRep 14(10):536

    Article  Google Scholar 

  • de Rooij SR, van Pelt AM, Ozanne SE, Korver CM, van Daalen SK, Painter RC, Schwab M, Viegas MH, Roseboom TJ (2015) Prenatal undernutrition and leukocyte telomere length in late adulthood: the Dutch famine birth cohort study. Am J Clin Nutr 102(3):655–660

    Article  PubMed  CAS  Google Scholar 

  • de Rooij SR, Caan MW, Swaab DF, Nederveen AJ, Majoie CB, Schwab M, Painter RC, Roseboom TJ (2016) Prenatal famine exposure has sex-specific effects on brain size. Brain J Neurol 139(Pt 8):2136–2142

    Article  Google Scholar 

  • Desai M, Gayle DA, Casillas E, Boles J, Ross MG (2009) Early undernutrition attenuates the inflammatory response in adult rat offspring. J Matern-Fetal Neonatal Med Off J Eur Assoc Perinat Med Fed Asia Ocean Perinat Soc Int Soc Perinat Obstet 22(7):571–575

    CAS  Google Scholar 

  • Diaz-Cintra S, Garcia-Ruiz M, Corkidi G, Cintra L (1994) Effects of prenatal malnutrition and postnatal nutritional rehabilitation on CA3 hippocampal pyramidal cells in rats of four ages. Brain Res 662(1–2):117–126

    Article  CAS  PubMed  Google Scholar 

  • Dlouha D, Maluskova J, Kralova Lesna I, Lanska V, Hubacek JA (2017) Comparison of the relative telomere length measured in leukocytes and eleven different human tissues. Physiol Res 63 Suppl 3:S343–350

    Google Scholar 

  • Doblhammer G, van den Berg GJ, Lumey LH (2013) A re-analysis of the long-term effects on life expectancy of the Great Finnish Famine of 1866–68. Popul Stud 67(3):309–322

    Article  Google Scholar 

  • Donovan EL, Hernandez CE, Matthews LR, Oliver MH, Jaquiery AL, Bloomfield FH, Harding JE (2013) Periconceptional undernutrition in sheep leads to decreased locomotor activity in a natural environment. J Dev Orig Health Dis 4(4):296–299

    Article  CAS  PubMed  Google Scholar 

  • Duran P, Cintra L, Galler JR, Tonkiss J (2005) Prenatal protein malnutrition induces a phase shift advance of the spontaneous locomotor rhythm and alters the rest/activity ratio in adult rats. Nutr Neurosci 8(3):167–172

    Article  CAS  PubMed  Google Scholar 

  • Ekamper P, van Poppel F, Stein AD, Lumey LH (1982) Independent and additive association of prenatal famine exposure and intermediary life conditions with adult mortality between age 18–63 years. Soc Sci Med 119(2014):232–239

    Google Scholar 

  • Ekamper P, van Poppel F, Stein AD, Bijwaard GE, Lumey LH (2015) Prenatal famine exposure and adult mortality from cancer, cardiovascular disease, and other causes through age 63 years. Am J Epidemiol 181(4):271–279

    Article  PubMed  PubMed Central  Google Scholar 

  • Finer S, Iqbal MS, Lowe R, Ogunkolade BW, Pervin S, Mathews C, Smart M, Alam DS, Hitman GA (2016) Is famine exposure during developmental life in rural Bangladesh associated with a metabolic and epigenetic signature in young adulthood? A historical cohort study. BMJ Open 6(11):e011768

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Finkel T, Holbrook NJ (2000) Oxidants, oxidative stress and the biology of ageing. Nature 408(6809):239–247

    Article  CAS  PubMed  Google Scholar 

  • Franke K, Ziegler G, Kloppel S, Gaser C (2010) Estimating the age of healthy subjects from T1-weighted MRI scans using kernel methods: exploring the influence of various parameters. NeuroImage 50(3):883–892

    Article  PubMed  Google Scholar 

  • Franke K, Clarke GD, Dahnke R, Gaser C, Kuo AH, Li C, Schwab M, Nathanielsz PW (2017) Premature brain aging in baboons resulting from moderate fetal undernutrition. Front Aging Neurosci 9:92

    Article  PubMed  PubMed Central  Google Scholar 

  • Franke K, Gaser C, Roseboom TJ, Schwab M, de Rooij SR (2018) Premature brain aging in humans exposed to maternal nutrient restriction during early gestation. NeuroImage 173:460–471

    Article  PubMed  Google Scholar 

  • Gould JM, Smith PJ, Airey CJ, Mort EJ, Airey LE, Warricker FDM, Pearson-Farr JE, Weston EC, Gould PJW, Semmence OG, Restall KL, Watts JA, McHugh PC, Smith SJ, Dewing JM, Fleming TP, Willaime-Morawek S (2018) Mouse maternal protein restriction during preimplantation alone permanently alters brain neuron proportion and adult short-term memory. Proc Natl Acad Sci USA 115(31):E7398–e7407

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gutierrez-Arzapalo PY, Rodriguez-Rodriguez P, Ramiro-Cortijo D, Lopez de Pablo AL, Lopez-Gimenez MR, Condezo-Hoyos L, Greenwald SE, Gonzalez MDC, Arribas SM (2017) Role of fetal nutrient restriction and postnatal catch-up growth on structural and mechanical alterations of rat aorta. J Physiol

    Google Scholar 

  • Hales CN, Barker DJ (2001) The thrifty phenotype hypothesis. Br Med Bull 60:5–20

    Article  CAS  PubMed  Google Scholar 

  • Hanson HA, Smith KR (2013) Early origins of longevity: prenatal exposures to food shortage among early Utah pioneers. J Dev Orig Health Dis 4(2):170–181

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He P, Liu L, Salas JMI, Guo C, Cheng Y, Chen G, Zheng X (2018) Prenatal malnutrition and adult cognitive impairment: a natural experiment from the 1959–1961 Chinese famine. Br J Nutr 120(2):198–203

    Article  CAS  PubMed  Google Scholar 

  • Heijmans BT, Tobi EW, Stein AD, Putter H, Blauw GJ, Susser ES, Slagboom PE, Lumey LH (2008) Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc Natl Acad Sci USA 105(44):17046–17049

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hirani V, Blyth F, Naganathan V, Le Couteur DG, Seibel MJ, Waite LM, Handelsman DJ, Cumming RG (2015) Sarcopenia is associated with incident disability, institutionalization, and mortality in community-dwelling older men: the concord health and ageing in men project. J Am Med Dir Assoc 16(7):607–613

    Article  PubMed  Google Scholar 

  • Hult M, Tornhammar P, Ueda P, Chima C, Bonamy AK, Ozumba B, Norman M (2010) Hypertension, diabetes and overweight: looming legacies of the Biafran famine. PLoS ONE 5(10):e13582

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Inskip HM, Crozier SR, Godfrey KM, Borland SE, Cooper C, Robinson SM (2009) Women’s compliance with nutrition and lifestyle recommendations before pregnancy: general population cohort study. BMJ (Clinical research ed.) 338:b481

    Article  Google Scholar 

  • Jennings BJ, Ozanne SE, Dorling MW, Hales CN (1999) Early growth determines longevity in male rats and may be related to telomere shortening in the kidney. FEBS Lett 448(1):4–8

    Article  CAS  PubMed  Google Scholar 

  • Kang Y, Zhang Y, Feng Z, Liu M, Li Y, Yang H, Wang D, Zheng L, Lou D, Cheng L, Chen C, Zhou W, Feng Y, Li X, Duan J, Yu M, Yang S, Liu Y, Wang X, Deng B, Liu C, Yao X, Zhu C, Liang C, Zeng X, Ren S, Li Q, Zhong Y, Zhang Y, Kang J, Yan Y, Meng H, Zhong Z, Zhou W, Wang Y, Li T, Song W (2017) Nutritional deficiency in early life facilitates aging-associated cognitive decline. Curr Alzheimer Res 14(8):841–849

    Article  CAS  PubMed  Google Scholar 

  • Kannisto V, Christensen K, Vaupel JW (1997) No increased mortality in later life for cohorts born during famine. Am J Epidemiol 145(11):987–994

    Article  CAS  PubMed  Google Scholar 

  • Kones R, Rumana U (2017) Cardiometabolic diseases of civilization: history and maturation of an evolving global threat. An update and call to action. Ann Med 49(3):260–274

    Article  PubMed  Google Scholar 

  • Li Y, He Y, Qi L, Jaddoe VW, Feskens EJ, Yang X, Ma G, Hu FB (2010) Exposure to the Chinese famine in early life and the risk of hyperglycemia and type 2 diabetes in adulthood. Diabetes 59(10):2400–2406

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Y, Jaddoe VW, Qi L, He Y, Lai J, Wang J, Zhang J, Hu Y, Ding EL, Yang X, Hu FB, Ma G (2011) Exposure to the Chinese famine in early life and the risk of hypertension in adulthood. J Hypertens 29(6):1085–1092

    Article  CAS  PubMed  Google Scholar 

  • Li J, Na L, Ma H, Zhang Z, Li T, Lin L, Li Q, Sun C, Li Y (2015) Multigenerational effects of parental prenatal exposure to famine on adult offspring cognitive function. Sci Rep 5:13792

    Article  PubMed  PubMed Central  Google Scholar 

  • Lindeboom M, Portrait F, van den Berg GJ (2010) Long-run effects on longevity of a nutritional shock early in life: the Dutch Potato famine of 1846–1847. J Health Econ 29(5):617–629

    Article  PubMed  Google Scholar 

  • Liu L, Pang ZC, Sun JP, Xue B, Wang SJ, Ning F, Qiao Q (2017) Exposure to famine in early life and the risk of obesity in adulthood in Qingdao: evidence from the 1959–1961 Chinese famine. Nutr Metab Cardiovasc Dis: NMCD 27(2):154–160

    Article  PubMed  Google Scholar 

  • Lumey LH, Stein AD, Kahn HS, Romijn JA (2009) Lipid profiles in middle-aged men and women after famine exposure during gestation: the Dutch Hunger Winter Families Study. Am J Clin Nutr 89(6):1737–1743

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morimoto S, Calzada L, Sosa TC, Reyes-Castro LA, Rodriguez-Gonzalez GL, Morales A, Nathanielsz PW, Zambrano E (2012) Emergence of ageing-related changes in insulin secretion by pancreatic islets of male rat offspring of mothers fed a low-protein diet. Br J Nutr 107(11):1562–1565

    Article  CAS  PubMed  Google Scholar 

  • Mortimer JA, Borenstein AR, Gosche KM, Snowdon DA (2005) Very early detection of Alzheimer neuropathology and the role of brain reserve in modifying its clinical expression. J Geriatr Psychiatry Neurol 18(4):218–223

    Article  PubMed  PubMed Central  Google Scholar 

  • Ozanne S (2014) Nutrigenomic programming of cardiovascular and metabolic diseases. Free Radic Biol Med 75(Suppl 1):S11

    Article  PubMed  Google Scholar 

  • Ozanne SE, Hales CN (2004) Lifespan: catch-up growth and obesity in male mice. Nature 427(6973):411–412

    Article  CAS  PubMed  Google Scholar 

  • Painter RC, de Rooij SR, Bossuyt PM, Simmers TA, Osmond C, Barker DJ, Bleker OP, Roseboom TJ (2006) Early onset of coronary artery disease after prenatal exposure to the Dutch famine. Am J Clin Nutr 84(2):322–327; quiz 466–467

    Article  CAS  PubMed  Google Scholar 

  • Painter RC, de Rooij SR, Hutten BA, Bossuyt PM, de Groot E, Osmond C, Barker DJ, Bleker OP, Roseboom TJ (2007) Reduced intima media thickness in adults after prenatal exposure to the Dutch famine. Atherosclerosis 193(2):421–427

    Article  CAS  PubMed  Google Scholar 

  • Ravelli AC, van der Meulen JH, Michels RP, Osmond C, Barker DJ, Hales CN, Bleker OP (1998) Glucose tolerance in adults after prenatal exposure to famine. Lancet (London, England) 351(9097):173–177

    Article  CAS  Google Scholar 

  • Ravelli AC, van Der Meulen JH, Osmond C, Barker DJ, Bleker OP (1999) Obesity at the age of 50 y in men and women exposed to famine prenatally. Am J Clin Nutr 70(5):811–816

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez-Rodriguez P, Lopez de Pablo AL, Garcia-Prieto CF, Somoza B, Quintana-Villamandos B, Gomez de Diego JJ, Gutierrez-Arzapalo PY, Ramiro-Cortijo D, Gonzalez MC, Arribas SM (2017) Long term effects of fetal undernutrition on rat heart. Role of hypertension and oxidative stress. PloS ONE 12(2):e0171544

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Roeder LM, Chow BF (1972) Maternal undernutrition and its long-term effects on the offspring. Am J Clin Nutr 25(8):812–821

    Article  CAS  PubMed  Google Scholar 

  • Roseboom TJ, van der Meulen JH, Osmond C, Barker DJ, Ravelli AC, Schroeder-Tanka JM, van Montfrans GA, Michels RP, Bleker OP (2000a) Coronary heart disease after prenatal exposure to the Dutch famine, 1944–45. Heart (British Cardiac Society) 84(6):595–598

    Article  CAS  Google Scholar 

  • Roseboom TJ, van der Meulen JH, Osmond C, Barker DJ, Ravelli AC, Bleker OP (2000b) Plasma lipid profiles in adults after prenatal exposure to the Dutch famine. Am J Clin Nutr 72(5):1101–1106

    Article  CAS  PubMed  Google Scholar 

  • Shi Z, Nicholls SJ, Taylor AW, Magliano DJ, Appleton S, Zimmet P (2018) Early life exposure to Chinese famine modifies the association between hypertension and cardiovascular disease. J Hypertens 36(1):54–60

    Article  CAS  PubMed  Google Scholar 

  • Snoeck A, Remacle C, Reusens B, Hoet JJ (1990) Effect of a low protein diet during pregnancy on the fetal rat endocrine pancreas. Biol Neonate 57(2):107–118

    Article  CAS  PubMed  Google Scholar 

  • Stein AD, Zybert PA, van der Pal-de Bruin K, Lumey (2006) Exposure to famine during gestation, size at birth, and blood pressure at age 59 y: evidence from the Dutch Famine. Eur J Epidemiol 21(10):759–765

    Article  PubMed  Google Scholar 

  • Stern Y (2002) What is cognitive reserve? Theory and research application of the reserve concept. J Int Neuropsychol Soc JINS 8(3):448–460

    Article  PubMed  Google Scholar 

  • Tarry-Adkins JL, Martin-Gronert MS, Chen JH, Cripps RL, Ozanne SE (2008) Maternal diet influences DNA damage, aortic telomere length, oxidative stress, and antioxidant defense capacity in rats. FASEB J: Off Publ Fed Am Soc Exp Biol 22(6):2037–2044

    Article  CAS  Google Scholar 

  • Tarry-Adkins JL, Chen JH, Smith NS, Jones RH, Cherif H, Ozanne SE (2009) Poor maternal nutrition followed by accelerated postnatal growth leads to telomere shortening and increased markers of cell senescence in rat islets. FASEB J: Off Publ Fed Am Soc Exp Biol 23(5):1521–1528

    Article  CAS  Google Scholar 

  • Tarry-Adkins JL, Fernandez-Twinn DS, Chen JH, Hargreaves IP, Neergheen V, Aiken CE, Ozanne SE (2016) Poor maternal nutrition and accelerated postnatal growth induces an accelerated aging phenotype and oxidative stress in skeletal muscle of male rats. Dis Models Mech 9(10):1221–1229

    Article  CAS  Google Scholar 

  • Thurner S, Klimek P, Szell M, Duftschmid G, Endel G, Kautzky-Willer A, Kasper DC (2013) Quantification of excess risk for diabetes for those born in times of hunger, in an entire population of a nation, across a century. Proc Natl Acad Sci USA 110(12):4703–4707

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tobi EW, Slieker RC, Stein AD, Suchiman HE, Slagboom PE, van Zwet EW, Heijmans BT, Lumey LH (2015) Early gestation as the critical time-window for changes in the prenatal environment to affect the adult human blood methylome. Int J Epidemiol 44(4):1211–1223

    Article  PubMed  PubMed Central  Google Scholar 

  • Tobi EW, RC Slieker, Luijk R, Dekkers KF, Stein AD, Xu KM, Slagboom PE, van Zwet EW, Lumey LH, Heijmans BT (2018) DNA methylation as a mediator of the association between prenatal adversity and risk factors for metabolic disease in adulthood. Sci Adv 4(1):eaao4364

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Trombetti A, Reid KF, Hars M, Herrmann FR, Pasha E, Phillips EM, Fielding RA (2016) Age-associated declines in muscle mass, strength, power, and physical performance: impact on fear of falling and quality of life. Osteoporos Int J Establ Result Coop Eur Found Osteoporos Natl Osteoporos Found USA 27(2):463–471

    Article  CAS  Google Scholar 

  • van Abeelen AF, Veenendaal MV, Painter RC, de Rooij SR, Dijkgraaf MG, Bossuyt PM, Elias SG, Grobbee DE, Uiterwaal CS, Roseboom TJ (2012) Survival effects of prenatal famine exposure. Am J Clin Nutr 95(1):179–183

    Article  PubMed  CAS  Google Scholar 

  • Wang PX, Wang JJ, Lei YX, Xiao L, Luo ZC (2012) Impact of fetal and infant exposure to the Chinese Great Famine on the risk of hypertension in adulthood. PLoS ONE 7(11):e49720

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang C, An Y, Yu H, Feng L, Liu Q, Lu Y, Wang H, Xiao R (2016) Association between exposure to the Chinese famine in different stages of early life and decline in cognitive functioning in adulthood. Front Behav Neurosci 10:146

    PubMed  PubMed Central  Google Scholar 

  • Wang Z, Li C, Yang Z, Ma J, Zou Z (2017) Fetal and infant exposure to severe Chinese famine increases the risk of adult dyslipidemia: results from the China health and retirement longitudinal study. BMC Public Health 17(1):488

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Waterland RA, Kellermayer R, Laritsky E, Rayco-Solon P, Harris RA, Travisano M, Zhang W, Torskaya MS, Zhang J, Shen L, Manary MJ, Prentice AM (2010) Season of conception in rural gambia affects DNA methylation at putative human metastable epialleles. PLoS Genet 6(12):e1001252

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Watkins AJ, Lucas ES, Torrens C, Cleal JK, Green L, Osmond C, Eckert JJ, Gray WP, Hanson MA, Fleming TP (2010) Maternal low-protein diet during mouse pre-implantation development induces vascular dysfunction and altered renin-angiotensin-system homeostasis in the offspring. Br J Nutr 103(12):1762–1770

    Article  CAS  PubMed  Google Scholar 

  • Xu H, Zhang Z, Li L, Liu J (2018) Early life exposure to China’s 1959–61 famine and midlife cognition. Int J Epidemiol 47(1):109–120

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Susanne R. de Rooij .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

de Rooij, S.R. (2019). Prenatal Undernutrition and Ageing and Longevity. In: Vaiserman, A. (eds) Early Life Origins of Ageing and Longevity. Healthy Ageing and Longevity, vol 9. Springer, Cham. https://doi.org/10.1007/978-3-030-24958-8_10

Download citation

Publish with us

Policies and ethics