Prenatal undernutrition and cognitive function in late adulthood
Open accessAbstract
At the end of World War II, a severe 5-mo famine struck the cities in the western part of The Netherlands. At its peak, the rations dropped to as low as 400 calories per day. In 1972, cognitive performance in 19-y-old male conscripts was reported not to have been affected by exposure to the famine before birth. In the present study, we show that cognitive function in later life does seem affected by prenatal undernutrition. We found that at age 56 to 59, men and women exposed to famine during the early stage of gestation performed worse on a selective attention task, a cognitive ability that usually declines with increasing age. We hypothesize that this decline may be an early manifestation of an accelerated cognitive aging process.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
A growth-restricted fetus has fewer insulin-producing beta cells and reduced vascularization in the pancreas, and compromised structure and maturation of the brain, lungs, and liver.
“In addition, the pancreas has fewer insulin-producing beta cells and reduced vascularization (159, 340, 473), and the structure and maturation of the brain (142), lungs (358, 359, 424, 460) and liver (209, 474) are compromised.”
From Placental Origins of Chronic Disease (2016) · cites this paper as [142]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
The Hospital Anxiety and Depression Scale
Zigmond, A. S., & Snaith, R. P. (1983) · Acta Psychiatrica Scandinavica · doi:10.1111/j.1600-0447.1983.tb09716.x · Cited by 47,139 · see citing works
Studies of interference in serial verbal reactions
Stroop, J. R. (1935) · Journal of Experimental Psychology · doi:10.1037/h0054651 · Cited by 18,622 · see citing works
Half a century of research on the Stroop effect: An integrative review.
MacLeod, C. M. (1991) · Psychological Bulletin · doi:10.1037/0033-2909.109.2.163 · Cited by 5,500 · see citing works
Extending Healthy Life Span—From Yeast to Humans
Fontana, L., Partridge, L., & Longo, V. D. (2010) · Science · doi:10.1126/science.1172539 · Cited by 3,023 · see citing works
Glucose tolerance in adults after prenatal exposure to famine
Ravelli, A., van der Meulen, J., Michels, R., Osmond, C., Barker, D., Hales, C., & Bleker, O. (1998) · The Lancet · doi:10.1016/s0140-6736(97)07244-9 · Cited by 1,606 · see citing works
Obesity at the age of 50 y in men and women exposed to famine prenatally
Ravelli, A. C. J., van der Meulen, J., Osmond, C., Barker, D. J. P., & Bleker, O. P. (1999) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/70.5.811 · Cited by 1,165 · see citing works
The Dutch Famine and Its Long-Term Consequences for Adult Health
Roseboom, T., de Rooij, S., & Painter, R. (2006) · Early Human Development · doi:10.1016/j.earlhumdev.2006.07.001 · Cited by 1,137 · see citing works
Self-citationBreteler, M. M. B., Swieten, J. C. V., Bots, M. L., Grobbee, D. E., Claus, J. J., Hout, J. H. W. V. D., van Harskamp, F., Tanghe, H. L. J., de Jong, P. T. V. M., van Gijn, J., et al. (1994) · Neurology · doi:10.1212/wnl.44.7.1246 · Cited by 1,006 · see citing works
Hibbeln, J. R., Davis, J. M., Steer, C., Emmett, P., Rogers, I., Williams, C., & Golding, J. (2007) · The Lancet · doi:10.1016/s0140-6736(07)60277-3 · Cited by 987 · see citing works
Alzheimer Disease as a Vascular Disorder
de la Torre, J. C. (2002) · Stroke · doi:10.1161/01.str.0000014421.15948.67 · Cited by 844 · see citing works
Schizophrenia After Prenatal Famine
Susser, E. (1996) · Archives of General Psychiatry · doi:10.1001/archpsyc.1996.01830010027005 · Cited by 741 · see citing works
Famine and Human Development. The Dutch Hunger Winter of 1944-1945.
(1975) · Annals of Internal Medicine · doi:10.7326/0003-4819-83-2-290_1 · Cited by 658 · see citing works
The nutritional basis of the fetal origins of adult disease
Harding, J. E. (2001) · International Journal of Epidemiology · doi:10.1093/ije/30.1.15 · Cited by 561 · see citing works
Carter, C. S., Mintun, M. A., Nichols, T. E., & Cohen, J. D. (1997) · American Journal of Psychiatry · doi:10.1176/ajp.154.12.1670 · Cited by 389 · see citing works
Maternal DHA and the Development of Attention in Infancy and Toddlerhood
Colombo, J. A., Kannass, K. N., Shaddy, D. J., Kundurthi, S., Maikranz, J. M., Anderson, C. J., Blaga, O. M., & Carlson, S. E. (2004) · Child Development · doi:10.1111/j.1467-8624.2004.00737.x · Cited by 285 · see citing works
Nutrition and Mental Performance
STEIN, Z. A., Susser, M. W., Saenger, G. H., & MAROLLA, F. A. (1972) · Science · doi:10.1126/science.178.4062.708 · Cited by 271 · see citing works
Schizophrenia After Prenatal Famine
van Os, J. (1997) · Archives of General Psychiatry · doi:10.1001/archpsyc.1997.01830180095015 · Cited by 264 · see citing works
Prenatal Exposure to Famine and Brain Morphology in Schizophrenia
Pol, H. E. H., Hoek, H. W., Susser, E., Brown, A. S., Dingemans, A. E., Schnack, H. G., van Haren, N. E. M., Ramos, L. M. P., Wied, C. C. G., & Kahn, R. S. (2000) · American Journal of Psychiatry · doi:10.1176/appi.ajp.157.7.1170 · Cited by 215 · see citing works
Chapter 22 Cognitive aging and increased distractibility: Costs and potential benefits
Healey, M. K., Campbell, K. L., & Hasher, L. (2008) · Progress in brain research · doi:10.1016/s0079-6123(07)00022-2 · Cited by 177 · see citing works
Schizoid personality disorder after prenatal exposure to famine
Hoek, H. W., Susser, E., Buck, K. A., Lumey, L. H., Lin, S. P., & Gorman, J. M. (1996) · American Journal of Psychiatry · doi:10.1176/ajp.153.12.1637 · Cited by 168 · see citing works
Famine and Human Development: The Dutch Hunger Winter 1944-1945
Smith, C. A. (1976) · Archives of Pediatrics and Adolescent Medicine · doi:10.1001/archpedi.1976.02120030112028 · Cited by 153 · see citing works
Schizophrenia and the Stroop Effect
Henik, A., & Salo, R. E. (2004) · Behavioral and Cognitive Neuroscience Reviews · doi:10.1177/1534582304263252 · Cited by 148 · see citing works
Cognitive frailty: Predementia syndrome and vascular risk factors
Panza, F., D’Introno, A., Colacicco, A. M., Capurso, C. A., Parigi, A. D., Capurso, S. A., Caselli, R. J., Pilotto, A., Scafato, E., Capurso, A., et al. (2005) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2005.05.008 · Cited by 148 · see citing works
Balota, D. A., Tse, C., Hutchison, K. A., Spieler, D. H., Duchek, J. M., & Morris, J. C. (2010) · Psychology and Aging · doi:10.1037/a0017474 · Cited by 139 · see citing works
Vitamin B 12 Status of Pregnant Indian Women and Cognitive Function in their 9-year-old Children
Bhate, V., Deshpande, S. S., Bhat, D., Joshi, N. P., Ladkat, R., Watve, S., Fall, C. H. D., de Jager, C. A., Refsum, H., & Yajnik, C. S. (2008) · Food and Nutrition Bulletin · doi:10.1177/156482650802900401 · Cited by 127 · see citing works
Martyn, C. N., Galé, C. R., Sayer, A. A., & Fall, C. H. D. (1996) · BMJ · doi:10.1136/bmj.312.7043.1393a · Cited by 110 · see citing works
Kirman, B. H. (1976) · BMJ · doi:10.1136/bmj.1.6006.403-a · Cited by 106 · see citing works
Ranade, S. C., Rose, A., Rao, M. S. R., Gallego, J., Gressèns, P., & Mani, S. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.01.002 · Cited by 101 · see citing works
Caloric restriction and brain function
Guyonnet, S., & Vellas, B. J. (2008) · Current Opinion in Clinical Nutrition & Metabolic Care · doi:10.1097/mco.0b013e328313968f · Cited by 97 · see citing works
Interpreting Stroop interference: An analysis of differences between task versions.
Salo, R. E., Henik, A., & Robertson, L. C. (2001) · Neuropsychology · doi:10.1037//0894-4105.15.4.462 · Cited by 82 · see citing works
Interpreting Stroop interference: An analysis of differences between task versions.
Salo, R. E., Henik, A., & Robertson, L. C. (2001) · Neuropsychology · doi:10.1037/0894-4105.15.4.462 · Cited by 78 · see citing works
Reynolds, M., Johnston, J. M., Dodge, H. H., DeKosky, S. T., & Ganguli, M. (1999) · Neurology · doi:10.1212/wnl.53.1.228 · Cited by 59 · see citing works
Swieten, J. C. V., Staal, S., Kappelle, L. J., Derix, M. M. A., & van Gijn, J. (1996) · Journal of Neurology · doi:10.1007/bf02444014 · Cited by 56 · see citing works
Cognitive Functions in Subjects with Incidental Cerebral Hyperintensities
Fukui, T., Sugita, K., Satō, Y., Takeuchi, T., & Tsukagoshi, H. (2008) · European Neurology · doi:10.1159/000117055 · Cited by 43 · see citing works
Maze Studies on Progeny of Underfed Mother Rats
SIMONSON, M., & Chow, B. F. (1970) · Journal of Nutrition · doi:10.1093/jn/100.6.685 · Cited by 42 · see citing works
Schweizer, R., Ranke, M. B., Binder, G., Herdach, F., Zapadlo, M., Grauer, M.-L., Schwarze, C. P., & Wollmann, H. A. (2000) · Hormone Research in Paediatrics · doi:10.1159/000023572 · Cited by 39 · see citing works
Bush, M., & Leathwood, P. D. (1975) · British Journal Of Nutrition · doi:10.1079/bjn19750042 · Cited by 39 · see citing works
Incidental learning is impaired during early‐life undernutrition
Rogers, P. J., Tonkiss, J., & Smart, J. L. (1986) · Developmental Psychobiology · doi:10.1002/dev.420190204 · Cited by 18 · see citing works
Nutting, C. B., & Baskette, J. E., Jr. (1941) · Nature · doi:10.1038/147335a0 · Cited by 1 · see citing works
Flagged first, then by citations
Research works printed but not linked: 4
- [31]National Bureau of Food Distribution in Wartime Rations per day period 1 Oct 1944– 22 July 1945 for the western Netherlands. 1945 (Translated from the Dutch) [[Google Scholar](https://scholar.google.com/scholar_lookup?journal=Rations%20per%20day%20period%201%20Oct%201944%E2%80%93%2022%20July%201945%20for%20the%20western%20Netherlands&publication_year=1945&)]
- [32]Burger GCE, Sandstead HR, Drummond JC. Malnutrition and Starvation in Western Netherlands, September 1944 to July 1945. Part I and II. The Hague: General State Printing Office; 1948. [[Google Scholar](https://scholar.google.com/scholar_lookup?title=Malnutrition%20and%20Starvation%20in%20Western%20Netherlands,%20September%201944%20to%20July%201945.%20Part%20I%20and%20II&author=GCE%20Burger&author=HR%20Sandstead&author=JC%20Drummond&publication_year=1948&)]
- [34]Bakker B, Sieben I. International Socio-Economic Index of occupational status (1992) Soc Wetenschappen. 1997;40:1–22. (Translated from the Dutch) [[Google Scholar](https://scholar.google.com/scholar_lookup?journal=Soc%20Wetenschappen&title=International%20Socio-Economic%20Index%20of%20occupational%20status%20(1992)&author=B%20Bakker&author=I%20Sieben&volume=40&publication_year=1997&pages=1-22&)]
- [36]Heim A. AH4 Group Test of General Intelligence. Windsor, United Kingdom: NFER-Nelson Publishing Company Ltd; 1970. [[Google Scholar](https://scholar.google.com/scholar_lookup?title=AH4%20Group%20Test%20of%20General%20Intelligence&author=A%20Heim&publication_year=1970&)]
Cited by
Sorted by citations
Placental Origins of Chronic Disease
Burton, G. J., Fowden, A. L., & Thornburg, K. L. (2016) · Physiological Reviews · doi:10.1152/physrev.00029.2015 · Cited by 717 · see citing works
The role of nutrition in children's neurocognitive development, from pregnancy through childhood
Nyaradi, A., Li, J., Hickling, S., Foster, J. K., & Oddy, W. H. (2013) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2013.00097 · Cited by 575 · see citing works
Hungry in the womb: What are the consequences? Lessons from the Dutch famine
Roseboom, T. J., Painter, R. C., van Abeelen, A. F. M., Veenendaal, M. V. E., & de Rooij, S. R. (2011) · Maturitas · doi:10.1016/j.maturitas.2011.06.017 · Cited by 488 · see citing works
Self-citationPrenatal Famine and Adult Health
Lumey, L. H., Stein, A. D., & Susser, E. (2011) · Annual Review of Public Health · doi:10.1146/annurev-publhealth-031210-101230 · Cited by 460 · see citing works
The Dutch hunger winter and the developmental origins of health and disease
Schulz, L. C. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1012911107 · Cited by 438 · see citing works
The epigenetics of maternal cigarette smoking during pregnancy and effects on child development
Knopik, V. S., Maccani, M. A., Francazio, S. K., & McGeary, J. E. (2012) · Development and Psychopathology · doi:10.1017/s0954579412000776 · Cited by 282 · see citing works
Food for thought: how nutrition impacts cognition and emotion
Spencer, S. J., Kőrösi, A., Layé, S., Shukitt‐Hale, B., & Barrientos, R. M. (2017) · npj Science of Food · doi:10.1038/s41538-017-0008-y · Cited by 279 · see citing works
The role of nutrition on epigenetic modifications and their implications on health
Jiménez-Chillarón, J. C., Díaz, R., Martínez, D., Pentinat, T., Ramón-Krauel, M., Ribó, S., & Plösch, T. (2012) · Biochimie · doi:10.1016/j.biochi.2012.06.012 · Cited by 266 · see citing works
The Effects of World War II on Economic and Health Outcomes across Europe
Kesternich, I., Siflinger, B. M., Smith, J. P., & Winter, J. (2013) · The Review of Economics and Statistics · doi:10.1162/rest_a_00353 · Cited by 259 · see citing works
Hajj, N. E., Pliushch, G., Schneider, E., Dittrich, M. T., Müller, T., Korenkov, M., Aretz, M., Zechner, U., Lehnen, H., & Haaf, T. (2012) · Diabetes · doi:10.2337/db12-0289 · Cited by 256 · see citing works
Fetal Programming and Metabolic Syndrome
Rinaudo, P. F., & Wang, E. T. (2011) · Annual Review of Physiology · doi:10.1146/annurev-physiol-020911-153245 · Cited by 250 · see citing works
Maternal Nutrition and Neurodevelopment: A Scoping Review
Cortés-Albornoz, M. C., García-Guáqueta, D. P., Vélez-van-Meerbeke, A., & Talero‐Gutiérrez, C. (2021) · Nutrients · doi:10.3390/nu13103530 · Cited by 244 · see citing works
The Programming Power of the Placenta
Sferruzzi-Perri, A. N., & Camm, E. J. (2016) · Frontiers in Physiology · doi:10.3389/fphys.2016.00033 · Cited by 223 · see citing works
Epigenetic inheritance of polycystic ovary syndrome — challenges and opportunities for treatment
Stener‐Victorin, E., & Deng, Q. (2021) · Nature Reviews Endocrinology · doi:10.1038/s41574-021-00517-x · Cited by 223 · see citing works
Hajj, N. E., & Haaf, T. (2013) · Fertility and Sterility · doi:10.1016/j.fertnstert.2012.12.044 · Cited by 205 · see citing works
Prenatal growth in humans and postnatal brain maturation into late adolescence
Raznahan, A., GREENSTEIN, D. K., Lee, N., CLASEN, L. S., & Giedd, J. N. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1203350109 · Cited by 190 · see citing works
Energy metabolism and energy-sensing pathways in mammalian embryonic and adult stem cell fate
Rafalski, V. A., Mancini, E., & Brunet, A. (2012) · Journal of Cell Science · doi:10.1242/jcs.114827 · Cited by 179 · see citing works
Early life adversity shapes neural circuit function during sensitive postnatal developmental periods
Malave, L., van Dijk, M. T., & Anacker, C. (2022) · Translational Psychiatry · doi:10.1038/s41398-022-02092-9 · Cited by 177 · see citing works
Lucassen, P. J., Naninck, E. F. G., van Goudoever, J. B., Fitzsimons, C. P., Joëls, M., & Kőrösi, A. (2013) · Trends in Neurosciences · doi:10.1016/j.tins.2013.08.002 · Cited by 173 · see citing works
Kirolos, A., Goyheneix, M., Eliasz, M. K., Chisala, M. N., Lissauer, S., Gladstone, M., & Kerac, M. (2022) · BMJ Global Health · doi:10.1136/bmjgh-2022-009330 · Cited by 141 · see citing works
Lehnen, H., Zechner, U., & Haaf, T. (2013) · Molecular Human Reproduction · doi:10.1093/molehr/gat020 · Cited by 141 · see citing works
Alamy, M., & Bengelloun, W. A. (2012) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2012.03.009 · Cited by 139 · see citing works
Scholte, R. S., van den Berg, G. J., & Lindeboom, M. (2014) · Journal of Health Economics · doi:10.1016/j.jhealeco.2014.10.002 · Cited by 139 · see citing works
Sex hormone activity in alcohol addiction: Integrating organizational and activational effects
Lenz, B., Müller, C. P., Stoessel, C., Sperling, W., Biermann, T., Hillemacher, T., Bleich, S., & Kornhuber, J. (2011) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2011.11.001 · Cited by 136 · see citing works
Lindsay, K. L., Buß, C., Wadhwa, P. D., & Entringer, S. (2018) · Biological Psychiatry · doi:10.1016/j.biopsych.2018.06.021 · Cited by 135 · see citing works
Fitzgerald, E., Hor, K., & Drake, A. J. (2020) · Early Human Development · doi:10.1016/j.earlhumdev.2020.105190 · Cited by 136 · see citing works
Angiogenic Factors in Preeclampsia and Related DisordersPreprint
Cerdeira, A. S., & Karumanchi, S. A. (2012) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a006585 · Cited by 133 · see citing works
Achieving universal health coverage in France: policy reforms and the challenge of inequalities
Nay, O., Béjean, S., Benamouzig, D., Bergeron, H., Castel, P., & Ventelou, B. (2016) · The Lancet · doi:10.1016/s0140-6736(16)00580-8 · Cited by 132 · see citing works
Life experience and demographic influences on cognitive function in older adults.
Brewster, P. W. H., Melrose, R. J., Marquine, M. J., Johnson, J. K., Nápoles, A. M., MacKay‐Brandt, A., Farias, S. T., Reed, B., & Mungas, D. (2014) · Neuropsychology · doi:10.1037/neu0000098 · Cited by 126 · see citing works
Lesuis, S. L., Hoeijmakers, L., Kőrösi, A., de Rooij, S. R., Swaab, D. F., Kessels, H. W. H. G., Lucassen, P. J., & Krugers, H. J. (2018) · Alzheimer s Research & Therapy · doi:10.1186/s13195-018-0422-7 · Cited by 120 · see citing works
Wang, S., Sun‐Waterhouse, D., Waterhouse, G. I. N., Zheng, L. P., Su, G., & Zhao, M. (2021) · Trends in Food Science & Technology · doi:10.1016/j.tifs.2021.04.056 · Cited by 111 · see citing works
van den Berg, G. J., Pinger, P., & Schoch, J. (2015) · The Economic Journal · doi:10.1111/ecoj.12250 · Cited by 107 · see citing works
Early life exposure to China’s 1959–61 famine and midlife cognition
Xu, H., Zhang, Z., Li, L., & Liu, J. (2017) · International Journal of Epidemiology · doi:10.1093/ije/dyx222 · Cited by 106 · see citing works
Bleker, L. S., de Rooij, S. R., Painter, R. C., Ravelli, A. C., & Roseboom, T. J. (2021) · BMJ Open · doi:10.1136/bmjopen-2020-042078 · Cited by 102 · see citing works
Self-citationStefan Thurner, A., Klimek, P., Szell, M., Duftschmid, G., Endel, G., Kautzky‐Willer, A., & Kasper, D. C. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1215626110 · Cited by 95 · see citing works
Berghänel, A., Heistermann, M., Schülke, O., & Ostner, J. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1707152114 · Cited by 93 · see citing works
Iron deficiency during pregnancy: the consequences for placental function and fetal outcome
McArdle, H. J., Gambling, L., & Kennedy, C. (2013) · Proceedings of The Nutrition Society · doi:10.1017/s0029665113003637 · Cited by 93 · see citing works
Hoeijmakers, L., Lucassen, P. J., & Kőrösi, A. (2015) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2014.00103 · Cited by 92 · see citing works
Prenatal famine exposure and cognition at age 59 years
de Groot, R. H. M., Stein, A. D., Jolles, J., van Boxtel, M. P. J., Blauw, G. J., van de Bor, M., & Lumey, L. H. (2011) · International Journal of Epidemiology · doi:10.1093/ije/dyq261 · Cited by 90 · see citing works
The involvement of astrocytes in early‐life adversity induced programming of the brain
Abbink, M. R., van Deijk, A. F., Heine, V. M., Verheijen, M. H. G., & Kőrösi, A. (2019) · Glia · doi:10.1002/glia.23625 · Cited by 92 · see citing works
CRITICAL PERIODS DURING CHILDHOOD AND ADOLESCENCE
van den Berg, G. J., Lundborg, P., Nystedt, P., & Rooth, D. (2014) · Journal of the European Economic Association · doi:10.1111/jeea.12112 · Cited by 100 · see citing works
Impact of Demographic and Obstetric Factors on Infant Brain Volumes: A Population Neuroscience Study
Knickmeyer, R., Xia, K., Lu, Z., Ahn, M., Jha, S., Zou, F., Zhu, H.-T., Styner, M., & Gilmore, J. (2016) · Cerebral Cortex · doi:10.1093/cercor/bhw331 · Cited by 85 · see citing works
Metabolic syndrome: Role of maternal undernutrition and fetal programming
Ramakrishnan, L. (2013) · Reviews in Endocrine and Metabolic Disorders · doi:10.1007/s11154-013-9266-4 · Cited by 85 · see citing works
The emerging role of dietary fructose in obesity and cognitive decline
Lakhan, S. E., & Kirchgessner, A. L. (2013) · Nutrition Journal · doi:10.1186/1475-2891-12-114 · Cited by 83 · see citing works
dos Santos, J. F., Cavalcante, C. D. M. B., Barbosa, F. T., Gitaí, D. L. G., Duzzioni, M., Tilelli, C. Q., Shetty, A. K., & de Castro, O. W. (2018) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-018-4833-2 · Cited by 80 · see citing works
Mell, H., Safra, L., Algan, Y., Baumard, N., & Chevallier, C. (2017) · Evolution and Human Behavior · doi:10.1016/j.evolhumbehav.2017.08.006 · Cited by 79 · see citing works
Premature brain aging in humans exposed to maternal nutrient restriction during early gestation
Franke, K., Christian Gaser, B., Roseboom, T. J., Schwab, M. G., & de Rooij, S. R. (2017) · NeuroImage · doi:10.1016/j.neuroimage.2017.10.047 · Cited by 79 · see citing works
Self-citationDoblhammer, G., van den Berg, G. J., & Fritze, T. (2013) · PLoS ONE · doi:10.1371/journal.pone.0074915 · Cited by 12 · see citing works
Neurodevelopment, Nutrition, and Inflammation: The Evolving Global Child Health Landscape
Bhutta, Z. A., Guerrant, R. L., & Nelson, C. A. (2017) · PEDIATRICS · doi:10.1542/peds.2016-2828d · Cited by 84 · see citing works
Effect of Prenatal Exposure to Tobacco Smoke on Inhibitory Control
Holz, N. E., Boecker, R., Baumeister, S., Hohm, E., Zohsel, K., Buchmann, A. F., Blomeyer, D., Jennen-Steinmetz, C., Hohmann, S., Wolf, I., et al. (2014) · JAMA Psychiatry · doi:10.1001/jamapsychiatry.2014.343 · Cited by 78 · see citing works
A war is forever: The long-run effects of early exposure to World War II on trust
Conzo, P., & Salustri, F. (2019) · European Economic Review · doi:10.1016/j.euroecorev.2019.103313 · Cited by 76 · see citing works
Early life stress and later health outcomes—findings from the Helsinki Birth Cohort Study
Eriksson, M. D., Räikkönen, K., & Eriksson, J. G. (2013) · American Journal of Human Biology · doi:10.1002/ajhb.22502 · Cited by 76 · see citing works
Roseboom, T. J. (2019) · Journal of Endocrinology · doi:10.1530/joe-18-0683 · Cited by 75 · see citing works
Self-citationLamar, M., Lerner, A. J., James, B. D., Yu, L., Glover, C. M., Wilson, R. S., & Barnes, L. L. (2020) · The Journals of Gerontology: Series B · doi:10.1093/geronb/gbz031 · Cited by 70 · see citing works
Prenatal famine exposure has sex-specific effects on brain size
de Rooij, S. R., Caan, M. W. A., Swaab, D. F., Nederveen, A. J., Majoie, C. B. L. M., Schwab, M. G., Painter, R. C., & Roseboom, T. J. (2016) · Brain · doi:10.1093/brain/aww132 · Cited by 72 · see citing works
Self-citationFan, W., & Qian, Y. (2014) · Social Science Research · doi:10.1016/j.ssresearch.2014.07.007 · Cited by 71 · see citing works
Early determinants of mental health
Räikkönen, K., Pesonen, A., Roseboom, T. J., & Eriksson, J. G. (2012) · Best Practice & Research Clinical Endocrinology & Metabolism · doi:10.1016/j.beem.2012.03.001 · Cited by 67 · see citing works
Self-citationEarly Life Exposure to the 1918 Influenza Pandemic and Old-Age Mortality by Cause of Death
Myrskylä, M., Mehta, N. K., & Chang, V. W. (2013) · American Journal of Public Health · doi:10.2105/ajph.2012.301060 · Cited by 67 · see citing works
Ginty, A. T., Phillips, A. C., Roseboom, T. J., Carroll, D., & de Rooij, S. R. (2011) · Psychophysiology · doi:10.1111/j.1469-8986.2011.01316.x · Cited by 67 · see citing works
Self-citationde Rooij, S. R., Bleker, L. S., Painter, R. C., Ravelli, A. C. J., & Roseboom, T. J. (2021) · International Journal of Environmental Health Research · doi:10.1080/09603123.2021.1888894 · Cited by 64 · see citing works
Self-citationGrowing up in wartime: Evidence from the era of two world wars
Havari, E., & Peracchi, F. (2016) · Economics & Human Biology · doi:10.1016/j.ehb.2016.09.002 · Cited by 64 · see citing works
Environmental enteric dysfunction: gut and microbiota adaptation in pregnancy and infancy
Cowardin, C. A., Syed, S., Iqbal, N. T., Jamil, Z., Sadiq, K., Iqbal, J., Ali, A., & Moore, S. R. (2022) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-022-00714-7 · Cited by 67 · see citing works
Developmental plasticity and its relevance to assisted human reproduction
Roseboom, T. J. (2018) · Human Reproduction · doi:10.1093/humrep/dey034 · Cited by 63 · see citing works
Self-citationAkitake, Y., Katsuragi, S., Hosokawa, M., 三島, 健., Ikeda, T., Miyazato, M., & Hosoda, H. (2014) · Nutrition Research · doi:10.1016/j.nutres.2014.10.014 · Cited by 60 · see citing works
Gage, S. H., Lawlor, D. A., Tilling, K. M., & Fraser, A. (2013) · American Journal of Epidemiology · doi:10.1093/aje/kws239 · Cited by 60 · see citing works
Early Life Origins Cognitive Decline: Findings in Elderly Men in the Helsinki Birth Cohort Study
Räikkönen, K., Kajantie, E., Pesonen, A., Heinonen, K., Alastalo, H., Leskinen, J. T., Nyman, K., HENRIKSSON, M. M., Lahti, J. M. T., Lahti‐Pulkkinen, M., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0054707 · Cited by 59 · see citing works
Birth Size and Brain Function 75 Years Later
Muller, M., Sigurdsson, S., Kjartansson, Ó., Jónsson, P., Garcia, M. E., von Bonsdorff, M. V., Gunnarsdottir, I., Thorsdottir, I., Harris, T., van Buchem, M., et al. (2014) · Pediatrics · doi:10.1542/peds.2014-1108 · Cited by 63 · see citing works
Long‐term Effects of Prenatal Stress and Glucocorticoid Exposure
Painter, R. C., Roseboom, T. J., & de Rooij, S. R. (2012) · Birth Defects Research Part C Embryo Today Reviews · doi:10.1002/bdrc.21021 · Cited by 57 · see citing works
Self-citationPreimplantation Stress and Development
Feuer, S. K., & Rinaudo, P. F. (2012) · Birth Defects Research Part C Embryo Today Reviews · doi:10.1002/bdrc.21022 · Cited by 57 · see citing works
An Update on the Relevance of the Life Course Perspective for Social Work
Hutchison, E. D. (2019) · Families in Society The Journal of Contemporary Social Services · doi:10.1177/1044389419873240 · Cited by 57 · see citing works
Prenatal substance exposure and offspring development: Does DNA methylation play a role?
Knopik, V. S., Marceau, K., Bidwell, L. C., & Rolan, E. (2018) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2018.01.009 · Cited by 45 · see citing works
Cooper, A. R., O’Neill, K. E., Allsworth, J. E., Jungheim, E. S., Odibo, A. O., Gray, D. L., Ratts, V. S., Moley, K. H., & Odem, R. R. (2011) · Fertility and Sterility · doi:10.1016/j.fertnstert.2011.08.038 · Cited by 56 · see citing works
Evidence for germline non-genetic inheritance of human phenotypes and diseases
Senaldi, L., & Smith-Raska, M. (2020) · Clinical Epigenetics · doi:10.1186/s13148-020-00929-y · Cited by 55 · see citing works
Franke, K., den Bergh, B. V. D. V., de Rooij, S., Kroegel, N., Nathanielsz, P., Rakers, F., Roseboom, T., Witte, O. W., & Schwab, M. (2020) · Neuroscience and Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.01.031 · Cited by 32 · see citing works
Self-citationBouillon, C., Léandri, R. D., Desch, L., Ernst, A., Bruno, C., Cerf, C., Chiron, A., Souchay, C., Burguet, A., Jimenez, C., et al. (2016) · PLoS ONE · doi:10.1371/journal.pone.0150857 · Cited by 52 · see citing works
Vargas-Martínez, F., Uvnás-Moberg, K., Petersson, M., Olausson, H., & Jiménez-Estrada, I. (2014) · Progress in neurobiology · doi:10.1016/j.pneurobio.2014.10.001 · Cited by 49 · see citing works
Jürges, H. (2012) · Journal of Health Economics · doi:10.1016/j.jhealeco.2012.11.001 · Cited by 50 · see citing works
Critical and Sensitive Periods in Development and Nutrition
Colombo, J. A., Gustafson, K. M., & Carlson, S. E. (2019) · Annals of Nutrition and Metabolism · doi:10.1159/000508053 · Cited by 52 · see citing works
Royer, M. F., Guerithault, N., Braden, B. B., Laska, M. N., & Bruening, M. M. (2021) · International Journal of Translational Medicine · doi:10.3390/ijtm1030015 · Cited by 50 · see citing works
Understanding Heterogeneity in the Effects of Birth Weight on Adult Cognition and Wages
Cook, C. J., & Fletcher, J. M. (2015) · Journal of Health Economics · doi:10.1016/j.jhealeco.2015.01.005 · Cited by 49 · see citing works
Wang, C., An, Y., Yu, H., Feng, L., Liu, Q., Lu, Y., Wang, H., & Xiao, R. (2016) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2016.00146 · Cited by 48 · see citing works
Developmental Origins of Health Span and Life Span: A Mini-Review
Preston, J. D., Reynolds, L. J., & Pearson, K. J. (2018) · Gerontology · doi:10.1159/000485506 · Cited by 48 · see citing works
Zhang, L., Yang, J., Liao, Z., Zhao, X., Hu, X., Zhu, W., & Zhang, Z. (2019) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph16071294 · Cited by 48 · see citing works
An examination of maternal prenatal BMI and human fetal brain development
Norr, M. E., Hect, J. L., Lenniger, C. J., van den Heuvel, M. P., & Thomason, M. E. (2020) · Journal of Child Psychology and Psychiatry · doi:10.1111/jcpp.13301 · Cited by 47 · see citing works
Mullin, P., Bray, A., Schoenberg, F. P., MacGibbon, K., Romero, R. J., Goodwin, T. M., & Fejzo, M. S. (2011) · Journal of Developmental Origins of Health and Disease · doi:10.1017/s2040174411000249 · Cited by 47 · see citing works
Epigenetic regulation of fetal brain development and neurocognitive outcome
Petanjek, Z., & Kostović, I. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1208085109 · Cited by 46 · see citing works
Life course health care and preemptive approach to non-communicable diseases
Imura, H. (2013) · Proceedings of the Japan Academy Series B · doi:10.2183/pjab.89.462 · Cited by 46 · see citing works
Are Brain and Cognitive Reserve Shaped by Early Life Circumstances?
de Rooij, S. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.825811 · Cited by 38 · see citing works
Immune dysfunction in developmental programming of type 2 diabetes mellitus
Golden, T., & Simmons, R. A. (2021) · Nature Reviews Endocrinology · doi:10.1038/s41574-020-00464-z · Cited by 46 · see citing works
Lanet, E., & Maurange, C. (2014) · Frontiers in Physiology · doi:10.3389/fphys.2014.00117 · Cited by 44 · see citing works
Potential maternal symptomatic benefit of gabapentin and review of its safety in pregnancy
Guttuso, T. J., Shaman, M., & Thornburg, L. L. (2014) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2014.08.013 · Cited by 44 · see citing works
Early life predictors of late life cerebral small vessel disease in four prospective cohort studies
Backhouse, E. V., Shenkin, S. D., McIntosh, A. M., Bastin, M. E., Whalley, H. C., Hernandez, M. V., Maniega, S. M., Harris, M. A., Stolicyn, A., Campbell, A. I., et al. (2021) · Brain · doi:10.1093/brain/awab331 · Cited by 45 · see citing works
Self-citationJackson, C. M., Mukherjee, S., Wilburn, A. N., Cates, C., Lewkowich, I. P., Deshmukh, H. S., Zacharias, W. J., & Chougnet, C. A. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.01285 · Cited by 43 · see citing works
Tremolizzo, L., Conti, E., Bomba, M., Uccellini, O., Rossi, M. S., Marfone, M., Corbetta, F., Santarone, M. E., Raggi, M. E., Neri, F., et al. (2013) · The World Journal of Biological Psychiatry · doi:10.3109/15622975.2013.860467 · Cited by 43 · see citing works
Li, J., Na, L., Ma, H., Zhang, Z., Li, T., Lin, L., Li, Q., Sun, C., & Li, Y. (2015) · Scientific Reports · doi:10.1038/srep13792 · Cited by 43 · see citing works
The Role of Nutrition in Children's Neurocognitive Development, From Pregnancy Through Childhood
Nyaradi, A., Li, J., Hickling, S., Foster, J. K., & Oddy, W. H. (2015) · Apple Academic Press eBooks · doi:10.1201/b18040-5 · Cited by 38 · see citing works
Prenatal famine exposure and adult health outcomes: an epigenetic link
Vaiserman, A. M., & Lushchak, O. V. (2021) · Current Zoology · doi:10.1093/eep/dvab013 · Cited by 38 · see citing works
Ancestral experience as a game changer in stress vulnerability and disease outcomes
Metz, G. A. S., Ng, J. W. Y., Kovalchuk, I., & Olson, D. M. (2015) · BioEssays · doi:10.1002/bies.201400217 · Cited by 36 · see citing works
Nutrition during pregnancy: Influence on the gut microbiome and fetal development
Barrientos, G., Ronchi, F., & Conrad, M. L. (2023) · American Journal of Reproductive Immunology · doi:10.1111/aji.13802 · Cited by 40 · see citing works
Autism Spectrum Disorders in Children Exposed in Utero to Hyperemesis Gravidarum
Getahun, D. T., Fassett, M. J., Jacobsen, S. J., Xiang, A. H., Takhar, H. S., Wing, D. A., & Peltier, M. R. (2019) · American Journal of Perinatology · doi:10.1055/s-0039-1696670 · Cited by 36 · see citing works
- Authors
- de Rooij, S. R., Wouters, H., Yonker, J. E., Painter, R. C., & Roseboom, T. J.
- Affiliations
- Departments of aClinical Epidemiology Biostatistics and Bioinformatics, and
- Calvin University (US)
- Amsterdam UMC Location University of Amsterdam (NL)
- University of Missouri (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2010-09-13
- Volume
- 107
- Issue
- 39
- Pages
- 16881-16886
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC2947913
- OpenAlex
- W2010036492
- Cited by
- 364
- References
- 38
- Citations by year
- 2026: 5 · 2025: 13 · 2024: 16 · 2023: 18 · 2022: 27 · 2021: 29 · 2020: 42 · 2019: 32 · 2018: 18 · 2017: 22 · 2016: 21 · 2015: 26 · 2014: 24 · 2013: 32 · 2012: 24
- FWCI
- 20.70
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Pure Amsterdam UMC (publishedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion)
- Funders
- European Science Foundation
- Medical Research Council
- Topics
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Cognitive Abilities and Testing
- Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
- Keywords
- prenatal malnutrition, Dutch famine, cognitive aging, old age, selective attention, cognitive decline, prenatal exposure
- MeSH terms
- Adult, Attention, Cognition, Cognition Disorders, Female, Humans, Male, Netherlands, Pregnancy, Starvation, Maternal Exposure, Prenatal Nutritional Physiological Phenomena, Malnutrition
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review