Effects of famine on placental size and efficiency
Abstract
Background Placental growth responds to maternal influences including diet. We have examined placental size, shape and efficiency among babies born around the time of the 5-month wartime famine in Holland 1944-1945.Methods We examined the birth records of 2414 term singleton babies born in Amsterdam during 1943-1947. The records included the size of the baby and the thickness of the placental surface, together with its length and breadth which we used to calculate its area and volume.Results Compared to babies born before the famine babies who were in utero during the famine had smaller placental areas. Babies whose mothers conceived after the famine ended also had smaller placental areas. Famine was associated with a 19 cm(2) decrease in area. Babies who were in mid-late gestation during the famine were 160 g lighter than would have been predicted from their placental area (p < 0.001). Babies who were in early gestation during the famine, or who were conceived after it had ended were 102 g heavier than would have been predicted from their placental area (p < 0.001). These latter babies were either longer or had larger head circumferences depending on when the mother experienced the famine. Among babies who were in early gestation during the famine the reduction in placental area was greater in boys than girls (p for interaction 0.03).Conclusion Famine impaired the normal processes of placentation, even among babies who were conceived after it had ended. In babies who were in mid-late gestation during the famine, the placenta was less efficient. In babies who were in early gestation during the famine, or who were conceived after it had ended, the placenta was more efficient. The placentas of boys and girls responded differently to famine.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
Hypertension was predicted by a short placental width and a more oval shape in men who were born after the war.
“However, hypertension was predicted by a short placental width and a more oval shape in men who were born after the war (471, 541).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [471]
The surface area of the placenta predicted hypertension with an odds ratio of 1.34 (95% CI 0.99 to 1.80) for an increase in surface area of 40 cm2.
“The surface area of the placenta also predicted hypertension with an odds ratio of 1.34 (95% CI 0.99 to 1.80) for an increase in surface area of 40 cm 2 .”
From Placental Origins of Chronic Disease (2016) · cites this paper as [471]
Among men exposed in utero to the starvation effects of the post-war famine in Holland, a reduced width of the placenta was associated with hypertension.
“Among men who were exposed in utero to the starvation effects of the post-war famine in Holland, a reduced width of the placenta was associated with hypertension (471).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [471]
Placental efficiency measured as the fetal to placental weight ratio was greater in response to undernutrition in late pregnancy than in control pregnancies before the famine.
“However, despite this, placental efficiency measured as the fetal to placental weight ratio was greater in response to the undernutrition in late pregnancy than seen in control pregnancies before the famine (350,”
From Placental Origins of Chronic Disease (2016) · cites this paper as [471]
In Dutch hunger winter populations, placental weight at term was increased when the famine occurred in the 1st trimester but was reduced, along with infant birth weight, in women who were in their 3rd trimester at the time of the famine.
“In the Dutch hunger winter populations, placental weight at term was increased when the famine occurred in the 1 st trimester but was reduced, along with infant birth weight, in women who were in their 3 rd trimester at the time of the famine (350, 471).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [471]
The size of the human placenta at term is affected by calorie intake and dietary composition during pregnancy.
“The size of the human placenta at term is known to be affected by the calorie intake and dietary composition during the pregnancy (216, 350, 471).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [471]
Cites
Fetal origins of coronary heart disease
Barker, D. J. P. (1995) · BMJ · doi:10.1136/bmj.311.6998.171 · Cited by 3,570 · see citing works
Self-citationGlucose 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
Self-citationBoys live dangerously in the womb
Eriksson, J. G., Kajantie, E., Osmond, C., Thornburg, K., & Barker, D. J. P. (2010) · American Journal of Human Biology · doi:10.1002/ajhb.20995 · Cited by 590 · see citing works
Self-citationJansson, T., & Powell, T. L. (2007) · Clinical Science · doi:10.1042/cs20060339 · Cited by 542 · see citing works
Forsen, T., Eriksson, J. G., Tuomilehto, J., Osmond, C., & Barker, D. J. P. (1999) · BMJ · doi:10.1136/bmj.319.7222.1403 · Cited by 481 · see citing works
Self-citationDoes fetal sex affect pregnancy outcome?
Renzo, G. C. D., Rosati, A., Sarti, R. D., Cruciani, L., & Cutuli, A. M. (2007) · Gender Medicine · doi:10.1016/s1550-8579(07)80004-0 · Cited by 447 · see citing works
Alexander, J. R., & Tanner, J. M. (1979) · Biometrics · doi:10.2307/2530274 · Cited by 395 · see citing works
The Role of the Placenta in Fetal Programming—A Review
Godfrey, K. M. (2002) · Placenta · doi:10.1053/plac.2002.0773 · Cited by 305 · see citing works
The effect of maternal anaemia and iron deficiency on the ratio of fetal weight to placental weight
Godfrey, K. M., Redman, C. W. G., Barker, D. J. P., & Osmond, C. (1991) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1991.tb13510.x · Cited by 301 · see citing works
Self-citationGender aspects of preterm birth
Ingemarsson, I. (2003) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1016/s1470-0328(03)00022-3 · Cited by 240 · see citing works
Gender aspects of preterm birth
Ingemarsson, I. (2003) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1046/j.1471-0528.2003.00022.x · Cited by 222 · see citing works
The surface area of the placenta and hypertension in the offspring in later life
Barker, D. J. P., Thornburg, K. L., Osmond, C., Kajantie, E., & Eriksson, J. G. (2010) · The International Journal of Developmental Biology · doi:10.1387/ijdb.082760db · Cited by 212 · see citing works
Self-citationCompensatory placental growth after restricted maternal nutrition in early pregnancy
Lunney, L. H. (1998) · Placenta · doi:10.1016/s0143-4004(98)90105-9 · Cited by 164 · see citing works
THE WEIGHT OF THE PLACENTA IN RELATION TO BIRTHWEIGHT
Thomson, A. M. W., Billewicz, W. Z., & Hytten, F. E. (1969) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1969.tb15722.x · Cited by 149 · see citing works
Ultrasound evidence of sexual difference in fetal size in first trimester.
Pedersen, J. F. (1980) · BMJ · doi:10.1136/bmj.281.6250.1253 · Cited by 140 · see citing works
Maternal undernutrition during mid-pregnancy in sheep: variable effects on placental growth
McCrabb, G. J., Egan, A. R., & Hosking, B. J. (1992) · The Journal of Agricultural Science · doi:10.1017/s002185960006809x · Cited by 114 · see citing works
The Placenta and Human Developmental Programming
(2010) · Cambridge University Press eBooks · doi:10.1017/cbo9780511933806 · Cited by 105 · see citing works
In preeclampsia, the placenta grows slowly along its minor axis
Kajantie, E., Thornburg, K. L. R., Eriksson, J. G., Osmond, C., & Barker, D. J. P. (2009) · The International Journal of Developmental Biology · doi:10.1387/ijdb.082833ek · Cited by 100 · see citing works
Self-citationChanges in Placental Size during Ramadan
Alwasel, S. H., Abotalib, Z., Aljarallah, J. S., Osmond, C., Alkharaz, S. M., Alhazza, I. M., Badr, G., & Barker, D. J. P. (2010) · Placenta · doi:10.1016/j.placenta.2010.04.010 · Cited by 92 · see citing works
Self-citationThe significance of placental/fetal weight ratios
Little, W. A. (1960) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(60)90372-0 · Cited by 60 · see citing works
Human Physiology: Age, Stress, and the Environment
(1994) · doi:10.1093/oso/9780192622655.001.0001 · Cited by 23 · see citing works
Flagged first, then by citations
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
Maternal–Fetal Nutrient Transport in Pregnancy Pathologies: The Role of the Placenta
Brett, K., Ferraro, Z. M., Yockell‐Lelièvre, J., Gruslin, A., & Adamo, K. B. (2014) · International Journal of Molecular Sciences · doi:10.3390/ijms150916153 · Cited by 459 · see citing works
“During the Dutch famine, babies who were exposed in mid to late gestation had less efficient placentas (birth weight adjusted for placenta area), in contrast, babies exposed in early gestation or who were conceived after the famine had ended had efficient placentas [114].”
BackgroundSex and gender differences in developmental programming of metabolism
Dearden, L., Bouret, S. G., & Ozanne, S. E. (2018) · Molecular Metabolism · doi:10.1016/j.molmet.2018.04.007 · Cited by 353 · see citing works
Gabory, A., Roseboom, T. J., Moore, T., Moore, L. G., & Junien, C. (2013) · Biology of Sex Differences · doi:10.1186/2042-6410-4-5 · Cited by 344 · see citing works
“Famine in mid to late gestation made the placenta less efficient as indicated by being born lighter than predicted from placental area, but more efficient when the famine occurred in early gestation or for conceptuses conceived after the famine had ended, since such babies were heavier than predicted [20].”
Self-citationTarrade, A., Panchenko, P., Junien, C., & Gabory, A. (2015) · Journal of Experimental Biology · doi:10.1242/jeb.110320 · Cited by 251 · see citing works
“The effect on the placental area was more severe for boys than girls (Roseboom et al., 2011).”
BackgroundPrenatal stress and epigenetics
Cao-Lei, L., de Rooij, S. R., King, S., Matthews, S. G., Metz, G. A. S., Roseboom, T. J., & Szyf, M. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.05.016 · Cited by 230 · see citing works
Self-citationReview: Sexual dimorphism in the formation, function and adaptation of the placenta
Kalisch-Smith, J. I., Simmons, D. G., Dickinson, H., & Moritz, K. M. (2016) · Placenta · doi:10.1016/j.placenta.2016.12.008 · Cited by 171 · see citing works
Prenatal influences on temperament development: the role of environmental epigenetics
Gartstein, M. A., & Skinner, M. K. (2018) · Development and Psychopathology · doi:10.1017/s0954579417001730 · Cited by 161 · see citing works
Wallace, J. M., Horgan, G. W., & Bhattacharya, S. (2012) · Placenta · doi:10.1016/j.placenta.2012.05.006 · Cited by 163 · see citing works
Nelissen, E. C. M., Dumoulin, J. C. M., Daunay, A., Evers, J. L. H., Tost, J., & van Montfoort, A. P. A. (2013) · Human Reproduction · doi:10.1093/humrep/des459 · Cited by 147 · see citing works
Kavitha, J., Rosario, F. J., Nijland, M. J., McDonald, T. J., Wu, G., Kanai, Y., Powell, T. L., Nathanielsz, P. W., & Jansson, T. (2013) · The FASEB Journal · doi:10.1096/fj.13-242271 · Cited by 131 · see citing works
“Babies who were in utero during the wartime famine in the winter of 1944–1945 in Holland (the Dutch famine cohort) were moderately growth restricted and showed increased incidence of obesity and metabolic and cardiovascular disease in adulthood (77), demonstrating that maternal nutrition during gestation has important…”
BackgroundThe sex-specific effects of famine on the association between placental size and later hypertension
van Abeelen, A. F. M., de Rooij, S. R., Osmond, C., Painter, R. C., Veenendaal, M. V. E., Bossuyt, P. M. M., Elias, S. G., Grobbee, D. E., van der Schouw, Y. T., Barker, D. J. P., et al. (2011) · Placenta · doi:10.1016/j.placenta.2011.06.012 · Cited by 114 · see citing works
“They grow faster than girls from an early stage of gestation [18], and they invest less in placentation [16,17,22].”
BackgroundSelf-citationThe placenta is the center of the chronic disease universe
Thornburg, K. L. R., & Marshall, N. (2015) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2015.08.030 · Cited by 116 · see citing works
The programming of cardiovascular disease
Thornburg, K. L. R. (2015) · Journal of Developmental Origins of Health and Disease · doi:10.1017/s2040174415001300 · Cited by 113 · see citing works
Reconciling the nutritional and glucocorticoid hypotheses of fetal programming
Cottrell, E. C., Holmes, M. C., Livingstone, D. E., Kenyon, C. J., & Seckl, J. R. (2012) · The FASEB Journal · doi:10.1096/fj.12-203489 · Cited by 102 · see citing works
“placental size at term (21), which correlate with re-”
BackgroundCuffe, J. S. M., O’Sullivan, L., Simmons, D. G., Anderson, S. T., & Moritz, K. M. (2012) · Endocrinology · doi:10.1210/en.2012-1479 · Cited by 97 · see citing works
“Famine during pregnancy has been shown to either increase or decrease placental thickness depending on the timing of the insult as well as the sex of the fetus (31).”
BackgroundPlacental adaptations supporting fetal growth during normal and adverse gestational environments
Sferruzzi-Perri, A. N., López‐Tello, J., & Salazar‐Petres, E. (2022) · Experimental Physiology · doi:10.1113/ep090442 · Cited by 104 · see citing works
Roland, M. C. P., Friis, C. M., Godang, K., Bollerslev, J., Haugen, G. N., & Henriksen, T. (2014) · PLoS ONE · doi:10.1371/journal.pone.0087303 · Cited by 95 · see citing works
“Data from pregnancies during the Dutch famine showed that placental area was reduced [20].”
BackgroundResource allocation in utero and health in later life
Barker, D. J. P., Lampl, M., Roseboom, T., & Winder, N. (2012) · Placenta · doi:10.1016/j.placenta.2012.06.009 · Cited by 81 · see citing works
Self-citationReijnders, I. F., Mulders, A. G. M. G. J., van der Windt, M., Steegers, E. A. P., & Steegers‐Theunissen, R. P. M. (2018) · Human Reproduction Update · doi:10.1093/humupd/dmy037 · Cited by 68 · see citing works
de 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
“In babies who were in mid–late gestation during the famine, the placenta was less efficient and in babies who were in early gestation during the famine, or who were conceived after the famine had ended, the placenta was more efficient (Roseboom et al. 2011).”
BackgroundSelf-citationIntergenerational Health Responses to Adverse and Enriched Environments
Bygren, L. O. (2013) · Annual Review of Public Health · doi:10.1146/annurev-publhealth-031912-114419 · Cited by 57 · see citing works
Zhao, Y., Zhou, Y., Zhu, Q., Xia, B., Ma, W., Xiao, X., Shi, H., & Zhang, Y. (2018) · Environment International · doi:10.1016/j.envint.2018.11.053 · Cited by 57 · see citing works
The breadth of the placental surface but not the length is associated with body size at birth
Alwasel, S. H., Abotalib, Z. M., Aljarallah, J. S., Osmond, C., Alomar, S. Y., Harrath, A. H., Thornburg, K. L. R., & Barker, D. J. (2012) · Placenta · doi:10.1016/j.placenta.2012.04.015 · Cited by 50 · see citing works
Self-citationCox, L. A., Li, C., Glenn, J. P., Lange, K. J., Spradling, K. D., Nathanielsz, P. W., & Jansson, T. (2013) · Journal of Nutrition · doi:10.3945/jn.112.172148 · Cited by 47 · see citing works
Yang, X., Hu, R., Shi, M., Wang, L., Yan, J., Gong, J., Zhang, Q.-J., He, J., & Wu, S. (2023) · Antioxidants · doi:10.3390/antiox12020360 · Cited by 44 · see citing works
“The placenta serves as the vital link between the fetal and the maternal circulations, sustaining pregnancy and embryonic development and growth by facilitating the transfer of nutrients and waste, contributing to immunological response, and acting as an endocrine organ [11,12].”
BackgroundPlacenta-Imprinted Gene Expression Association of Infant Neurobehavior
Marsit, C. J., Lambertini, L., Maccani, M. A., Koestler, D. C., Houseman, E. A., Padbury, J. F., Lester, B. M., & Chen, J. (2011) · The Journal of Pediatrics · doi:10.1016/j.jpeds.2011.10.028 · Cited by 44 · see citing works
“There is growing interest in the molecular mechanisms which underlie the epidemiologic observations of the developmental origins of health and disease, as well as a focus of study on the critical role of the placenta in mediating these effects[16, 28, 29].”
BackgroundCapellini, I. (2012) · Placenta · doi:10.1016/j.placenta.2012.07.004 · Cited by 42 · see citing works
Maternal Nutrition and Fetal/Infant Development
Jain, S., Maheshwari, A., & Jain, S. K. (2022) · Clinics in Perinatology · doi:10.1016/j.clp.2022.02.005 · Cited by 41 · see citing works
Placental Size Is Associated with Mental Health in Children and Adolescents
Khalife, N., Glover, V. A. S., Hartikainen, A., Taanila, A. M., Ebeling, H. E., Järvelin, M., & Rodriguez, A. (2012) · PLoS ONE · doi:10.1371/journal.pone.0040534 · Cited by 40 · see citing works
“Variation in the size of the placenta affects aspects of its function, in particular the ability to transfer nutrients to the fetus via changes in the exchange surface area [34]; in general, small placentas are associated with small fetuses [35].”
Hyperemesis gravidarum and placental dysfunction disorders
Koudijs, H. M., Savitri, A. I., Browne, J. L., Amelia, D., Baharuddin, M., Grobbee, D. E., & Uiterwaal, C. S. P. M. (2016) · BMC Pregnancy and Childbirth · doi:10.1186/s12884-016-1174-7 · Cited by 36 · see citing works
“Studies on famine and placental weight and PW/BW ratio suggest that with low caloric intake, the placenta compensatorily grows, probably to maintain adequate fetal nutrition [31, 32].”
Effects of Prenatal Nutrition and the Role of the Placenta in Health and Disease
Myatt, L., & Thornburg, K. L. R. (2018) · Methods in molecular biology · doi:10.1007/978-1-4939-7614-0_2 · Cited by 36 · see citing works
Pregnancies in Diabetes and Obesity: The Capacity-Load Model of Placental Adaptation
Desoyé, G., & Wells, J. C. K. (2021) · Diabetes · doi:10.2337/db20-1111 · Cited by 33 · see citing works
“Such sex differences are also apparent during maternal undernutrition, as shown in the Dutch famine, where exposure early in gestation was associated with a greater reduction in placental area in boys than girls (47).”
BackgroundDisgust in pregnancy and fetus sex—Longitudinal study
Żelaźniewicz, A., & Pawłowski, B. (2014) · Physiology & Behavior · doi:10.1016/j.physbeh.2014.11.032 · Cited by 31 · see citing works
“As reduction of caloric intake and dietary impoverishment during pregnancy, may impact maternal and fetal health in a variety of ways [10], to minimize the cost it would be adaptive to lower disgust sensitivity as soon as it is possible (i.”
BackgroundThe importance of maternal nutrition for health
Cetin, I., & Laoreti, A. (2015) · Journal of pediatric and neonatal individualized medicine · doi:10.7363/040220 · Cited by 31 · see citing works
“Babies in early gestation during the famine, or conceived after the famine end, had higher birthweights suggesting increased placental efficiency due to compensatory mechanisms (increased placental mass, surface and transport) [40-42].”
BackgroundEkström, E., Lindström, E., Raqib, R., Arifeen, S. E., Basu, S., Brismar, K., Selling, K. E., & Persson, L. Å. (2016) · International Journal of Epidemiology · doi:10.1093/ije/dyw199 · Cited by 30 · see citing works
“6) Parity 0 402 (30) 126 (40) 210 (31) 192 (29) 129 (29) 143 (32) 130 (28) 1 358 (27) 84 (27) 170 (25) 188 (28) 122 (28) 113 (25) 123 (27) 2 591 (44) 106 (34) 302 (44) 289 (43) 188 (43) 198 (44) 205 (45) Schooling (years) 0 500 (37) 90 (29) 256 (38) 244 (37) 173 (39) 160 (35) 167 (37) 1–4 139 (10) 44 (14) 73 (11) 139…”
The Placenta’s Role in Sexually Dimorphic Fetal Growth Strategies
Christians, J. K. (2021) · Reproductive Sciences · doi:10.1007/s43032-021-00780-3 · Cited by 28 · see citing works
Human growth and chronic disease: A memorial to Jim Tanner
Barker, D. J. P. (2012) · Annals of Human Biology · doi:10.3109/03014460.2012.712717 · Cited by 24 · see citing works
“Follow-up studies of people who were in utero during the war-time famine in Holland have shown q Informa UK, Ltd. that, although the babies’ birthweights were little affected, severe maternal caloric restriction at different stages of pregnancy was variously associated with obesity, dyslipidemia, insulin resistance an…”
BackgroundSelf-citationWiden, E. M., Nichols, A. R., Kahn, L. G., Factor-Litvak, P. R., Insel, B. J., Hoepner, L., Dube, S., Rauh, V., Perera, F. P., & Rundle, A. (2019) · BMC Pediatrics · doi:10.1186/s12887-019-1853-4 · Cited by 23 · see citing works
Placental mTOR Signaling and Sexual Dimorphism in Metabolic Health across the Lifespan of Offspring
Beetch, M., & Alejandro, E. U. (2021) · Children · doi:10.3390/children8110970 · Cited by 22 · see citing works
“The effect of MNR during the Dutch Famine on the placental area was more severe for male offspring compared to female [52].”
BackgroundUmbilical cord blood PBDEs concentrations in relation to placental size at birth
Zhao, Y. M., Song, Q., Cao, Z., Su, X., Hua, J., Zhang, Y., & He, X. (2018) · Chemosphere · doi:10.1016/j.chemosphere.2018.02.121 · Cited by 22 · see citing works
Christians, J. K., & Chow, N. A. (2022) · Journal of Developmental Origins of Health and Disease · doi:10.1017/s2040174422000204 · Cited by 21 · see citing works
Placental transcriptomic signatures of prenatal and preconceptional maternal stress
Baker, B. H., Freije, S. L., MacDonald, J. W., Bammler, T. K., Benson, C., Carroll, K. N., Enquobahrie, D. A., Karr, C. J., LeWinn, K. Z., Zhao, Q., et al. (2024) · Molecular Psychiatry · doi:10.1038/s41380-023-02403-6 · Cited by 20 · see citing works
“For instance, phenotypes related to the ef fi ciency of placental transfer, including weight, thickness, surface area, and the ratio of placental to fetal weight have been linked to both maternal nutrition [17, 18] and offspring coronary heart disease [19, 20].”
BackgroundPlacental Development and Nutritional Environment
Taniguchi, K., Kawai, T., & Hata, K. (2018) · Advances in experimental medicine and biology · doi:10.1007/978-981-10-5526-3_7 · Cited by 20 · see citing works
Barapatre, N., Haeussner, E., Grynspan, D., Schmitz, C., von Koch, F. E., & Frank, H. (2019) · Scientific Reports · doi:10.1038/s41598-019-38739-9 · Cited by 16 · see citing works
Fetal sex and risk of preeclampsia: Dose maternal race matter?
Mirzakhani, H., & Weiss, S. T. (2020) · The Journal of Maternal-Fetal & Neonatal Medicine · doi:10.1080/14767058.2020.1818221 · Cited by 16 · see citing works
“[13,39] [41,42] Fetuses with in-utero exposure to the Dutch famine showed sex-specific adaptations and compensatory expansion of the placental surface that was associated with hypertension in male offspring later in life.[43,44] Maternal obesity could result in sexspecific placental pathologies, with females to be at…”
BackgroundZhang, K.-D., Jia, X., Yu, W., Cheng, X., Li, Y.-Q., Wang, X., Wang, J., Li, Z., Mao, Y.-C., Zhao, J., et al. (2023) · BMC Pregnancy and Childbirth · doi:10.1186/s12884-023-05991-x · Cited by 16 · see citing works
“Research conducted by Alwasel et al. and Roseboom et al. [33, 34] identified diet as a factor affecting placental efficiency; however, our research did not gather data on the dietary habits of expectant mothers.”
ResultVandraas, K. F., Vikanes, Å. V., Støer, N. C., Vangen, S., Magnus, P. M., & Grjibovski, A. M. (2013) · Placenta · doi:10.1016/j.placenta.2013.08.001 · Cited by 15 · see citing works
Dimas, A., Politi, A., Papaioannou, G., Barber, T. M., Weickert, M. O., Grammatopoulos, D. K., Kumar, S., Kalantaridou, S., & Valsamakis, G. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23020695 · Cited by 13 · see citing works
Lindström, E., Persson, L. Å., Raqib, R., Arifeen, S. E., Basu, S., & Ekström, E. (2012) · Free Radical Research · doi:10.3109/10715762.2011.651467 · Cited by 12 · see citing works
Morphometry Examination of Placenta in Birth Weight of Full-Term Newborns in Puducherry, India
Kowsalya, V., Vijayakuma, R., Valli, G., Bharath, K. P., SRIKUMAR, R., Kumar, C. K., Fathima, I. G., & Vanajashi, N. (2013) · Pakistan Journal of Biological Sciences · doi:10.3923/pjbs.2013.895.897 · Cited by 10 · see citing works
Placental–Heart Axis: An Evolutionary Perspective
Matthews, J., Rajakumar, B., Carreon, C. K., & Morton, S. U. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms252011212 · Cited by 10 · see citing works
“Famine and periods of scarcity can similarly affect both the placenta and fetus [74].”
BackgroundGriffith, J. A., Dunn, A., DeVallance, E., Schafner, K. J., Engles, K. J., Batchelor, T., Goldsmith, W. T., Wix, K., Hussain, S., Bowdridge, E. C., et al. (2023) · Frontiers in Toxicology · doi:10.3389/ftox.2023.1096173 · Cited by 8 · see citing works
“Undernutrition in mid to late gestation caused a sex-based difference, with increased placental thickness in female fetuses compared to males (Roseboom et al., 2011).”
BackgroundSletner, L., Yajnik, C. S., Turowski, G. E., Michelsen, T. M., Sommer, C., Birkeland, K. I., Roald, B., & Jenum, A. K. (2024) · Placenta · doi:10.1016/j.placenta.2024.02.002 · Cited by 7 · see citing works
Svensson, K., Gennings, C., Hagenäs, L., Wolk, A., Håkansson, N., Wikström, S., & Bornehag, C. (2023) · British Journal Of Nutrition · doi:10.1017/s0007114523000983 · Cited by 6 · see citing works
“Results from the Dutch famine show that exposure to famine in early gestation had a greater effect on the placental size for boys (83) , as well as greater risk for CHD in adulthood (87) .”
Sangalli, J. R., Nociti, R. P., Chiaratti, M. R., Bridi, A., Botigelli, R. C., Ambrizi, D. R., Saraiva, H. F. R. D. A., Perecin, F., da Silveira, J. C., Ross, P. J., et al. (2024) · Biology of Reproduction · doi:10.1093/biolre/ioae175 · Cited by 5 · see citing works
“…undernutrition thus far, common phenotypes are always present, such as delayed embryonic development, reduced placenta and fetal growth, stunted offspring, abnormal skeletal muscle and cardiovascular development, metabolic alterations, and aberrant DNA methylation patterns [24, 25, 59–61].”
Maternal dietary patterns and placental outcomes among pregnant women in Los Angeles
Meng, Q., Rosario, I. D., Sung, K., Janzen, C., Devaskar, S. U., Carpenter, C. L., & Ritz, B. R. (2023) · Placenta · doi:10.1016/j.placenta.2023.12.002 · Cited by 4 · see citing works
David James Purslove Barker. 29 June 1938—27 August 2013
Barker, M. E., Fall, C. H. D., Osmond, C., Cooper, C. C., Fleming, T. P., Thornburg, K. L. R., & Burton, G. J. (2019) · Biographical Memoirs of Fellows of the Royal Society · doi:10.1098/rsbm.2019.0021 · Cited by 4 · see citing works
Self-citationMitsuda, N., Eitoku, M., Yamasaki, K., J-P, N. A., Fujieda, M., Suganuma, N., Kamijima, M., Yamazaki, S., Ohya, Y., Kishi, R., et al. (2022) · Placenta · doi:10.1016/j.placenta.2022.08.007 · Cited by 4 · see citing works
Perinatal Programming and Blood Pressure
Kallash, M., Ingelfinger, J. R., & Vehaskari, V. M. (2013) · Humana Press eBooks · doi:10.1007/978-1-62703-490-6_7 · Cited by 4 · see citing works
Yıldırım, S. B., Can, Ö. K., Tekin, E., Akoğlu, H. A., & Bulut, M. (2025) · Nutrition Bulletin · doi:10.1111/nbu.70019 · Cited by 2 · see citing works
“…have suggested that placental efficiency is influenced by the food intake during religious fasting or famine in pregnancy (Alwasel et al. 2010; Roseboom et al. 2011), a recent review reported that there is no strong evidence supporting an association between Ramadan fasting during pregnancy…”
Kubler, J. M., Beetham, K. S., Steane, S. E., Holland, O. J., Borg, D. J., Rae, K. M., Kumar, S., & Clifton, V. L. (2024) · Placenta · doi:10.1016/j.placenta.2024.12.027 · Cited by 2 · see citing works
Placentation as a Predictor of Feto-Placental Outcome: Effects of Early Nutrition
Duttaroy, A. K., & Basak, S. (2016) · Springer eBooks · doi:10.1007/978-3-319-38804-5_1 · Cited by 2 · see citing works
Nasralla, K., Kheiri, S. A., Kunna, A., Saadia, Z., Ali, A. O., & Alsammani, M. (2020) · Materia Socio Medica · doi:10.5455/msm.2020.32.196-199 · Cited by 2 · see citing works
Impact of anaemia in pregnancy on maternal and fetal wellbeing in Oman: a retrospective study
Gimono, P., Aljezawi, M., Alkhawaldeh, A., ALBashtawy, M., Salameh, B. S., Batran, A., Ayed, A., Khalifeh, A. H., Oweidat, I. A., Rababa, M., et al. (2024) · British Journal of Midwifery · doi:10.12968/bjom.2024.0036 · Cited by 1 · see citing works
Early Life Origins of Severe Personality Disorders: The Helsinki Birth Cohort Study
Lahti‐Pulkkinen, M. (2012) · Työväentutkimus Vuosikirja · Cited by 1 · see citing works
Nutrition and Pregnancy Outcomes
Bellissimo, C. J., Vickers, M. H., & Sloboda, D. M. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-801238-3.64688-3 · Cited by 1 · see citing works
The Significance of Gender in Perinatal Medicine
Hadley, K., & Sheiner, E. (2017) · Principles of Gender-Specific Medicine · doi:10.1016/b978-0-12-803506-1.00018-8
Kalisch-Smith, J. I. (2017) · The University of Queensland · doi:10.14264/uql.2017.1051
In utero undernourishment during WWII: Effects on height and weight of young adult women
Czapla, Z., Liczbińska, G., Piontek, J., & Malina, R. M. (2020) · Anthropological Review · doi:10.2478/anre-2020-0004
The Role of the Placenta in DOHaD
Lewis, R. M., & Sferruzzi-Perri, A. N. (2022) · Cambridge University Press eBooks · doi:10.1017/9781009272254.017
Sex-specific associations between birthweight and objectively measured energy intake in adulthoodPreprint
Guerithault, N., Stinson, E. J., de Baca, T. C., Looker, H. C., Votruba, S. B., Piaggi, P., Gluck, M. E., Krakoff, J. A., & Chang, D. C. (2023) · Research Square · doi:10.21203/rs.3.rs-2518158/v1
O’Callaghan, J. L. (2023) · Queensland University of Technology · doi:10.5204/thesis.eprints.244719
Guerithault, N., Stinson, E. J., de Baca, T. C., Looker, H. C., Votruba, S. B., Piaggi, P., Gluck, M. E., Krakoff, J. A., & Chang, D. C. (2024) · Appetite · doi:10.1016/j.appet.2024.107334
Nutrition and Pregnancy Outcomes
Bellissimo, C. J., Vickers, M. H., & Sloboda, D. M. (2024) · Elsevier eBooks · doi:10.1016/b978-0-443-21477-6.00199-1
IS THERE A RELATION BETWEEN CHORION FRONDOSUM THICKNESS AND SEVERE HYPEREMESIS GRAVIDARUM?
Arı, S. A., Karaca, I. O., & Şahin, Ç. (2025) · Archives of Current Medical Research · doi:10.47482/acmr.1608827
Ejeguo, A., & Sakpa, C. L. (2025) · Drug Discovery · doi:10.54905/disssi.v19i43.e2dd2017
Zhang, K., Jia, X., Yu, W., Cheng, X., Li, Y., Wang, X., Wang, J., Li, Z., Mao, Y., Zhao, J., et al. (2023) · Figshare · doi:10.6084/m9.figshare.24295703
Arcot, A., Gallagher, K., Goldstein, J. A., & Gernand, A. D. (2026) · PLoS ONE · doi:10.1371/journal.pone.0325415
“Past literature has reported differences in placental size by infant sex, during famine, and periods of fasting (i.e., Ramadan) with contradicting results [86,87].”
Arcot, A., Gallagher, K., Goldstein, J. A., & Gernand, A. D. (2026) · American Journal of Clinical Nutrition · doi:10.1016/j.ajcnut.2026.101280
Small placental size is common in stillbirths, including unexplained late-gestation stillbirths
Cheng, M., Marsden, T., Warrilow, K., Sexton, J. K., Coory, M. D., Gordijn, S. J., Kumar, S., Flenady, V., & Khong, T. Y. (2026) · Journal of Perinatal Medicine · doi:10.1515/jpm-2026-0349
- Authors
- Roseboom, T. J., Painter, R. C., de Rooij, S. R., van Abeelen, A. F. M., Veenendaal, M. V. E., Osmond, C., & Barker, D. J. P.
- Affiliations
- Amsterdam UMC Location University of Amsterdam (NL)
- Southampton General Hospital (GB)
- Corresponding author
- Roseboom, T.J.
- Venue
- Placenta
- Publisher
- Elsevier BV
- Published
- 2011-05
- Volume
- 32
- Issue
- 5
- Pages
- 395-399
- ISSN
- 0143-4004 (ISSN-L)
- OpenAlex
- W1998987314
- Cited by
- 84
- References
- 20
- Citations by year
- 2026: 3 · 2025: 3 · 2024: 8 · 2023: 8 · 2022: 7 · 2021: 4 · 2020: 3 · 2019: 3 · 2018: 6 · 2017: 5 · 2016: 5 · 2015: 6 · 2014: 3 · 2013: 8 · 2012: 10
- FWCI
- 6.75
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Placenta (publishedVersion)
- PubMed (publishedVersion)
- Pure Amsterdam UMC (publishedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- ePrints Soton (University of Southampton) (submittedVersion)
- Topics
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Health Sciences › Medicine › Obstetrics and Gynecology › Pregnancy and preeclampsia studies
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Prenatal Substance Exposure Effects
- Keywords
- famine, placental size, placental efficiency, fetal growth, maternal diet, pregnancy timing, sex differences, birth weight, placental volume
- MeSH terms
- Birth Weight, Female, Humans, Infant, Newborn, Male, Netherlands, Organ Size, Placentation, Pregnancy, Pregnancy Complications, Sex Characteristics, Starvation, History, 20th Century
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
