Origins of lifetime health around the time of conception: causes and consequences
Open accessAbstract
Parental environmental factors, including diet, body composition, metabolism, and stress, affect the health and chronic disease risk of people throughout their lives, as captured in the Developmental Origins of Health and Disease concept. Research across the epidemiological, clinical, and basic science fields has identified the period around conception as being crucial for the processes mediating parental influences on the health of the next generation. During this time, from the maturation of gametes through to early embryonic development, parental lifestyle can adversely influence long-term risks of offspring cardiovascular, metabolic, immune, and neurological morbidities, often termed developmental programming. We review periconceptional induction of disease risk from four broad exposures: maternal overnutrition and obesity; maternal undernutrition; related paternal factors; and the use of assisted reproductive treatment. Studies in both humans and animal models have demonstrated the underlying biological mechanisms, including epigenetic, cellular, physiological, and metabolic processes. We also present a meta-analysis of mouse paternal and maternal protein undernutrition that suggests distinct parental periconceptional contributions to postnatal outcomes. We propose that the evidence for periconceptional effects on lifetime health is now so compelling that it calls for new guidance on parental preparation for pregnancy, beginning before conception, to protect the health of offspring.
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?
These processes are vulnerable to disturbance of epigenetic mechanisms, leading to an altered profile of embryonic gene expression that persists throughout both pregnancy and childhood.
“These processes are vulnerable to disturbance of epigenetic mechanisms, leading to an altered profile of embryonic gene expression that persists throughout both pregnancy and childhood [9].”
From Associations between periconceptional lifestyle behaviours and adverse pregnancy outcomes (2021) · cites this paper as [9]
The Periconceptional developmental programming and ART section says embryo culture can alter gene expression and epigenetic patterns, and that ART-induced epigenetic profiles may persist through pregnancy into childhood. But it does not establish that an altered profile of embryonic gene expression itself persists for that period. The Diversity and commonality subsection cautions that epigenetic changes are not necessarily linked directly to changes in gene expression. (LLM, conf=0.88)
Experimental — accuracy not yet measuredThe risk of developing chronic inflammation can be traced to early development, and its effects persist across the life span to influence adult health and mortality risk.
“Evidence is emerging that the risk of developing chronic inflammation can be traced back to early development, and its effects are now known to persist throughout the life span to affect adulthood health and risk of mortality6–8.”
From Chronic inflammation in the etiology of disease across the life span (2019) · cites this paper as [7]
Systemic chronic inflammation during pregnancy and childhood can elevate the risk of non-communicable diseases across the life span.
“SCI during pregnancy and childhood can have serious developmental consequences that include elevating the risk of non-communicable diseases over the life span7,8,26,27.”
From Chronic inflammation in the etiology of disease across the life span (2019) · cites this paper as [7]
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
Sperm tsRNAs contribute to intergenerational inheritance of an acquired metabolic disorder
Chen, Q., Yan, M., Cao, Z., Li, X., Zhang, Y., Shi, J., Feng, G.-H., Peng, H., Zhang, X., Zhang, Y., et al. (2016) · Science · doi:10.1126/science.aad7977 · Cited by 1,470 · see citing works
Chronic high-fat diet in fathers programs β-cell dysfunction in female rat offspring
Ng, S.-F., Lin, R. C. Y., Laybutt, D. R., Barres, R., Owens, J. A., & Morris, M. J. (2010) · Nature · doi:10.1038/nature09491 · Cited by 1,327 · see citing works
Biogenesis and function of tRNA fragments during sperm maturation and fertilization in mammals
Sharma, U., Conine, C. C., Shea, J. M., Boskovic, A., Derr, A. G., Bing, X. Y., Belleannee, C., Kucukural, A., Serra, R. W., Sun, F., et al. (2016) · Science · doi:10.1126/science.aad6780 · Cited by 1,275 · see citing works
Early Developmental Conditioning of Later Health and Disease: Physiology or Pathophysiology?
Hanson, M. A., & Gluckman, P. D. (2014) · Physiological Reviews · doi:10.1152/physrev.00029.2013 · Cited by 1,188 · see citing works
Self-citationCarone, B. R., Fauquier, L., Habib, N., Shea, J. M., Hart, C. E., Li, R., Bock, C., Li, C., Gu, H., Zamore, P. D., et al. (2010) · Cell · doi:10.1016/j.cell.2010.12.008 · Cited by 1,157 · see citing works
Lillycrop, K. A., Phillips, E. S., Jackson, A. A., Hanson, M. A., & Burdge, G. C. (2005) · Journal of Nutrition · doi:10.1093/jn/135.6.1382 · Cited by 1,139 · see citing works
Self-citationInfluence of Maternal Obesity on the Long-Term Health of Offspring
Godfrey, K. M., Reynolds, R. M., Prescott, S. L., Nyirenda, M., Jaddoe, V. W. V., Eriksson, J. G., & Broekman, B. F. P. (2017) · The Lancet Diabetes & Endocrinology · doi:10.1016/s2213-8587(16)30107-3 · Cited by 1,059 · see citing works
Self-citationSamuelsson, A.-M., Matthews, P. A., Argenton, M., Christie, M. R., McConnell, J. M., Jansen, E. H. J. M., Piersma, A. H., Ozanne, S. E., Twinn, D. F., Remacle, C., et al. (2008) · Hypertension · doi:10.1161/hypertensionaha.107.101477 · Cited by 923 · see citing works
Sinclair, K. D., Allegrucci, C., Singh, R., Gardner, D. S., Sebastian, S., Bispham, J., Thurston, A., Huntley, J. F., Rees, W. D., Maloney, C. A., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0707258104 · Cited by 812 · see citing works
Kwong, W. Y., Wild, A. E., Roberts, P., Willis, A. C., & Fleming, T. P. (2000) · Development · doi:10.1242/dev.127.19.4195 · Cited by 798 · see citing works
Self-citationDNA methylation dynamics during epigenetic reprogramming in the germline and preimplantation embryosPreprint
Messerschmidt, D. M., Knowles, B. B., & Solter, D. (2014) · Genes & Development · doi:10.1101/gad.234294.113 · Cited by 734 · see citing works
The Obstetric Origins of Health for a Lifetime
BARKER, D. J. P., & THORNBURG, K. L. (2013) · Clinical Obstetrics & Gynecology · doi:10.1097/grf.0b013e31829cb9ca · Cited by 634 · see citing works
DNA methylation signatures link prenatal famine exposure to growth and metabolism
Tobi, E. W., Goeman, J. J., Monajemi, R., Gu, H., Putter, H., Zhang, Y., Slieker, R. C., Stok, A. P., Thijssen, P. E., Müller, F., et al. (2014) · Nature Communications · doi:10.1038/ncomms6592 · Cited by 630 · see citing works
Impact of Body Mass Index Values on Sperm Quantity and Quality
Kort, H. I., Massey, J. B., Elsner, C. W., Mitchell‐Leef, D., Shapiro, D. B., Witt, M. A., & Roudebush, W. E. (2006) · Journal of Andrology · doi:10.2164/jandrol.05124 · Cited by 617 · see citing works
Fullston, T., Teague, E. M. C. O., Palmer, N. O., DeBlasio, M. J., Mitchell, M., Corbett, M., Print, C. G., Owens, J. A., & Lane, M. (2013) · The FASEB Journal · doi:10.1096/fj.12-224048 · Cited by 600 · see citing works
Khosla, S., Dean, W., Brown, D., Reik, W., & Feil, R. (2001) · Biology of Reproduction · doi:10.1095/biolreprod64.3.918 · Cited by 560 · see citing works
Spermatozoal RNA profiles of normal fertile men
Ostermeier, G. C., Dix, D. J., Miller, D., Khatri, P., & Krawetz, S. A. (2002) · The Lancet · doi:10.1016/s0140-6736(02)09899-9 · Cited by 516 · see citing works
Maternal nutrition at conception modulates DNA methylation of human metastable epialleles
Dominguez-Salas, P., Moore, S. E., Baker, M. S., Bergen, A. W., Cox, S. E., Dyer, R. A., Fulford, A. J., Guan, Y., Laritsky, E., Silver, M. J., et al. (2014) · Nature Communications · doi:10.1038/ncomms4746 · Cited by 506 · see citing works
Self-citationInsulin dependant diabetes mellitus: implications for male reproductive function
Agbaje, I., Rogers, D. A., McVicar, C. M., McClure, N., Atkinson, A. B., Mallidis, C., & Lewis, S. E. M. (2007) · Human Reproduction · doi:10.1093/humrep/dem077 · Cited by 482 · see citing works
Lambrot, R., Xu, C., Saint‐Phar, S., Chountalos, G., Cohen, T. R., Paquet, M., Suderman, M. J., Hallett, M. T., & Kimmins, S. (2013) · Nature Communications · doi:10.1038/ncomms3889 · Cited by 476 · see citing works
Igosheva, N., Abramov, A. Y., Poston, L., Eckert, J. J., Fleming, T. P., Duchen, M. R., & McConnell, J. M. L. (2010) · PLoS ONE · doi:10.1371/journal.pone.0010074 · Cited by 466 · see citing works
Self-citationSeason of Conception in Rural Gambia Affects DNA Methylation at Putative Human Metastable Epialleles
Waterland, R. A., Kellermayer, R., Laritsky, E., Rayco‐Solon, P., Harris, R. A., Travisano, M., Zhang, W., Torskaya, M. S., Zhang, J., Shen, L., et al. (2010) · PLoS Genetics · doi:10.1371/journal.pgen.1001252 · Cited by 454 · see citing works
Self-citationSeli, E., Gardner, D., Schoolcraft, W., Moffatt, O. D., & Sakkas, D. (2004) · Fertility and Sterility · doi:10.1016/j.fertnstert.2003.12.039 · Cited by 420 · see citing works
Impact of stress on oocyte quality and reproductive outcome
Prasad, S., Tiwari, M., Pandey, A. N., Shrivastav, T. G., & Chaube, S. K. (2016) · Journal of Biomedical Science · doi:10.1186/s12929-016-0253-4 · Cited by 384 · see citing works
Cardiometabolic Differences in Children Born After in Vitro Fertilization: Follow-Up Study
Ceelen, M., van Weissenbruch, M. M., Vermeiden, J. P. W., van Leeuwen, F. E., & de Waal, H. A. D. (2008) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2007-2432 · Cited by 383 · see citing works
Robker, R. L., Akison, L. K., Bennett, B. D., Thrupp, P. N., Chura, L. R., Russell, D. L., Lane, M., & Norman, R. J. (2009) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2008-2648 · Cited by 382 · see citing works
Steegers-Theunissen, R. P. M., Twigt, J., Pestinger, V., & Sinclair, K. D. (2013) · Human Reproduction Update · doi:10.1093/humupd/dmt041 · Cited by 378 · see citing works
Bromfield, J. J., Schjenken, J. E., Chin, P. Y., Care, A. S., Jasper, M. J., & Robertson, S. A. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1305609111 · Cited by 374 · see citing works
Diet-Induced Obesity Model: Abnormal Oocytes and Persistent Growth Abnormalities in the Offspring
Jungheim, E. S., Schoeller, E. L., Marquard, K. L., Louden, E. D., Schaffer, J. E., & Moley, K. H. (2010) · Endocrinology · doi:10.1210/en.2010-0098 · Cited by 365 · see citing works
Luzzo, K. M., Wang, Q., Purcell, S. H., Chi, M. M.-Y., Jimenez, P. T., Grindler, N. M., Schedl, T., & Moley, K. H. (2012) · PLoS ONE · doi:10.1371/journal.pone.0049217 · Cited by 356 · see citing works
Rivera, R. M., Stein, P., Weaver, J. R., Mager, J., Schultz, R. M., & Bartolomei, M. S. (2007) · Human Molecular Genetics · doi:10.1093/hmg/ddm280 · Cited by 324 · see citing works
Scherrer, U., Rimoldi, S. F., Rexhaj, E., Stüber, T., Duplain, H., Garcin, S., de Marchi, S. F., NICOD, P. H., Germond, M., Allemann, Y., et al. (2012) · Circulation · doi:10.1161/circulationaha.111.071183 · Cited by 295 · see citing works
Sharkey, D. J., Macpherson, A. M., Tremellen, K. P., & Robertson, S. A. (2007) · Molecular Human Reproduction · doi:10.1093/molehr/gam028 · Cited by 294 · see citing works
Hammoud, S. S., Nix, D. A., Hammoud, A. O., et al. (2011) · Human Reproduction · doi:10.1093/humrep/der192 · Cited by 291 · see citing works
The effect of paternal diet‐induced obesity on sperm function and fertilization in a mouse model
Bakos, H. W., Mitchell, M., Setchell, B. P., & Lane, M. (2010) · International Journal of Andrology · doi:10.1111/j.1365-2605.2010.01092.x · Cited by 290 · see citing works
Multigenerational epigenetic adaptation of the hepatic wound-healing response
Zeybel, M., Hardy, T., Wong, Y. K., Mathers, J. C., Fox, C. R., Gackowska, A., Oakley, F., Burt, A. D., Wilson, C. L., Anstee, Q. M., et al. (2012) · Nature Medicine · doi:10.1038/nm.2893 · Cited by 279 · see citing works
Self-citationLazaraviciute, G., Kauser, M., Bhattacharya, S., Haggarty, P., & Bhattacharya, S. (2014) · Human Reproduction Update · doi:10.1093/humupd/dmu033 · Cited by 264 · see citing works
The maternal to zygotic transition in mammals
Li, L., Lu, X., & Dean, J. (2013) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2013.01.003 · Cited by 243 · see citing works
Bellver, J., Pellicer, A., García-Velasco, J. A., Ballesteros, A., Remohi, J. A., & Meseguer, M. (2013) · Fertility and Sterility · doi:10.1016/j.fertnstert.2013.06.001 · Cited by 235 · see citing works
Bakos, H. W., Henshaw, R. C., Mitchell, M., & Lane, M. (2010) · Fertility and Sterility · doi:10.1016/j.fertnstert.2010.11.044 · Cited by 230 · see citing works
Watkins, A. J., Ursell, E., Panton, R. W., Papenbrock, T., Hollis, L. J., Cunningham, C. M., Wilkins, A., Perry, V. H., Sheth, B., Kwong, W. Y., et al. (2007) · Biology of Reproduction · doi:10.1095/biolreprod.107.064220 · Cited by 227 · see citing works
Self-citationHuman embryos from overweight and obese women display phenotypic and metabolic abnormalities
Leary, C., Leese, H. J., & Sturmey, R. G. (2014) · Human Reproduction · doi:10.1093/humrep/deu276 · Cited by 223 · see citing works
Impact of body mass index on seminal oxidative stress
Tunc, O., Bakos, H. W., & Tremellen, K. P. (2010) · Andrologia · doi:10.1111/j.1439-0272.2009.01032.x · Cited by 220 · see citing works
Mouse embryo culture induces changes in postnatal phenotype including raised systolic blood pressure
Watkins, A. J., Platt, D., Papenbrock, T., Wilkins, A., Eckert, J. J., Kwong, W. Y., Osmond, C., Hanson, M. A., & Fleming, T. P. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0610317104 · Cited by 219 · see citing works
Self-citationSjöblom, C., Roberts, C. T., Wikland, M., & Robertson, S. A. (2005) · Endocrinology · doi:10.1210/en.2004-1260 · Cited by 218 · see citing works
McPherson, N. O., Bakos, H. W., Owens, J. A., Setchell, B. P., & Lane, M. (2012) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00401.2011 · Cited by 218 · see citing works
Dietary patterns and semen quality in young men
Gaskins, A. J., Colaci, D., Mendiola, J., Swan, S. H., & Chavarro, J. E. (2012) · Human Reproduction · doi:10.1093/humrep/des298 · Cited by 215 · see citing works
Yang, X., Wu, L., Chura, L. R., Liang, X., Lane, M., Norman, R. J., & Robker, R. L. (2012) · Fertility and Sterility · doi:10.1016/j.fertnstert.2012.02.034 · Cited by 206 · see citing works
Silver, M. J., Kessler, N. J., Hennig, B. J., Domínguez-Salas, P., Laritsky, E., Baker, M. S., Coarfa, C., Hernández‐Vargas, H., Castelino, J. M., Routledge, M. N., et al. (2015) · Genome biology · doi:10.1186/s13059-015-0660-y · Cited by 191 · see citing works
Self-citationWatkins, A. J., Wilkins, A., Cunningham, C. M., Perry, V. H., Seet, M. J., Osmond, C., Eckert, J. J., Torrens, C., Cagampang, F. R. A., Cleal, J. K., et al. (2008) · The Journal of Physiology · doi:10.1113/jphysiol.2007.149229 · Cited by 190 · see citing works
Self-citationSperm-derived histones contribute to zygotic chromatin in humans
van der Heijden, G. W., Ramos, L., Baart, E. B., van den Berg, I. M., Derijck, A. A. H. A., van der Vlag, J., Martini, E., & de Boer, P. (2008) · BMC Developmental Biology · doi:10.1186/1471-213x-8-34 · Cited by 181 · see citing works
Signaling in Cell Differentiation and MorphogenesisPreprint
Basson, M. A. (2012) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a008151 · Cited by 176 · see citing works
Turan, N., Katari, S., Gerson, L. F., Chalian, R. A., Foster, M., Gaughan, J., Coutifaris, C., & Sapienza, C. (2010) · PLoS Genetics · doi:10.1371/journal.pgen.1001033 · Cited by 171 · see citing works
Male-lineage transmission of an acquired metabolic phenotype induced by grand-paternal obesity
Cropley, J. E., Eaton, S. A., Aiken, A., Young, P. E., Giannoulatou, E., Ho, J. W. K., Buckland, M. E., Keam, S. P., Hutvágner, G., Humphreys, D. T., et al. (2016) · Molecular Metabolism · doi:10.1016/j.molmet.2016.06.008 · Cited by 171 · see citing works
Paternal low protein diet affects adult offspring cardiovascular and metabolic function in mice
Watkins, A. J., & Sinclair, K. D. (2014) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00981.2013 · Cited by 164 · see citing works
Self-citationQin, J., Sheng, X., Wu, D., Gao, S., You, Y., Yang, T.-B., & Wang, H. (2016) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-016-4250-3 · Cited by 163 · see citing works
Time to take human embryo culture seriously: Table I
Sunde, A., Brison, D. R., Dumoulin, J. C. M., Harper, J. C., Lundin, K., Magli, M. C., den Abbeel, E. V., & Veiga, A. (2016) · Human Reproduction · doi:10.1093/humrep/dew157 · Cited by 162 · see citing works
Gardner, D. K., & Harvey, A. J. (2015) · Reproduction Fertility and Development · doi:10.1071/rd14421 · Cited by 162 · see citing works
Valenzuela‐Alcaráz, B., Crispi, F., Bijnens, B. H., Cruz-Lemini, M., Creus, M. T., Sitges, M., Bartrons, J., Cı́vico, S., Balasch, J., & Gratacós, E. (2013) · Circulation · doi:10.1161/circulationaha.113.002428 · Cited by 161 · see citing works
Paternal diet-induced obesity impairs embryo development and implantation in the mouse
Mitchell, M., Bakos, H. W., & Lane, M. (2010) · Fertility and Sterility · doi:10.1016/j.fertnstert.2010.09.038 · Cited by 160 · see citing works
Rayco-Solon, P., Fulford, A. J., & Prentice, A. M. (2005) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/81.1.134 · Cited by 158 · see citing works
Self-citationKleijkers, S. H. M., Mantikou, E., Slappendel, E., Consten, D., van Echten‐Arends, J., Wetzels, A. M. M., van Wely, M., Smits, L. J. M., van Montfoort, A. P. A., Repping, S., et al. (2016) · Human Reproduction · doi:10.1093/humrep/dew156 · Cited by 150 · see citing works
The Early Origins of Obesity and Insulin Resistance: Timing, Programming and Mechanisms
Nicholas, L. M., Morrison, J. L., Rattanatray, L., Zhang, S., Ozanne, S. E., & McMillen, I. C. (2016) · International Journal of Obesity · doi:10.1038/ijo.2015.178 · Cited by 146 · see citing works
IVF culture medium affects post-natal weight in humans during the first 2 years of life
Kleijkers, S. H. M., van Montfoort, A. P. A., Smits, L. J. M., Viechtbauer, W., Roseboom, T. J., Nelissen, E. C. M., Coonen, E., Derhaag, J. G., Bastings, L., Schreurs, I. E. L., et al. (2014) · Human Reproduction · doi:10.1093/humrep/deu025 · Cited by 143 · see citing works
Transgenerational Inheritance of Glucose Intolerance in a Mouse Model of Neonatal Overnutrition
Pentinat, T., Ramon‐Krauel, M., Cebrià, J., Díaz, R., & Jiménez‐Chillarón, J. C. (2010) · Endocrinology · doi:10.1210/en.2010-0684 · Cited by 141 · see citing works
Kühnen, P., Handke, D., Waterland, R. A., Hennig, B. J., Silver, M. J., Fulford, A. J., Domínguez-Salas, P., Moore, S. E., Prentice, A. M., Spranger, J., et al. (2016) · Cell Metabolism · doi:10.1016/j.cmet.2016.08.001 · Cited by 132 · see citing works
Self-citationDevelopmental plasticity, cell fate specification and morphogenesis in the early mouse embryo
Bedzhov, I., Graham, S. J. L., Leung, C. Y., & Zernicka‐Goetz, M. (2014) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2013.0538 · Cited by 130 · see citing works
Differential RNAs in the sperm cells of asthenozoospermic patients
Jodar, M., Kalko, S. G., Castillo, J., et al. (2012) · Human Reproduction · doi:10.1093/humrep/des021 · Cited by 123 · see citing works
Wyman, A., Pinto, A., Sheridan, R. A., & Moley, K. H. (2007) · Endocrinology · doi:10.1210/en.2007-1273 · Cited by 122 · see citing works
Eckert, J. J., Porter, R., Watkins, A. J., Burt, E., Brooks, S., Leese, H. J., Humpherson, P. G., Cameron, I. T., & Fleming, T. P. (2012) · PLoS ONE · doi:10.1371/journal.pone.0052791 · Cited by 119 · see citing works
Self-citationNicholas, L. M., Rattanatray, L., MacLaughlin, S. M., Ozanne, S. E., Kleemann, D. O., Walker, S. K., Morrison, J. L., Zhang, S., Mühlhäusler, B. S., Martin‐Gronert, M. S., et al. (2013) · The FASEB Journal · doi:10.1096/fj.13-227918 · Cited by 115 · see citing works
Developmental biology: Support mothers to secure future public health
Barker, D. J. P., Barker, M. E., Fleming, T. P., & Lampl, M. (2013) · Nature · doi:10.1038/504209a · Cited by 106 · see citing works
Self-citationEarly-life nutrition modulates the epigenetic state of specific rDNA genetic variants in mice
Holland, M. L., Lowe, R., Caton, P. W., Gemma, C., Carbajosa, G., Danson, A. F., Carpenter, A. A. M., Loche, E., Ozanne, S. E., & Rakyan, V. K. (2016) · Science · doi:10.1126/science.aaf7040 · Cited by 106 · see citing works
Wang, P.-X., Wang, J., Lei, Y.-X., Xiao, L., & Luo, Z. (2012) · PLoS ONE · doi:10.1371/journal.pone.0049720 · Cited by 94 · see citing works
Ruebel, M. L., Cotter, M., Sims, C. R., Moutos, D. M., Badger, T. M., Cleves, M. A., Shankar, K., & Andres, A. (2017) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2016-3524 · Cited by 89 · see citing works
Hammoud, A. O., Gibson, M., Stanford, J. B., White, G. L., Carrell, D. T., & Peterson, M. (2008) · Fertility and Sterility · doi:10.1016/j.fertnstert.2007.10.038 · Cited by 87 · see citing works
Watkins, A. J., Sirovica, S., Stokes, B., Isaacs, M. A., Addison, O., & Martin, R. A. (2017) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2017.02.009 · Cited by 87 · see citing works
Self-citationWilliams, C. L., Teeling, J. L., Perry, V. H., & Fleming, T. P. (2011) · BMC Biology · doi:10.1186/1741-7007-9-49 · Cited by 85 · see citing works
Self-citationMcPherson, N. O., Fullston, T., Kang, W. X., Sandeman, L., Corbett, M. A., Owens, J. A., & Lane, M. (2016) · Scientific Reports · doi:10.1038/srep27010 · Cited by 85 · see citing works
Rumbold, A. R., Moore, V., Whitrow, M. J., Oswald, T. K., Moran, L., Fernandez, R. C., Barnhart, K. T., & Davies, M. J. (2017) · Human Reproduction · doi:10.1093/humrep/dex085 · Cited by 85 · see citing works
Fleming, T. P., Watkins, A. J., Sun, C., Velazquez, M. A., Smyth, N. R., & Eckert, J. J. (2015) · Reproduction Fertility and Development · doi:10.1071/rd14455 · Cited by 83 · see citing works
Self-citationCostello, P. M., Rowlerson, A. M., Astaman, N. A., Anthony, F. E. W., Sayer, A. A., Cooper, C. C., Hanson, M. A., & Green, L. (2008) · The Journal of Physiology · doi:10.1113/jphysiol.2008.150987 · Cited by 79 · see citing works
Self-citationHansen, P. J., Dobbs, K. B., Denicol, A. C., & Siqueira, L. G. B. (2015) · Cell and Tissue Research · doi:10.1007/s00441-015-2287-4 · Cited by 72 · see citing works
Sinclair, K. D., & Watkins, A. J. (2013) · Reproduction Fertility and Development · doi:10.1071/rd13290 · Cited by 69 · see citing works
Self-citationReproductive outcomes in oocyte donation cycles are associated with donor BMI
Cardozo, E. R., Karmon, A. E., Gold, J., Petrozza, J. C., & Styer, A. K. (2015) · Human Reproduction · doi:10.1093/humrep/dev298 · Cited by 66 · see citing works
Gårdebjer, E. M., Anderson, S. T., Pantaleon, M., Wlodek, M. E., & Moritz, K. M. (2015) · The FASEB Journal · doi:10.1096/fj.14-268979 · Cited by 65 · see citing works
Cleal, J. K., Poore, K. R., Newman, J. P., et al. (2007) · Pediatric Research · doi:10.1203/pdr.0b013e31813cbe60 · Cited by 60 · see citing works
Sun, C., Velazquez, M. A., Marfy-Smith, S., Sheth, B., Cox, A. L., Johnston, D. A., Smyth, N. R., & Fleming, T. P. (2014) · Development · doi:10.1242/dev.103952 · Cited by 60 · see citing works
Self-citationAberrant DNA methylation of imprinted H19 gene in human preimplantation embryos
Chen, S., Shi, X.-Y., Zheng, H., et al. (2010) · Fertility and Sterility · doi:10.1016/j.fertnstert.2010.01.120 · Cited by 58 · see citing works
Rexhaj, E., Pireva, A., Paoloni‐Giacobino, A., Allemann, Y., Cerny, D., Dessen, P., Sartori, C. S., Scherrer, U., & Rimoldi, S. F. (2015) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00621.2014 · Cited by 58 · see citing works
Gkourogianni, A., Kosteria, I., Telonis, A. G., Margeli, A., Mantzou, A., Konsta, M. A. P., Loutradis, D., Mastorakos, G. P., Papassotiriou, I., Klapa, M. I., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0094001 · Cited by 55 · see citing works
Torrens, C., Snelling, T. H., Chau, R., Shanmuganathan, M., Cleal, J. K., Poore, K. R., Noakes, D. E., Poston, L., Hanson, M. A., & Green, L. (2009) · Experimental Physiology · doi:10.1113/expphysiol.2009.047340 · Cited by 51 · see citing works
Self-citationMaternal nutrition modifies trophoblast giant cell phenotype and fetal growth in mice
Watkins, A. J., Lucas, E. S., Marfy-Smith, S., Bates, N., Kimber, S. J., & Fleming, T. P. (2015) · Reproduction · doi:10.1530/rep-14-0667 · Cited by 46 · see citing works
Self-citationVelazquez, M. A., Smith, C. G., Smyth, N. R., Osmond, C., & Fleming, T. P. (2016) · Human Reproduction · doi:10.1093/humrep/dew177 · Cited by 46 · see citing works
Self-citationSun, C., Denisenko, O. N., Sheth, B., Cox, A. L., Lucas, E. S., Smyth, N. R., & Fleming, T. P. (2015) · BMC Developmental Biology · doi:10.1186/s12861-015-0053-1 · Cited by 42 · see citing works
Self-citationDenisenko, O. N., Lucas, E. S., Sun, C., Watkins, A. J., Mar, D., Bomsztyk, K., & Fleming, T. P. (2016) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2016.04.001 · Cited by 39 · see citing works
Self-citationBurrage, D., Braddick, L., Cleal, J. K., et al. (2008) · The Journal of Physiology · doi:10.1113/jphysiol.2008.165944 · Cited by 22 · see citing works
McKay, J. A., Adriaens, M. E., Evelo, C. T., Ford, D., & Mathers, J. C. (2016) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201600079 · Cited by 18 · see citing works
Self-citationHorii, T., Suetake, I., Yanagisawa, E., et al. (2011) · Journal of Reproduction and Development · doi:10.1262/jrd.10-194a · Cited by 12 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- [98]Hanson M Godfrey K Poston L Bustreo F Stephenson J Preconception health Annual Report of the Chief Medical Officer 2014, The Health of the 51%: Women Davies SC London Department of Health 2015 53 66 Chapter 5
Cited by
Sorted by citations
Chronic inflammation in the etiology of disease across the life span
Furman, D., Campisi, J., Verdin, E., Carrera-Bastos, P., Targ, S., Franceschi, C., Ferrucci, L., Gilroy, D. W., Fasano, A., Miller, G. W., et al. (2019) · Nature Medicine · doi:10.1038/s41591-019-0675-0 · Cited by 4,915 · see citing works
The double burden of malnutrition: aetiological pathways and consequences for health
Wells, J. C., Sawaya, A. L., Wibaek, R., Mwangome, M., Poullas, M. S., Yajnik, C. S., & Demaio, A. (2020) · The Lancet · doi:10.1016/s0140-6736(19)32472-9 · Cited by 993 · see citing works
Self-citationThe importance of nutrition in pregnancy and lactation: lifelong consequences
Marshall, N. E., Abrams, B., Barbour, L. A., Catalano, P., Christian, P., Friedman, J. E., Hay, W. W., Hernandez, T. L., Krebs, N. F., Oken, E., et al. (2022) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2021.12.035 · Cited by 709 · see citing works
Central nervous pathways of insulin action in the control of metabolism and food intake
Kullmann, S., Kleinridders, A., Small, D. M., Fritsche, A., Häring, H.-U., Preissl, H., & Heni, M. (2020) · The Lancet Diabetes & Endocrinology · doi:10.1016/s2213-8587(20)30113-3 · Cited by 233 · see citing works
Life course epidemiology and public health
Wagner, C., Carmeli, C., Jackisch, J., Kivimäki, M., van der Linden, B. W. A., Cullati, S., & Chiolero, A. (2024) · The Lancet Public Health · doi:10.1016/s2468-2667(24)00018-5 · Cited by 188 · see citing works
Inequalities in early childhood care and development in low/middle-income countries: 2010–2018
Lu, C., Cuartas, J., Fink, G., McCoy, D., Liu, K., Li, Z., Daelmans, B., & Richter, L. (2020) · BMJ Global Health · doi:10.1136/bmjgh-2020-002314 · Cited by 188 · see citing works
Cardiometabolic-Based Chronic Disease, Addressing Knowledge and Clinical Practice Gaps
Mechanick, J. I., Farkouh, M. E., Newman, J. D., & Garvey, W. T. (2020) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2019.11.046 · Cited by 113 · see citing works
Vaivada, T., Lassi, Z. S., Irfan, O., Salam, R. A., Das, J. K., Oh, C., Carducci, B., Jain, R. P., Als, D., Sharma, N., et al. (2022) · The Lancet · doi:10.1016/s0140-6736(21)02725-2 · Cited by 89 · see citing works
Bagby, S. P., Martin, D., Chung, S. T., & Rajapakse, N. (2019) · American Journal of Public Health · doi:10.2105/ajph.2018.304864 · Cited by 79 · see citing works
Preconception health in England: a proposal for annual reporting with core metrics
Stephenson, J., Vogel, C., Hall, J., Hutchinson, J., Mann, S., Duncan, H., Woods-Townsend, K., de Lusignan, S., Poston, L., Cade, J., et al. (2019) · The Lancet · doi:10.1016/s0140-6736(19)30954-7 · Cited by 72 · see citing works
Self-citationCai, C., Busch, S., Wang, R., Sivak, A., & Davenport, M. H. (2022) · Journal of Affective Disorders · doi:10.1016/j.jad.2022.04.143 · Cited by 65 · see citing works
Hill, B., Skouteris, H., Teede, H. J., Bailey, C., Baxter, J.-A. B., Bergmeier, H. J., Borges, A. L. V., Harrison, C. L., Jack, B., Jorgensen, L., et al. (2019) · Journal of Clinical Medicine · doi:10.3390/jcm8122119 · Cited by 65 · see citing works
Self-citationIntergenerational Metabolic Syndrome and Neuronal Network Hyperexcitability in Autism
Rivell, A., & Mattson, M. P. (2019) · Trends in Neurosciences · doi:10.1016/j.tins.2019.08.006 · Cited by 50 · see citing works
McGowan, L., Lennon-Caughey, E., Chun, C., McKinley, M. C., & Woodside, J. V. (2020) · BMC Pregnancy and Childbirth · doi:10.1186/s12884-020-2733-5 · Cited by 47 · see citing works
Phillips-Beck, W., Sinclair, S., Campbell, R., Star, L., Cidro, J., Wicklow, B., Guillemette, L., Morris, M. I., & McGavock, J. M. (2019) · Journal of Developmental Origins of Health and Disease · doi:10.1017/s2040174418000661 · Cited by 44 · see citing works
Associations between periconceptional lifestyle behaviours and adverse pregnancy outcomes
Maas, V. Y. F., Poels, M., Lamain-de Ruiter, M., Kwee, A., Bekker, M. N., Franx, A., & Koster, M. P. H. (2021) · BMC Pregnancy and Childbirth · doi:10.1186/s12884-021-03935-x · Cited by 43 · see citing works
Kiosia, A., Dagbasi, A., Berkley, J. A., Wilding, J. P. H., Prendergast, A. J., Li, J. V., Swann, J., Mathers, J. C., Kerac, M., Morrison, D., et al. (2024) · Nutrition Bulletin · doi:10.1111/nbu.12670 · Cited by 43 · see citing works
Self-citationRubini, E., Baijens, I. M. M., Horánszky, A., Schoenmakers, S., Sinclair, K. D., Zana, M., Dinnyés, A., Steegers-Theunissen, R. P. M., & Rousian, M. (2021) · Genes · doi:10.3390/genes12101634 · Cited by 35 · see citing works
Gaillard, R., & Jaddoe, V. W. V. (2023) · Nature Reviews Cardiology · doi:10.1038/s41569-023-00869-z · Cited by 34 · see citing works
Uddin, G. M., Youngson, N. A., Chowdhury, S. S., Hagan, C., Sinclair, D. A., & Morris, M. J. (2020) · Cells · doi:10.3390/cells9040791 · Cited by 32 · see citing works
Sampathkumar, S., Parkhi, D., Ghebremichael-Weldeselassie, Y., Sukumar, N., & Saravanan, P. (2023) · Nutrition & Diabetes · doi:10.1038/s41387-023-00251-5 · Cited by 23 · see citing works
Boonpattrawong, N. P., Golbidi, S., Tai, D. C., Aleliunas, R. E., Bernatchez, P., Miller, J. W., Laher, I., & Devlin, A. M. (2020) · Physiological Reports · doi:10.14814/phy2.14582 · Cited by 14 · see citing works
Payne, E., Schoenaker, D., Turner, K., Murphy, H. R., Skouteris, H., Ismail, K., Silverio, S. A., & Benton, M. (2026) · Health Expectations · doi:10.1111/hex.70617 · Cited by 4 · see citing works
Panteris, E., Kakatsaki, I., Koukou, Z., Kolvatzis, C., Papanikolaou, S., & Hatzidaki, E. (2026) · Pathophysiology · doi:10.3390/pathophysiology33030067
- Authors
- Fleming, T. P., Watkins, A. J., Velazquez, M. A., Mathers, J. C., Prentice, A. M., Stephenson, J., Barker, M., Saffery, R., Yajnik, C. S., Eckert, J. J., Hanson, M. A., Forrester, T., Gluckman, P. D., & Godfrey, K. M.
- Affiliations
- University of Southampton (GB)
- University of Nottingham (GB)
- Newcastle University (GB)
- London School of Hygiene & Tropical Medicine (GB)
- University College London (GB)
- University Hospital Southampton NHS Foundation Trust (GB)
- The University of Melbourne (AU)
- University of the West Indies (JM)
- Agency for Science, Technology and Research (SG)
- Corresponding author
- Godfrey, Keith M
- ORCID
- Venue
- The Lancet
- Publisher
- Elsevier BV
- Published
- 2018-05
- Volume
- 391
- Issue
- 10132
- Pages
- 1842-1852
- ISSN
- 0099-5355 (ISSN-L)
- 0140-6736
- PMC
- PMC5975952
- OpenAlex
- W2787931223
- Cited by
- 1,147
- References
- 99
- Citations by year
- 2026: 117 · 2025: 127 · 2024: 129 · 2023: 132 · 2022: 168 · 2021: 137 · 2020: 170 · 2019: 131 · 2018: 35
- FWCI
- 22.60
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- The Lancet (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- ePrints Soton (University of Southampton) (acceptedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Repository@Nottingham (University of Nottingham) (submittedVersion, cc-by)
- Funders
- Medical Research Council (MC_UU_12011/4, MC-A760-5QX00)
- State Government of Victoria
- Aston University
- Nestlé Nutrition Institute
- Rosetrees Trust
- National Institute for Health Research (NF-SI-0515-10042)
- Seventh Framework Programme (317146, 278418, FP7/2007-2013)
- British Heart Foundation
- Department for International Development, UK Government
- Biotechnology and Biological Sciences Research Council (BB/1001840/1, BB/F007450/1)
- Topics
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Prenatal Substance Exposure Effects
- Health Sciences › Medicine › Obstetrics and Gynecology › Gestational Diabetes Research and Management
- Keywords
- periconceptional period, developmental origins of health and disease, developmental programming, maternal overnutrition, maternal obesity, maternal undernutrition, paternal factors, assisted reproduction, epigenetics, gamete maturation, embryonic development, offspring cardiovascular risk, metabolic risk, neurological risk, preconception health, protein malnutrition
- MeSH terms
- Animals, Diet, Female, Fertilization, Humans, Obesity, Pregnancy, Prenatal Exposure Delayed Effects, Prenatal Nutritional Physiological Phenomena, Epigenesis, Genetic, Embryonic Development, Mice
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