Epigenome-wide analysis identifies genes and pathways linked to neurobehavioral variation in preterm infants

Everson, Todd M.; Marsit, Carmen J.; Michael O’Shea, T.; Burt, Amber; Hermetz, Karen; Carter, Brian S.; Helderman, Jennifer; Hofheimer, Julie A.; McGowan, Elisabeth C.; Neal, Charles R.; Pastyrnak, Steven L.; Smith, Lynne M.; Soliman, Antoine; DellaGrotta, Sheri A.; Dansereau, Lynne M.; Padbury, James F.; Lester, Barry M.

doi:10.1038/s41598-019-42654-4

Cited by 84Epigenetics and DNA MethylationInfant Development and Preterm CareBirth, Development, and Health

Epigenome-wide analysis identifies genes and pathways linked to neurobehavioral variation in preterm infants

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Everson, Todd M., Marsit, Carmen J., Michael O’Shea, T., Burt, Amber, Hermetz, Karen, Carter, Brian S., Helderman, Jennifer, Hofheimer, Julie A. +9 more·2019·Scientific Reports

DOI 10.1038/s41598-019-42654-4PMC PMC6474865

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Abstract Background & Objectives Neonatal neurobehavioral performance measures, such as the NICU Network Neurobehavioral Scale (NNNS), have been developed to assess the neurobehavioral characteristics of infants and provide insights into future developmental trajectories. The identification of molecular biomarkers of very early life neurobehavioral experiences could lead to better predictions of the long-term developmental outcomes of high-risk infants including preterm infants. To this end, we aimed to examine whether variability in DNA methylation (DNAm) or epigenetic age from surrogate tissues are associated with NNNS profiles in a cohort of infants born less than 30 weeks postmenstrual age (PMA). Methods This study was performed within the Neonatal Neurobehavior and Outcomes in Very Preterm Infants (NOVI) Study and included those infants with complete NNNS assessment data and DNAm measured from buccal cells, collected at near term-equivalent age using the Illumina EPIC array (N=536). We tested whether epigenetic age and age acceleration differed between infants based on their NNNS profile classifications. Then we performed an epigenome-wide association study, to test whether DNAm at individual epigenetic loci varied between these NNNS profile groupings. Models were adjusted for recruitment site, infant sex, postmenstrual age, and estimated tissue heterogeneity. Results We found that infants with an optimal NNNS profile had slightly older epigenetic age than other NOVI infants (β 1 = 0.201, p-value = 0.026), and that infants with an atypical NNNS profile had differential methylation at 29 CpG sites (FDR < 10%). The genes annotated to these differentially methylated CpGs included PLA2G4E , TRIM9 , GRIK3 , and MACROD2 , which have previously been associated with neurological structure and function, or with neurobehavioral disorders. Conclusions Greater epigenetic age is associated with optimal NNNS responses while altered DNAm of multiple genes are associated with an atypical neurobehavioral profile at near-term equivalent age. These findings build upon the existing evidence that epigenetic variations in buccal cells may serve as markers of neonatal neurobehavior and might facilitate early identification of children at risk for abnormal developmental outcome.

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Human infants born preterm that exhibit an atypical neurobehavioral profile have significantly differential methylation of GRIK3 when compared with infants showing a more typical neurobehavioral profile.
“Similarly, human infants born preterm that exhibit an atypical neurobehavioral profile, including poor attention, self-regulation, and quality of movement, as well as increased arousal, excitability, and systemic signs of prenatal stress, have significantly differential methylation of GRIK3 when compared with infants showing a more typical neurobehavioral profile (Everson et al., 2019).”
From Glutamate receptors in domestication and modern human evolution (2020) · cites this paper as Everson et al., 2019

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Nylund, K. L., Asparouhov, T., & Muthén, B. O. (2007) · Structural Equation Modeling: A Multidisciplinary Journal · doi:10.1080/10705510701575396 · Cited by 11,415 · see citing works
DNA methylation age of human tissues and cell types
Horvath, S. (2013) · Genome Biology · doi:10.1186/gb-2013-14-10-r115 · Cited by 7,075 · see citing works
DNA methylation-based biomarkers and the epigenetic clock theory of ageing
Horvath, S., & Raj, K. (2018) · Nature Reviews Genetics · doi:10.1038/s41576-018-0004-3 · Cited by 3,095 · see citing works
The new NHGRI-EBI Catalog of published genome-wide association studies (GWAS Catalog)
MacArthur, J., Bowler, E., Cerezo, M., Gil, L., Hall, P., Hastings, E., Junkins, H., McMahon, A., Milano, A., Morales, J., et al. (2017) · Nucleic Acids Research · doi:10.1093/nar/gkw1133 · Cited by 2,161 · see citing works
A beta-mixture quantile normalization method for correcting probe design bias in Illumina Infinium 450 k DNA methylation data
Teschendorff, A. E., Marabita, F., Lechner, M., Bartlett, T. E., Tegner, J. N., Gómez-Cabrero, D., & Beck, S. (2012) · Bioinformatics · doi:10.1093/bioinformatics/bts680 · Cited by 1,652 · see citing works
Meta-Analysis of Neurobehavioral Outcomes in Very Preterm and/or Very Low Birth Weight Children
Aarnoudse-Moens, C. S. H., Weisglas-Kuperus, N., van Goudoever, J. B., & Oosterlaan, J. (2009) · Pediatrics · doi:10.1542/peds.2008-2816 · Cited by 1,587 · see citing works
Critical evaluation of the Illumina MethylationEPIC BeadChip microarray for whole-genome DNA methylation profiling
Pidsley, R., Zotenko, E., Peters, T. J., Lawrence, M. G., Risbridger, G. P., Molloy, P., Van Djik, S., Muhlhausler, B., Stirzaker, C., & Clark, S. J. (2016) · Genome biology · doi:10.1186/s13059-016-1066-1 · Cited by 1,480 · see citing works
DNA methylation age of blood predicts all-cause mortality in later life
Marioni, R. E., Shah, S., McRae, A. F., Chen, B. H., Colicino, E., Harris, S. E., Gibson, J., Henders, A. K., Redmond, P., Cox, S. R., et al. (2015) · Genome Biology · doi:10.1186/s13059-015-0584-6 · Cited by 1,261 · see citing works
Accounting for cellular heterogeneity is critical in epigenome-wide association studies
Jaffe, A. E., & Irizarry, R. A. (2014) · Genome Biology · doi:10.1186/gb-2014-15-2-r31 · Cited by 1,067 · see citing works
ConsensusPathDB: toward a more complete picture of cell biology
Kamburov, A., Pentchev, K., Galicka, H., Wierling, C., Lehrach, H., & Herwig, R. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkq1156 · Cited by 671 · see citing works
Impact of Bronchopulmonary Dysplasia, Brain Injury, and Severe Retinopathy on the Outcome of Extremely Low-Birth-Weight Infants at 18 Months
Schmidt, B. K., Asztalos, E. V., Roberts, R. S., Robertson, C. M. T., Sauve, R. S., Whitfield, M. F., & for the Trial of Indomethacin Prophylaxis in Preterms (TIPP) Investigators (2003) · JAMA · doi:10.1001/jama.289.9.1124 · Cited by 630 · see citing works
Poor Predictive Validity of the Bayley Scales of Infant Development for Cognitive Function of Extremely Low Birth Weight Children at School Age
Hack, M., Taylor, H. G., Drotar, D., Schluchter, M., Cartar, L., Wilson-Costello, D. E., Klein, N., Friedman, H., Minich, N. M., & Morrow, M. (2005) · PEDIATRICS · doi:10.1542/peds.2005-0173 · Cited by 604 · see citing works
A genome-wide scan for common alleles affecting risk for autism
Anney, R., Klei, L., Pinto, D., Regan, R., Conroy, J., Magalhaes, T. R., Correia, C., Abrahams, B. S., Sykes, N., Pagnamenta, A. T., et al. (2010) · Human Molecular Genetics · doi:10.1093/hmg/ddq307 · Cited by 593 · see citing works
ConsensusPathDB--a database for integrating human functional interaction networks
Kamburov, A., Wierling, C., Lehrach, H., & Herwig, R. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkn698 · Cited by 565 · see citing works
The epigenetic clock is correlated with physical and cognitive fitness in the Lothian Birth Cohort 1936
Marioni, R. E., Shah, S. H., McRae, A. F., Ritchie, S. J., Terrera, G. M., Harris, S. E., Gibson, J., Redmond, P. H., Cox, S. R., Pattie, A., et al. (2015) · International Journal of Epidemiology · doi:10.1093/ije/dyu277 · Cited by 559 · see citing works
Epidemiology of preterm birth
Purisch, S. E., & Gyamfi‐Bannerman, C. (2017) · Seminars in Perinatology · doi:10.1053/j.semperi.2017.07.009 · Cited by 518 · see citing works
Neurodevelopmental Outcomes of Infants Born Prematurely
Aylward, G. P. (2014) · Journal of Developmental & Behavioral Pediatrics · doi:10.1097/01.dbp.0000452240.39511.d4 · Cited by 511 · see citing works
Epigenetic age of the pre-frontal cortex is associated with neuritic plaques, amyloid load, and Alzheimer’s disease related cognitive functioning
Levine, M. E., Lu, A. T., Bennett, D. A., & Horvath, S. (2015) · Aging · doi:10.18632/aging.100864 · Cited by 455 · see citing works
Neurodevelopmental Outcomes of Extremely Low Birth Weight Infants &lt;32 Weeks’ Gestation Between 1993 and 1998
Vohr, B. R., Wright, L. L., Poole, W. K., McDonald, S. A., & for the NICHD Neonatal Research Network Follow-up Study (2005) · Pediatrics · doi:10.1542/peds.2004-2247 · Cited by 388 · see citing works
Behavioral Outcomes and Evidence of Psychopathology Among Very Low Birth Weight Infants at Age 20 Years
Hack, M., Youngstrom, E. A., Cartar, L., SCHLUCHTER, M. D., Taylor, H. G., Flannery, D. J., Klein, N., & Borawski, E. A. (2004) · PEDIATRICS · doi:10.1542/peds.2003-1017-l · Cited by 377 · see citing works
Neurodevelopmental outcomes of preterm infants
Allen, M. C. (2008) · Current Opinion in Neurology · doi:10.1097/wco.0b013e3282f88bb4 · Cited by 371 · see citing works
Rare Copy Number Variation Discovery and Cross-Disorder Comparisons Identify Risk Genes for ADHD
Lionel, A. C., Crosbie, J., Barbosa, N., Goodale, T., Thiruvahindrapuram, B., Rickaby, J., Gazzellone, M. J., Carson, A. R., Howe, J., Wang, Z., et al. (2011) · Science Translational Medicine · doi:10.1126/scitranslmed.3002464 · Cited by 366 · see citing works
Neurodevelopmental outcomes of preterm infants
Song, I. G. (2022) · Korean Journal of Pediatrics · doi:10.3345/cep.2022.00822 · Cited by 362 · see citing works
Frailty is associated with the epigenetic clock but not with telomere length in a German cohort
Breitling, L. P., Saum, K.-U., Perna, L., Schöttker, B., Holleczek, B., & Brenner, H. (2016) · Clinical Epigenetics · doi:10.1186/s13148-016-0186-5 · Cited by 296 · see citing works
The Neonatal Intensive Care Unit Network Neurobehavioral Scale procedures
Lester, B. M., Tronick, E. Z., & in collaboration with T. Berry Brazelton, M. (2004) · PEDIATRICS · doi:10.1542/peds.113.s2.641 · Cited by 295 · see citing works
Self-citation
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Knight, A. K., Craig, J. M., Theda, C., Bækvad‐Hansen, M., Bybjerg‐Grauholm, J., Hansen, C. S., Hollegaard, M. V., HOUGAARD, D. M., Mortensen, P. B., Weinsheimer, S., et al. (2016) · Genome biology · doi:10.1186/s13059-016-1068-z · Cited by 291 · see citing works
Neurodevelopmental Outcome of the Premature Infant
Stephens, B. E., & Vohr, B. R. (2009) · Pediatric Clinics of North America · doi:10.1016/j.pcl.2009.03.005 · Cited by 283 · see citing works
Behavioral Outcomes of Extremely Low Birth Weight Children at Age 8 Years
Hack, M., Taylor, H. G., SCHLUCHTER, M. D., Andreias, L., Drotar, D., & Klein, N. (2009) · Journal of Developmental & Behavioral Pediatrics · doi:10.1097/dbp.0b013e31819e6a16 · Cited by 278 · see citing works
CACNA1H mutations in autism spectrum disorders
Splawski, I., Yoo, D. S., Stotz, S. C., Cherry, A., Clapham, D. E., & Keating, M. T. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m603316200 · Cited by 255 · see citing works
Neonatal Neurobehavior Predicts Medical and Behavioral Outcome
Liu, J., Bann, C., Lester, B. M., Tronick, E. Z., Das, A., LaGasse, L. L., Bauer, C. R., Shankaran, S., & Bada, H. S. (2009) · PEDIATRICS · doi:10.1542/peds.2009-0204 · Cited by 211 · see citing works
Self-citation
Pattern of Learning Disabilities in Children With Extremely Low Birth Weight and Broadly Average Intelligence
GRUNAU, R. E., Whitfield, M. F., & Davis, C. R. (2002) · Archives of Pediatrics and Adolescent Medicine · doi:10.1001/archpedi.156.6.615 · Cited by 192 · see citing works
A Novel Cell-Type Deconvolution Algorithm Reveals Substantial Contamination by Immune Cells in Saliva, Buccal and Cervix
Zheng, S., Webster, A. P., Dong, D., Feber, A., Graham, D. G., Sullivan, R., Jevons, S., Lovat, L. B., Beck, S., Widschwendter, M., et al. (2018) · Epigenomics · doi:10.2217/epi-2018-0037 · Cited by 189 · see citing works
School-Age Consequences of Birth Weight Less Than 750 g: A Review and Update
Taylor, H. G., Klein, N., & Hack, M. (2000) · Developmental Neuropsychology · doi:10.1207/s15326942dn1703_2 · Cited by 173 · see citing works
Buccals are likely to be a more informative surrogate tissue than blood for epigenome-wide association studies
Lowe, R., Gemma, C., Beyan, H., Hawa, M. I., Bazeos, A., Leslie, R. D., Montpetit, A., Rakyan, V. K., & Ramagopalan, S. V. (2013) · Epigenetics · doi:10.4161/epi.24362 · Cited by 160 · see citing works
History and description of the Neonatal Intensive Care Unit Network Neurobehavioral Scale
Lester, B. M., & Tronick, E. Z. (2004) · PEDIATRICS · doi:10.1542/peds.113.s2.634 · Cited by 154 · see citing works
Self-citation
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Xu, B., Woodroffe, A., Rodriguez‐Murillo, L., Roos, J. L., van Rensburg, E. J., Abecasis, G. R., Gogos, J. A., & Karayiorgou, M. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0908584106 · Cited by 154 · see citing works
Factor X Deficiency
Menegatti, M., & Peyvandi, F. (2009) · Seminars in Thrombosis and Hemostasis · doi:10.1055/s-0029-1225763 · Cited by 139 · see citing works
The Correlation Of Methylation Levels Measured Using Illumina 450K And EPIC Beadchips In Blood Samples
Logue, M. W., Smith, A. K., Wolf, E. J., Maniates, H., Stone, A., Schichman, S. A., McGlinchey, R. E., Milberg, W., & Miller, M. W. (2017) · Epigenomics · doi:10.2217/epi-2017-0078 · Cited by 139 · see citing works
Conduct disorder and ADHD: Evaluation of conduct problems as a categorical and quantitative trait in the international multicentre ADHD genetics study
Anney, R., Lasky-Su, J., O'Dushlaine, C., Kenny, E., Neale, B., Mulligan, A., Franke, B., Zhou, K., Chen, W., Christiansen, H., et al. (2008) · American Journal of Medical Genetics Part B: Neuropsychiatric Genetics · doi:10.1002/ajmg.b.30871 · Cited by 135 · see citing works
Effects of preterm birth and fetal growth retardation on cardiovascular risk factors in young adulthood
Evensen, K. A. I., Steinshamn, S., Tjønna, A. E., Stølen, T., Høydal, M. A., Wisløff, U., Brubakk, A., & Vik, T. (2008) · Early Human Development · doi:10.1016/j.earlhumdev.2008.10.008 · Cited by 131 · see citing works
The epigenetic clock and physical development during childhood and adolescence: longitudinal analysis from a UK birth cohort
Simpkin, A. J., Howe, L. D., Tilling, K. M., Gaunt, T. R., Lyttleton, O., McArdle, W. L., Ring, S. M., Horvath, S., Smith, G. D., & Relton, C. L. (2016) · International Journal of Epidemiology · doi:10.1093/ije/dyw307 · Cited by 131 · see citing works
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Viveros, M., Llorente, R., Suárez, J., Llorente‐Berzal, A., López‐Gallardo, M., & de Fonseca, F. R. (2011) · Journal of Psychopharmacology · doi:10.1177/0269881111408956 · Cited by 124 · see citing works
A calcium-dependent acyltransferase that produces N-acyl phosphatidylethanolamines
Ogura, Y., Parsons, W. H., Kamat, S. S., & Cravatt, B. F. (2016) · Nature Chemical Biology · doi:10.1038/nchembio.2127 · Cited by 120 · see citing works
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Omid Kohannim, A. (2012) · Frontiers in Neuroscience · doi:10.3389/fnins.2012.00115 · Cited by 114 · see citing works
Social Lifestyle, Risk-taking Behavior, and Psychopathology in Young Adults Born Very Preterm or with a Very Low Birthweight
Hille, E. T. M., Dorrepaal, C. A., Perenboom, R. J. M., Gravenhorst, J. B., Brand, R., & Verloove-Vanhorick, S. P. (2008) · The Journal of Pediatrics · doi:10.1016/j.jpeds.2007.11.041 · Cited by 105 · see citing works
Mosaic Epigenetic Dysregulation of Ectodermal Cells in Autism Spectrum Disorder
Berko, E. R., Suzuki, M., Beren, F., Lemetre, C., Alaimo, C. M., Calder, R. B., Ballaban‐Gil, K. R., Gounder, B., Kampf, K., Kirschen, J., et al. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004402 · Cited by 105 · see citing works
Regions of variable DNA methylation in human placenta associated with newborn neurobehavior
Paquette, A. G., Houseman, E. A., Green, B. B., Lesseur, C., Armstrong, D. A., Lester, B. M., & Marsit, C. J. (2016) · Epigenetics · doi:10.1080/15592294.2016.1195534 · Cited by 105 · see citing works
Self-citation
Neurobehavior at Term and White and Gray Matter Abnormalities in Very Preterm Infants
Brown, N. C., Inder, T. E., Bear, M. J., Hunt, R. W., Anderson, P. J., & Doyle, L. W. (2009) · The Journal of Pediatrics · doi:10.1016/j.jpeds.2009.01.038 · Cited by 100 · see citing works
The E3 Ubiquitin Ligase TRIM9 Is a Filopodia Off Switch Required for Netrin-Dependent Axon Guidance
Menon, S., Boyer, N. P., Winkle, C. C., McClain, L. M., Hanlin, C. C., Pandey, D. B., Rothenfußer, S., Taylor, A. M., & Gupton, S. L. (2015) · Developmental Cell · doi:10.1016/j.devcel.2015.11.022 · Cited by 95 · see citing works
Neurodevelopmental Outcomes of Extremely Low Birth Weight Infants
Vohr, B. R., Wright, L., Poole, W. K., & McDonald, S. A. (2005) · Cited by 95 · see citing works
Neonatal pain and COMT Val158Met genotype in relation to serotonin transporter (SLC6A4) promoter methylation in very preterm children at school age
Chau, C. M. Y., Ranger, M., Sulistyoningrum, D. C., Devlin, A. M., Oberlander, T. F., & GRUNAU, R. E. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00409 · Cited by 93 · see citing works
Neurobehavior Related to Epigenetic Differences in Preterm Infants
Lester, B. M., Marsit, C. J., Giarraputo, J., Hawes, K., LaGasse, L. L., & Padbury, J. F. (2015) · Epigenomics · doi:10.2217/epi.15.63 · Cited by 89 · see citing works
Self-citation
Frequency and transmission of glutamate receptors GRIK2 and GRIK3 polymorphisms in patients with obsessive compulsive disorder
Delorme, R., Krebs, M., Chabane, N., Roy, I., Millet, B., Mouren-Siméoni, M. C., Maier, W., Bourgeron, T., & Leboyer, M. (2004) · Neuroreport · doi:10.1097/00001756-200403220-00025 · Cited by 88 · see citing works
Patterns of Altered Neurobehavior in Preterm Infants within the Neonatal Intensive Care Unit
Pineda, R. G., Tjoeng, T. H., Vavasseur, C., Kidokoro, H., Neil, J. J., & Inder, T. E. (2012) · The Journal of Pediatrics · doi:10.1016/j.jpeds.2012.08.011 · Cited by 88 · see citing works
Pain-related stress during the Neonatal Intensive Care Unit stay and SLC6A4 methylation in very preterm infants
Provenzi, L., Fumagalli, M., Sirgiovanni, I., Giorda, R., Pozzoli, U., Morandi, F., Beri, S., Menozzi, G., Mosca, F., Borgatti, R., et al. (2015) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2015.00099 · Cited by 88 · see citing works
Mechanisms by which a CACNA1H mutation in epilepsy patients increases seizure susceptibility
Eckle, V., Shcheglovitov, A., Vitko, I., Dey, D., Yap, C. C., Winckler, B., & Perez‐Reyes, E. (2013) · The Journal of Physiology · doi:10.1113/jphysiol.2013.264176 · Cited by 86 · see citing works
Epigenomic profiling of preterm infants reveals DNA methylation differences at sites associated with neural function
Sparrow, S. A., Manning, J. R., Cartier, J., Anblagan, D., Bastin, M. E., Piyasena, C., Pataky, R., Moore, E. J., Semple, S. I., Wilkinson, A. G., et al. (2016) · Translational Psychiatry · doi:10.1038/tp.2015.210 · Cited by 85 · see citing works
“Gap hunting” to characterize clustered probe signals in Illumina methylation array data
Andrews, S. V., Ladd‐Acosta, C., Feinberg, A. P., Hansen, K. D., & Fallin, M. D. (2016) · Epigenetics & Chromatin · doi:10.1186/s13072-016-0107-z · Cited by 84 · see citing works
Serotonin Transporter Gene ( SLC6A4 ) Methylation Associates With Neonatal Intensive Care Unit Stay and 3-Month-Old Temperament in Preterm Infants
Montirosso, R., Provenzi, L., Fumagalli, M., Sirgiovanni, I., Giorda, R., Pozzoli, U., Beri, S., Menozzi, G., Tronick, E., Morandi, F., et al. (2016) · Child Development · doi:10.1111/cdev.12492 · Cited by 83 · see citing works
Mutations in EBF3 Disturb Transcriptional Profiles and Cause Intellectual Disability, Ataxia, and Facial Dysmorphism
Harms, F. L., Girisha, K. M., Hardigan, A. A., Kortüm, F., Shukla, A., Alawi, M., Dalal, A. B., Brady, L., Tarnopolsky, M. A., Bird, L. M., et al. (2016) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2016.11.012 · Cited by 79 · see citing works
Accelerated DNA methylation age in adolescent girls: associations with elevated diurnal cortisol and reduced hippocampal volume
Davis, E., Humphreys, K. L., McEwen, L. M., Sacchet, M. D., Camacho, M. C., MacIsaac, J. L., Lin, D., Kobor, M. S., & Gotlib, I. H. (2017) · Translational Psychiatry · doi:10.1038/tp.2017.188 · Cited by 79 · see citing works
Infant Neurobehavioral Dysregulation: Behavior Problems in Children With Prenatal Substance Exposure
Lester, B. M., Bagner, D. M., Liu, J., LaGasse, L. L., Seifer, R., Bauer, C. R., Shankaran, S., Bada, H. S., Higgins, R. D., & Das, A. (2009) · PEDIATRICS · doi:10.1542/peds.2008-2898 · Cited by 74 · see citing works
Self-citation
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Schiffer, H. H., & Heinemann, S. (2006) · American Journal of Medical Genetics Part B Neuropsychiatric Genetics · doi:10.1002/ajmg.b.30374 · Cited by 71 · see citing works
Epigenetic Mechanisms in The Placenta Related to Infant Neurodevelopment
Lester, B. M., & Marsit, C. J. (2018) · Epigenomics · doi:10.2217/epi-2016-0171 · Cited by 71 · see citing works
Self-citation
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Sucharew, H. J., Khoury, J. C., Xu, Y. Y., Succop, P. S., & Yolton, K. A. (2012) · Paediatric and Perinatal Epidemiology · doi:10.1111/j.1365-3016.2012.01288.x · Cited by 68 · see citing works
The epigenetic clock and pubertal, neuroendocrine, psychiatric, and cognitive outcomes in adolescents
Suarez, A., Lahti, J. M. T., Czamara, D., Lahti‐Pulkkinen, M., Girchenko, P. V., Andersson, S., Strandberg, T. E., Reynolds, R. M., Kajantie, E., Binder, E. B., et al. (2018) · Clinical Epigenetics · doi:10.1186/s13148-018-0528-6 · Cited by 62 · see citing works
MACROD2 gene associated with autistic-like traits in a general population sample
Jones, R., Cadby, G., Blangero, J., Abraham, L. J., Whitehouse, A., & Moses, E. K. (2014) · Psychiatric Genetics · doi:10.1097/ypg.0000000000000052 · Cited by 59 · see citing works
Major Congenital Anomalies Place Extremely Low Birth Weight Infants at Higher Risk for Poor Growth and Developmental Outcomes
Walden, R. V., Taylor, S., Hansen, N. I., Poole, W. K., Stoll, B. J., Abuelo, D. N., & Vohr, B. R. (2007) · PEDIATRICS · doi:10.1542/peds.2007-0354 · Cited by 57 · see citing works
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Winkle, C. C., Olsen, R. H. J., Kim, H., Moy, S. S., Song, J., & Gupton, S. L. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.3876-15.2016 · Cited by 57 · see citing works
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Plooster, M., Menon, S., Winkle, C. C., Urbina, F., Monkiewicz, C., Phend, K. D., Weinberg, R. J., & Gupton, S. L. (2017) · Molecular Biology of the Cell · doi:10.1091/mbc.e16-08-0594 · Cited by 53 · see citing works
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Preterm births - United States, 2007.
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Takenouchi, T., Hashida, N., Torii, C., Kosaki, R., Takahashi, T., & Kosaki, K. (2013) · American Journal of Medical Genetics Part A · doi:10.1002/ajmg.a.36240 · Cited by 36 · see citing works
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Dlugos, D., Scattergood, T. M., Ferraro, T. N., Berrettinni, W. H., & Buono, R. J. (2005) · Epilepsy & Behavior · doi:10.1016/j.yebeh.2005.01.014 · Cited by 28 · see citing works
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Coleman, M. B., Glass, P., Brown, J. E., Kadom, N., Tsuchida, T. N., Scafidi, J., Chang, T., Vézina, G., & Massaro, A. N. (2013) · Early Human Development · doi:10.1016/j.earlhumdev.2013.05.006 · Cited by 26 · see citing works
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Research works printed but not linked: 2

[3]Institute of Medicine. Preterm Birth: Causes, Consequences and Prevention. (National Academic Press, 2006).
[38]Lester BM Tronick EZ Brazelton TB The Neonatal Intensive Care Unit Network Neurobehavioral Scale procedures Pediatrics 2004 113 641 667 14993524

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Additional file 4 of DNA methylation patterns at birth predict health outcomes in young adults born very low birthweight
Cameron, V. A., Jones, G. T., Horwood, L. J., Pilbrow, A. P., Martin, J., Frampton, C. M., Ip, W. T., Troughton, R. W., Greer, C., Yang, J., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22617349
Additional file 7 of DNA methylation patterns at birth predict health outcomes in young adults born very low birthweight
Cameron, V. A., Jones, G. T., Horwood, L. J., Pilbrow, A. P., Martin, J., Frampton, C. M., Ip, W. T., Troughton, R. W., Greer, C., Yang, J., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22617358
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Additional file 12 of DNA methylation patterns at birth predict health outcomes in young adults born very low birthweight
Cameron, V. A., Jones, G. T., Horwood, L. J., Pilbrow, A. P., Martin, J., Frampton, C., Ip, W. T., Troughton, R. W., Greer, C., Yang, J., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22617373
Additional file 6 of Batch-effect detection, correction and characterisation in Illumina HumanMethylation450 and MethylationEPIC BeadChip array data
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Additional file 14 of Batch-effect detection, correction and characterisation in Illumina HumanMethylation450 and MethylationEPIC BeadChip array data
Ross, J. P., van Dijk, S. J., Phang, M., Skilton, M. R., Molloy, P. L., & Oytam, Y. (2022) · Figshare · doi:10.6084/m9.figshare.19687241
Additional file 15 of DNA methylation patterns at birth predict health outcomes in young adults born very low birthweight
Cameron, V. A., Jones, G. T., Horwood, L. J., Pilbrow, A. P., Martin, J., Frampton, C., Ip, W. T., Troughton, R. W., Greer, C., Yang, J., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22617385
Additional file 3 of Batch-effect detection, correction and characterisation in Illumina HumanMethylation450 and MethylationEPIC BeadChip array data
Ross, J. P., van Dijk, S. J., Phang, M., Skilton, M. R., Molloy, P. L., & Oytam, Y. (2022) · Figshare · doi:10.6084/m9.figshare.19687253
Additional file 7 of Batch-effect detection, correction and characterisation in Illumina HumanMethylation450 and MethylationEPIC BeadChip array data
Ross, J. P., van Dijk, S. J., Phang, M., Skilton, M. R., Molloy, P. L., & Oytam, Y. (2022) · Figshare · doi:10.6084/m9.figshare.19687265
Additional file 6 of DNA methylation patterns at birth predict health outcomes in young adults born very low birthweight
Cameron, V. A., Jones, G. T., Horwood, L. J., Pilbrow, A. P., Martin, J., Frampton, C., Ip, W. T., Troughton, R. W., Greer, C., Yang, J., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22617355
Additional file 4 of Batch-effect detection, correction and characterisation in Illumina HumanMethylation450 and MethylationEPIC BeadChip array data
Ross, J. P., van Dijk, S. J., Phang, M., Skilton, M. R., Molloy, P. L., & Oytam, Y. (2022) · Figshare · doi:10.6084/m9.figshare.19687256
Additional file 8 of Batch-effect detection, correction and characterisation in Illumina HumanMethylation450 and MethylationEPIC BeadChip array data
Ross, J. P., van Dijk, S. J., Phang, M., Skilton, M. R., Molloy, P. L., & Oytam, Y. (2022) · Figshare · doi:10.6084/m9.figshare.19687268
Additional file 10 of Batch-effect detection, correction and characterisation in Illumina HumanMethylation450 and MethylationEPIC BeadChip array data
Ross, J. P., van Dijk, S. J., Phang, M., Skilton, M. R., Molloy, P. L., & Oytam, Y. (2022) · Figshare · doi:10.6084/m9.figshare.19687229
Additional file 1 of DNA methylation patterns at birth predict health outcomes in young adults born very low birthweight
Cameron, V. A., Jones, G. T., Horwood, L. J., Pilbrow, A. P., Martin, J., Frampton, C., Ip, W. T., Troughton, R. W., Greer, C., Yang, J., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22617337
Additional file 9 of Batch-effect detection, correction and characterisation in Illumina HumanMethylation450 and MethylationEPIC BeadChip array data
Ross, J. P., van Dijk, S. J., Phang, M., Skilton, M. R., Molloy, P. L., & Oytam, Y. (2022) · Figshare · doi:10.6084/m9.figshare.19687271
Additional file 2 of Batch-effect detection, correction and characterisation in Illumina HumanMethylation450 and MethylationEPIC BeadChip array data
Ross, J. P., van Dijk, S. J., Phang, M., Skilton, M. R., Molloy, P. L., & Oytam, Y. (2022) · Figshare · doi:10.6084/m9.figshare.19687250
Additional file 14 of DNA methylation patterns at birth predict health outcomes in young adults born very low birthweight
Cameron, V. A., Jones, G. T., Horwood, L. J., Pilbrow, A. P., Martin, J., Frampton, C., Ip, W. T., Troughton, R. W., Greer, C., Yang, J., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22617382
Additional file 2 of DNA methylation patterns at birth predict health outcomes in young adults born very low birthweight
Cameron, V. A., Jones, G. T., Horwood, L. J., Pilbrow, A. P., Martin, J., Frampton, C., Ip, W. T., Troughton, R. W., Greer, C., Yang, J., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22617343
Additional file 11 of DNA methylation patterns at birth predict health outcomes in young adults born very low birthweight
Cameron, V. A., Jones, G. T., Horwood, L. J., Pilbrow, A. P., Martin, J., Frampton, C., Ip, W. T., Troughton, R. W., Greer, C., Yang, J., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22617370
Additional file 8 of DNA methylation patterns at birth predict health outcomes in young adults born very low birthweight
Cameron, V. A., Jones, G. T., Horwood, L. J., Pilbrow, A. P., Martin, J., Frampton, C., Ip, W. T., Troughton, R. W., Greer, C., Yang, J., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22617361
Additional file 3 of DNA methylation patterns at birth predict health outcomes in young adults born very low birthweight
Cameron, V. A., Jones, G. T., Horwood, L. J., Pilbrow, A. P., Martin, J., Frampton, C., Ip, W. T., Troughton, R. W., Greer, C., Yang, J., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22617346
Additional file 13 of Batch-effect detection, correction and characterisation in Illumina HumanMethylation450 and MethylationEPIC BeadChip array data
Ross, J. P., van Dijk, S. J., Phang, M., Skilton, M. R., Molloy, P. L., & Oytam, Y. (2022) · Figshare · doi:10.6084/m9.figshare.19687238
Additional file 1 of Serious neonatal morbidities are associated with differences in DNA methylation among very preterm infants
Everson, T. M., O’Shea, T. M., Burt, A., Hermetz, K. E., Carter, B. S., Helderman, J., Hofheimer, J. A., McGowan, E. C., Neal, C. R., Pastyrnak, S. L., et al. (2020) · Figshare · doi:10.6084/m9.figshare.13115328
Self-citation
Additional file 12 of Batch-effect detection, correction and characterisation in Illumina HumanMethylation450 and MethylationEPIC BeadChip array data
Ross, J. P., van Dijk, S. J., Phang, M., Skilton, M. R., Molloy, P. L., & Oytam, Y. (2022) · Figshare · doi:10.6084/m9.figshare.19687235
Additional file 5 of Batch-effect detection, correction and characterisation in Illumina HumanMethylation450 and MethylationEPIC BeadChip array data
Ross, J. P., van Dijk, S. J., Phang, M., Skilton, M. R., Molloy, P. L., & Oytam, Y. (2022) · Figshare · doi:10.6084/m9.figshare.19687259
Additional file 5 of DNA methylation patterns at birth predict health outcomes in young adults born very low birthweight
Cameron, V. A., Jones, G. T., Horwood, L. J., Pilbrow, A. P., Martin, J., Frampton, C., Ip, W. T., Troughton, R. W., Greer, C., Yang, J., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22617352
Additional file 1 of Batch-effect detection, correction and characterisation in Illumina HumanMethylation450 and MethylationEPIC BeadChip array data
Ross, J. P., van Dijk, S. J., Phang, M., Skilton, M. R., Molloy, P. L., & Oytam, Y. (2022) · Figshare · doi:10.6084/m9.figshare.19687247
Additional file 9 of DNA methylation patterns at birth predict health outcomes in young adults born very low birthweight
Cameron, V. A., Jones, G. T., Horwood, L. J., Pilbrow, A. P., Martin, J., Frampton, C., Ip, W. T., Troughton, R. W., Greer, C., Yang, J., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22617364
Additional file 13 of DNA methylation patterns at birth predict health outcomes in young adults born very low birthweight
Cameron, V. A., Jones, G. T., Horwood, L. J., Pilbrow, A. P., Martin, J., Frampton, C., Ip, W. T., Troughton, R. W., Greer, C., Yang, J., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22617379
Additional file 10 of DNA methylation patterns at birth predict health outcomes in young adults born very low birthweight
Cameron, V. A., Jones, G. T., Horwood, L. J., Pilbrow, A. P., Martin, J., Frampton, C., Ip, W. T., Troughton, R. W., Greer, C., Yang, J., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22617367
Additional file 11 of Batch-effect detection, correction and characterisation in Illumina HumanMethylation450 and MethylationEPIC BeadChip array data
Ross, J. P., van Dijk, S. J., Phang, M., Skilton, M. R., Molloy, P. L., & Oytam, Y. (2022) · Figshare · doi:10.6084/m9.figshare.19687232
Neonatal and Early Childhood Epigenetic Variation Linked to Social and Behavioral Outcomes in Very Preterm ChildrenPreprint
Patel, P., Huang, Y., Camerota, M., Cragin, C. A., Carter, B. S., Check, J. F., Helderman, J., Hofheimer, J. A., McGowan, E. C., Neal, C. R., et al. (2026) · medRxiv · doi:10.64898/2026.02.19.26346629
Self-citation
Twists and Turmoil: Comanaging Mood and Movement in a Child with Cerebral Palsy
Riordan, H. (2026) · Springer eBooks · doi:10.1007/978-3-032-10099-3_18

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Patel, P., Huang, Y., Camerota, M., Cragin, C. A., Carter, B. S., Check, J. F., Helderman, J., Hofheimer, J. A., McGowan, E. C., Neal, C. R., et al. (2026) · medRxiv · doi:10.64898/2026.02.19.26346629
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Paniagua, U., Lester, B. M., Marsit, C. J., Camerota, M., Carter, B. S., Check, J. F., Helderman, J., Hofheimer, J. A., McGowan, E. C., Neal, C. R., et al. (2023) · Epigenetics · doi:10.1080/15592294.2023.2280738 · Cited by 10 · see citing works
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Camerota, M., Lester, B., Castellanos, F. X., Carter, B. S., Check, J., Helderman, J., Hofheimer, J., McGowan, E., Neal, C. R., Pastyrnak, S., et al. (2024) · Translational Psychiatry · doi:10.1038/s41398-024-02841-y · Cited by 10 · see citing works
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Serious neonatal morbidities are associated with differences in DNA methylation among very preterm infants
Everson, T. M., O’Shea, T. M., Burt, A., Hermetz, K. E., Carter, B. S., Helderman, J., Hofheimer, J. A., McGowan, E. C., Neal, C. R., Pastyrnak, S. L., et al. (2020) · Clinical Epigenetics · doi:10.1186/s13148-020-00942-1 · Cited by 49 · see citing works
Self-citation

Authors: Everson, T. M., Marsit, C. J., Michael O’Shea, T., Burt, A., Hermetz, K., Carter, B. S., Helderman, J., Hofheimer, J. A., McGowan, E. C., Neal, C. R., Pastyrnak, S. L., Smith, L. M., Soliman, A., DellaGrotta, S. A., Dansereau, L. M., Padbury, J. F., & Lester, B. M.
Affiliations: Emory University (US)
Children's Mercy Hospital (US)
Wake Forest University Health Sciences (US)
University of North Carolina at Chapel Hill (US)
Brown University (US)
University of Hawaiʻi at Mānoa (US)
Spectrum Health (US)
Harbor–UCLA Medical Center (US)
Miller Children's & Women's Hospital (US)
Corresponding author: Everson, Todd M.
ORCID: Everson, Todd M.
Marsit, Carmen J.
Burt, Amber
Hermetz, Karen
Carter, Brian S.
Hofheimer, Julie A.
McGowan, Elisabeth C.
Pastyrnak, Steven L.
Smith, Lynne M.
Soliman, Antoine
Padbury, James F.
Lester, Barry M.
Venue: Scientific Reports
Publisher: Springer Science and Business Media LLC
Published: 2019-04-19
Volume: 9
Issue: 1
Pages: 6322-6322
ISSN: 2045-2322 (ISSN-L)
DOI: 10.1038/s41598-019-42654-4
PMC: PMC6474865
OpenAlex: W2898171560
Cited by: 82
References: 86
Citations by year: 2026: 3 · 2025: 5 · 2024: 6 · 2023: 19 · 2022: 30 · 2021: 5 · 2020: 11 · 2019: 3
FWCI: 4.05
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0 (tdm)
creativecommons.org/licenses/by/4.0 (vor)
Locations: Scientific Reports (publishedVersion, cc-by)
bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Funders: U.S. Department of Health & Human Services | NIH | Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01HD084515, R01HD072267)
U.S. Department of Health & Human Services | National Institutes of Health (UH3OD023347)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Infant Development and Preterm Care
Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
Keywords: preterm infants, DNA methylation, epigenome-wide association study, neurobehavioral development, NICU Network Neurobehavioral Scale, epigenetic age, accelerated aging, buccal cell DNA, neonatal biomarkers, brain-behavior relationship, developmental prediction, TRIM9, GRIK3, MACROD2
MeSH terms: Child, Female, Humans, Infant, Infant, Newborn, Infant, Premature, Diseases, Male, Nerve Tissue Proteins, Infant Behavior, CpG Islands, Infant, Very Low Birth Weight, DNA Methylation

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Epigenome-wide analysis identifies genes and pathways linked to neurobehavioral variation in preterm infants

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