Influence of Prenatal Lead Exposure on Genomic Methylation of Cord Blood DNA
Open accessAbstract
Background: Fetal lead exposure is associated with adverse pregnancy outcomes and developmental and cognitive deficits; however, the mechanism(s) by which lead-induced toxicity occurs remains unknown. Epigenetic fetal programming via DNA methylation may provide a pathway by which environmental lead exposure can influence disease susceptibility. Objective: This study was designed to determine whether prenatal lead exposure is associated with alterations in genomic methylation of leukocyte DNA levels from umbilical cord samples. Methods: We measured genomic DNA methylation, as assessed by Alu and LINE-1 (long interspersed nuclear element-1) methylation via pyrosequencing, on 103 umbilical cord blood samples from the biorepository of the Early Life Exposures in Mexico to Environmental Toxicants (ELEMENT) study group. Prenatal lead exposure had been assessed by measuring maternal bone lead levels at the mid-tibial shaft and the patella using a spot-source 109Cd K-shell X-ray fluorescence instrument. Results: We found an inverse dose–response relationship in which quartiles of patella lead correlated with cord LINE-1 methylation (p for trend = 0.01) and and tibia lead correlated with Alu methylation (p for trend = 0.05). In mixed effects regression models, maternal tibia lead was negatively associated with umbilical cord genomic DNA methylation of Alu (β= −0.027; p = 0.01). We found no associations between cord blood lead and cord genomic DNA methylation. Conclusions: Prenatal lead exposure is inversely associated with genomic DNA methylation in cord blood. These data suggest that the epigenome of the developing fetus can be influenced by maternal cumulative lead burden, which may influence long-term epigenetic programming and disease susceptibility throughout the life course.
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?
Maternal lead levels are inversely correlated with genomic DNA methylation of the LINE-1 element in umbilical cord blood.
“Similarly, maternal lead levels are inversely correlated with genomic DNA methylation of the LINE-1 element in umbilical cord blood [ 45 ].”
From DNA methylation: a mechanism linking environmental chemical exposures to risk of autism spectrum disorders? (2016) · cites this paper as [45]
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
1 retracted
Chang, H., Anway, M. D., Rekow, S. S., & Skinner, M. K. (2006) · Endocrinology · doi:10.1210/en.2006-0987 · Cited by 148 · see citing works
RetractedWEIGHT IN INFANCY AND DEATH FROM ISCHAEMIC HEART DISEASE
Barker, D. J. P., Osmond, C., Winter, P. D., Margetts, B., & Simmonds, S. J. (1989) · The Lancet · doi:10.1016/s0140-6736(89)90710-1 · Cited by 3,574 · see citing works
Environmental epigenomics and disease susceptibility
Jirtle, R. L., & Skinner, M. K. (2007) · Nature Reviews Genetics · doi:10.1038/nrg2045 · Cited by 2,492 · see citing works
Lanphear, B. P., Hornung, R., Khoury, J., Yolton, K., Baghurst, P., Bellinger, D. C., Canfield, R. L., Dietrich, K. N., Bornschein, R., Greene, T., et al. (2005) · Environmental Health Perspectives · doi:10.1289/ehp.7688 · Cited by 2,205 · see citing works
Intellectual Impairment in Children with Blood Lead Concentrations below 10 μg per Deciliter
Canfield, R. L., Henderson, C. R., Cory-Slechta, D. A., Cox, C., Jusko, T. A., & Lanphear, B. P. (2003) · New England Journal of Medicine · doi:10.1056/nejmoa022848 · Cited by 2,081 · see citing works
Transposable elements: targets for early nutritional effects on epigenetic gene regulation
Waterland, R. A., & Jirtle, R. L. (2003) · Molecular and Cellular Biology · doi:10.1128/mcb.23.15.5293-5300.2003 · Cited by 2,019 · see citing works
Mobile Elements: Drivers of Genome Evolution
Kazazian, H. H. (2004) · Science · doi:10.1126/science.1089670 · Cited by 1,922 · see citing works
Dolinoy, D. C., Huang, D., & Jirtle, R. L. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0703739104 · Cited by 1,369 · see citing works
Percentage Points for a Generalized ESD Many-Outlier Procedure
ROSNER, B. A. (1983) · Technometrics · doi:10.1080/00401706.1983.10487848 · Cited by 1,204 · see citing works
Calvert, H., Horwich, A., Newlands, E. S., Beǵent, R. H. J., Rustin, G. J. S., Kaye, S. B., Harris, A. L., Williams, C. J., & Slevin, M. L. (1988) · The Lancet · doi:10.1016/s0140-6736(88)92709-2 · Cited by 1,183 · see citing works
The Long-Term Effects of Exposure to Low Doses of Lead in Childhood
Needleman, H. L., Schell, A., Bellinger, D. C., Leviton, A., & Allred, E. N. (1990) · New England Journal of Medicine · doi:10.1056/nejm199001113220203 · Cited by 1,156 · see citing works
DNA methylation in health and disease
Robertson, K. D., & Wolffe, A. P. (2000) · Nature Reviews Genetics · doi:10.1038/35049533 · Cited by 1,056 · see citing works
A simple method for estimating global DNA methylation using bisulfite PCR of repetitive DNA elements
Yang, A. S. (2004) · Nucleic Acids Research · doi:10.1093/nar/gnh032 · Cited by 1,033 · see citing works
Fetal programming and adult health
Godfrey, K. M., & Barker, D. J. P. (2001) · Public Health Nutrition · doi:10.1079/phn2001145 · Cited by 987 · see citing works
Dolinoy, D. C., Weidman, J. R., Waterland, R. A., & Jirtle, R. L. (2006) · Environmental Health Perspectives · doi:10.1289/ehp.8700 · Cited by 932 · see citing works
Birth weight and risk of cardiovascular disease in a cohort of women followed up since 1976
Rich-Edwards, J. W., Stampfer, M. J., Manson, J. E., ROSNER, B. A., Hankinson, S. E., Colditz, G. A., Hennekens, C. H., & Willett, W. C. (1997) · BMJ · doi:10.1136/bmj.315.7105.396 · Cited by 814 · see citing works
DNA hypomethylation and human diseases
Wilson, A. S., Power, B. E., & Molloy, P. L. (2007) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2006.08.007 · Cited by 804 · see citing works
Valinluck, V. (2004) · Nucleic Acids Research · doi:10.1093/nar/gkh739 · Cited by 756 · see citing works
Yi, P., Melnyk, S., Pogribna, M., Pogribny, I. P., Hine, R. J., & James, S. J. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m002725200 · Cited by 640 · see citing works
Changes in DNA Methylation Patterns in Subjects Exposed to Low-Dose Benzene
Bollati, V., Baccarelli, A., Hou, L., Bonzini, M., Fustinoni, S., Cavallo, D. M., Byun, H., Jiang, J., Marinelli, B., Pesatori, A. C., et al. (2007) · Cancer Research · doi:10.1158/0008-5472.can-06-2995 · Cited by 612 · see citing works
Endocrine Disruptor Vinclozolin Induced Epigenetic Transgenerational Adult-Onset Disease
Anway, M. D., Leathers, C. W., & Skinner, M. K. (2006) · Endocrinology · doi:10.1210/en.2006-0640 · Cited by 557 · see citing works
Epigenetic gene regulation: Linking early developmental environment to adult disease
Dolinoy, D. C., Weidman, J. R., & Jirtle, R. L. (2006) · Reproductive Toxicology · doi:10.1016/j.reprotox.2006.08.012 · Cited by 494 · see citing works
Wu, J., Basha, R. M., Brock, B., Cox, D. P., Cardozo‐Pelaez, F., McPherson, C. A., Harry, J., Rice, D. C., Maloney, B., Chen, D., et al. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.4405-07.2008 · Cited by 473 · see citing works
Large-scale structure of genomic methylation patternsPreprint
Rollins, R. A., Haghighi, F. G., Edwards, J. R., Das, R., Zhang, M. Q., Ju, J., & Bestor, T. H. (2005) · Genome Research · doi:10.1101/gr.4362006 · Cited by 389 · see citing works
Lead neurotoxicity: From exposure to molecular effects
Toscano, C. D., & Guilarte, T. R. (2005) · Brain Research Reviews · doi:10.1016/j.brainresrev.2005.02.004 · Cited by 387 · see citing works
James, S. J., Melnyk, S., Pogribna, M., Pogribny, I. P., & Caudill, M. A. (2002) · Journal of Nutrition · doi:10.1093/jn/132.8.2361s · Cited by 367 · see citing works
Changes in Bone Density With Lactation
Sowers, M. R. (1993) · JAMA · doi:10.1001/jama.1993.03500240074029 · Cited by 356 · see citing works
Basha, R. M., Wei, W., Bakheet, S. A., Benitez, N. B., Siddiqi, H. K., Ge, Y., Lahiri, D. K., & Zawia, N. H. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.4335-04.2005 · Cited by 353 · see citing works
Effects of Particulate Matter on Genomic DNA Methylation Content and iNOS Promoter Methylation
Tarantini, L., Bonzini, M., Apostoli, P., Pegoraro, V., Bollati, V., Marinelli, B., Cantone, L., Rizzo, G., Hou, L., Schwartz, J. D., et al. (2008) · Environmental Health Perspectives · doi:10.1289/ehp.11898 · Cited by 349 · see citing works
Waalkes, M. P., Ward, J. M., Liu, J., & Diwan, B. A. (2003) · Toxicology and Applied Pharmacology · doi:10.1016/s0041-008x(02)00022-4 · Cited by 343 · see citing works
Pregnancy increases mobilization of lead from maternal skeleton
Gulson, B. L., Jameson, C. W., Mahaffey, K. R., Mizon, K. J., Korsch, M. J., & Vimpani, G. (1997) · Journal of Laboratory and Clinical Medicine · doi:10.1016/s0022-2143(97)90058-5 · Cited by 319 · see citing works
Transplacental transport of lead.
Goyer, R. A. (1990) · Environmental Health Perspectives · doi:10.1289/ehp.9089101 · Cited by 305 · see citing works
Gulson, B. L., Mizon, K. J., Korsch, M. J., Palmer, J. M., & Donnelly, J. B. (2003) · The Science of The Total Environment · doi:10.1016/s0048-9697(02)00355-8 · Cited by 291 · see citing works
Lead intoxication: antioxidant defenses and oxidative damage in rat brain
Adonaylo, V. N., & Oteiza, P. I. (1999) · Toxicology · doi:10.1016/s0300-483x(99)00051-7 · Cited by 273 · see citing works
Estecio, M. R., Gharibyan, V., Shen, L., Ibrahim, A. E. K., Doshi, K. D., He, R. L., Jelı́nek, J., Yang, A. S., Yan, P. S., Huang, T. H. ‐., et al. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000399 · Cited by 270 · see citing works
Blood Lead Levels Measured Prospectively and Risk of Spontaneous Abortion
Borja‐Aburto, V. H., Hertz‐Picciotto, I., Lopez, M. R., Farías, P., Rı́os, C., & Blanco, J. (1999) · American Journal of Epidemiology · doi:10.1093/oxfordjournals.aje.a010057 · Cited by 251 · see citing works
Decrease in Birth Weight in Relation to Maternal Bone-Lead Burden
González‐Cossío, T., Peterson, K. E., Sanı́n, L.-H., Fishbein, E., Palazuelos, E., Aro, A., Hernández‐Ávila, M., & Hu, H. (1997) · PEDIATRICS · doi:10.1542/peds.100.5.856 · Cited by 236 · see citing works
Self-citationSurveillance for elevated blood lead levels among children--United States, 1997-2001.
Meyer, P. A., Pivetz, T., Dignam, T. A., Homa, D. M., Schoonover, J., & Brody, D. J. (2003) · PubMed · Cited by 165 · see citing works
Andrews, K. W., Savitz, D. A., & Hertz‐Picciotto, I. (1994) · American Journal of Industrial Medicine · doi:10.1002/ajim.4700260103 · Cited by 165 · see citing works
Xie, Y., Liu, J., Benbrahim‐Tallaa, L., Ward, J. M., Logsdon, D. L., Diwan, B. A., & Waalkes, M. P. (2007) · Toxicology · doi:10.1016/j.tox.2007.03.021 · Cited by 163 · see citing works
Choi, I., Estecio, M. R., Nagano, Y., Kim, D. H., White, J. A., Yao, J. C., Issa, J. J., & Rashid, A. (2007) · Modern Pathology · doi:10.1038/modpathol.3800825 · Cited by 161 · see citing works
Waalkes, M. P. (2003) · Carcinogenesis · doi:10.1093/carcin/bgg181 · Cited by 155 · see citing works
Maternal Bone Lead as an Independent Risk Factor for Fetal Neurotoxicity: A Prospective Study
Gomaa, A. E., Hu, H., Bellinger, D. C., Schwartz, J. D., Tsaih, S., González‐Cossío, T., Schnaas, L., Peterson, K. E., Aro, A., & Hernández‐Ávila, M. (2002) · PEDIATRICS · doi:10.1542/peds.110.1.110 · Cited by 149 · see citing works
Self-citationEffect of magnitude and timing of maternal pregnancy blood lead (Pb) levels on birth outcomes
Jelliffe‐Pawlowski, L. L., Miles, S., Courtney, J. G., Materna, B. L., & Charlton, V. (2006) · Journal of Perinatology · doi:10.1038/sj.jp.7211453 · Cited by 141 · see citing works
DNA Methylation, Genomic Imprinting, and Mammalian DevelopmentPreprint
Li, E., Beard, C., Forster, A. C., Bestor, T. H., & Jaenisch, R. (1993) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.1993.058.01.035 · Cited by 108 · see citing works
Improvements in the calibration of109Cd K X-ray fluorescence systems for measuring bone lead in vivo
Aro, A., Todd, A. C., Amarasiriwardena, C. J., & Hu, H. (1994) · Physics in Medicine and Biology · doi:10.1088/0031-9155/39/12/009 · Cited by 96 · see citing works
Self-citationAntonio-García, M. T., & Massó-González, E. L. (2008) · Food and Chemical Toxicology · doi:10.1016/j.fct.2008.01.053 · Cited by 91 · see citing works
Weight gain and maturity in fetuses exposed to low levels of lead
Bellinger, D. C., Leviton, A., Rabinowitz, M. B., Allred, E. N., Needleman, H. L., & Schoenbaum, S. C. (1991) · Environmental Research · doi:10.1016/s0013-9351(05)80097-0 · Cited by 79 · see citing works
Impact of Breastfeeding on the Mobilization of Lead from Bone
Téllez‐Rojo, M. M. (2002) · American Journal of Epidemiology · doi:10.1093/aje/155.5.420 · Cited by 67 · see citing works
Self-citationPerrin, D., Ballestar, E., Fraga, M. F., Frappart, L., Esteller, M., Guérin, J.-F., & Dante, R. (2006) · Oncogene · doi:10.1038/sj.onc.1210039 · Cited by 49 · see citing works
Changes in bone density with lactation
Sowers, M., Corton, G., Shapiro, B., Jannausch, M. L., Crutchfield, M., Smith, M., Randolph, J. F., & Hollis, B. W. (1994) · International Journal of Gynecology & Obstetrics · doi:10.1016/0020-7292(94)90210-0 · Cited by 41 · see citing works
BARLTROP, D. (1968) · Postgraduate Medical Journal · doi:10.1136/pgmj.44.513.537 · Cited by 40 · see citing works
The effect of on DNA methylation in isolated rat liver nuclei
Cox, R., Prescott, C., & Irving, C. C. (1977) · Biochimica et Biophysica Acta (BBA) - Nucleic Acids and Protein Synthesis · doi:10.1016/0005-2787(77)90070-3 · Cited by 31 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Environmental chemical exposures and human epigenetics
Hou, L., Zhang, X., Wang, D., & Baccarelli, A. (2011) · International Journal of Epidemiology · doi:10.1093/ije/dyr154 · Cited by 489 · see citing works
Zhang, F. F., Cardarelli, R., Carroll, J. F., Fulda, K. G., Kaur, M., González, K., Vishwanatha, J. K., Santella, R. M., & Morabia, A. (2011) · Epigenetics · doi:10.4161/epi.6.5.15335 · Cited by 399 · see citing works
Clinical and molecular aspects of lead toxicity: An update
Mitra, P., Sharma, S., Purohit, P., & Sharma, P. (2017) · Critical Reviews in Clinical Laboratory Sciences · doi:10.1080/10408363.2017.1408562 · Cited by 390 · see citing works
Developmental Neurotoxicants in E-Waste: An Emerging Health Concern
Chen, A., Dietrich, K. N., Huo, X., & Ho, S. (2010) · Environmental Health Perspectives · doi:10.1289/ehp.1002452 · Cited by 359 · see citing works
Teh, A. L., Pan, H., Chen, L., Ong, M.-L., Dogra, S., Wong, J., MacIsaac, J. L., Mah, S. M., McEwen, L. M., Saw, S.-M., et al. (2014) · Genome Research · doi:10.1101/gr.171439.113 · Cited by 352 · see citing works
DNA methylation in white blood cells
Terry, M. B., Delgado‐Cruzata, L., Vin‐Raviv, N., Wu, H. C., & Santella, R. M. (2011) · Epigenetics · doi:10.4161/epi.6.7.16500 · Cited by 318 · see citing works
Cortessis, V. K., Thomas, D. C., Levine, A. J., Breton, C. V., Mack, T. M., Siegmund, K. D., Haile, R. W., & Laird, P. W. (2012) · Human Genetics · doi:10.1007/s00439-012-1189-8 · Cited by 319 · see citing works
Comprehending the Body in the Era of the Epigenome
Lock, M. M. (2015) · Current Anthropology · doi:10.1086/680350 · Cited by 248 · see citing works
Biomarkers of Lead Exposure and DNA Methylation within Retrotransposons
Wright, R. O., Schwartz, J., Wright, R. J., Bollati, V., Tarantini, L., Park, S. K., Hu, H., Sparrow, D., Vokonas, P., & Baccarelli, A. (2010) · Environmental Health Perspectives · doi:10.1289/ehp.0901429 · Cited by 235 · see citing works
Self-citationRuiz-Hernandez, A., Kuo, C.-C., Rentero-Garrido, P., Tang, W., Redón, J., Ordovás, J. M., Navas‐Acién, A., & Téllez-Plaza, M. (2015) · Clinical Epigenetics · doi:10.1186/s13148-015-0055-7 · Cited by 208 · see citing works
Bakulski, K., Rozek, L., Dolinoy, D., Paulson, H., & Hu, H. (2012) · Current Alzheimer Research · doi:10.2174/156720512800617991 · Cited by 193 · see citing works
Self-citationWilhelm-Benartzi, C. S., Houseman, E. A., Maccani, M. A., Poage, G. M., Koestler, D. C., Langevin, S. M., Gagne, L. A., Banister, C. E., Padbury, J. F., & Marsit, C. J. (2011) · Environmental Health Perspectives · doi:10.1289/ehp.1103927 · Cited by 190 · see citing works
Environment, lifestyle, and Parkinson's disease: Implications for prevention in the next decade
Marras, C., Canning, C. G., & Goldman, S. M. (2019) · Movement Disorders · doi:10.1002/mds.27720 · Cited by 192 · see citing works
The Impact of Toxins on the Developing Brain
Lanphear, B. P. (2015) · Annual Review of Public Health · doi:10.1146/annurev-publhealth-031912-114413 · Cited by 186 · see citing works
Epigenetics and its implications for ecotoxicology
Vandegehuchte, M., & Janssen, C. (2011) · Ecotoxicology · doi:10.1007/s10646-011-0634-0 · Cited by 183 · see citing works
Neurodevelopmental Disorders and Environmental Toxicants: Epigenetics as an Underlying Mechanism
Tran, N. Q. V., & Miyake, K. (2017) · International Journal of Genomics · doi:10.1155/2017/7526592 · Cited by 183 · see citing works
Ray, P. D., Yosim, A. E., & Fry, R. C. (2014) · Frontiers in Genetics · doi:10.3389/fgene.2014.00201 · Cited by 178 · see citing works
Before the beginning: environmental exposures and reproductive and obstetrical outcomes
Segal, T. R., & Giudice, L. C. (2019) · Fertility and Sterility · doi:10.1016/j.fertnstert.2019.08.001 · Cited by 173 · see citing works
Keil, K. P., & Lein, P. J. (2016) · Environmental Epigenetics · doi:10.1093/eep/dvv012 · Cited by 167 · see citing works
Influence of Prenatal Arsenic Exposure and Newborn Sex on Global Methylation of Cord Blood DNA
Pilsner, J. R., Hall, M. N., Liu, X., Ilievski, V., Slavkovich, V. N., Levy, D., Factor-Litvak, P. R., Yunus, M., Rahman, M., Graziano, J. H., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0037147 · Cited by 160 · see citing works
Self-citationHypothesis: Environmental regulation of 5-hydroxymethylcytosine by oxidative stress
Chia, N., Wang, L., Lu, X., Senut, M., Brenner, C. A., & Ruden, D. M. (2011) · Epigenetics · doi:10.4161/epi.6.7.16461 · Cited by 157 · see citing works
Sanders, A. P., Smeester, L., Rojas, D., DeBussycher, T., Wu, M. C., Wright, F. A., Zhou, Y., Laine, J. E., Rager, J. E., Swamy, G. K., et al. (2013) · Epigenetics · doi:10.4161/epi.26798 · Cited by 154 · see citing works
Epigenetics of early-life lead exposure and effects on brain development
Senut, M.-C., Cingolani, P., Sen, A., Kruger, A., Shaik, A., Hirsch, H., Suhr, S. T., & Ruden, D. (2012) · Epigenomics · doi:10.2217/epi.12.58 · Cited by 151 · see citing works
Pilsner, J. R., Zagel, A. L., Nam, D., Letcher, R. J., Sonne, C., Dietz, R., & Basu, N. (2009) · Molecular Ecology · doi:10.1111/j.1365-294x.2009.04452.x · Cited by 148 · see citing works
Self-citationResponse of transposable elements to environmental stressors
Miousse, I. R., Chalbot, M. G., Lumen, A., Ferguson, A., Kavouras, I. G., & Koturbash, I. (2015) · Mutation Research/Reviews in Mutation Research · doi:10.1016/j.mrrev.2015.05.003 · Cited by 144 · see citing works
DNA methylation, early life environment, and health outcomes
Mitchell, C., Schneper, L. M., & Notterman, D. A. (2016) · Pediatric Research · doi:10.1038/pr.2015.193 · Cited by 146 · see citing works
Genotoxic and epigenetic mechanisms in arsenic carcinogenicity
Bustaffa, E., Stoccoro, A., Bianchi, F., & Migliore, L. (2014) · Archives of Toxicology · doi:10.1007/s00204-014-1233-7 · Cited by 144 · see citing works
Gundacker, C., Genčík, M., & Hengstschläger, M. (2010) · Mutation Research/Reviews in Mutation Research · doi:10.1016/j.mrrev.2010.06.003 · Cited by 142 · see citing works
Gundacker, C., Forsthuber, M., Szigeti, T., Kakucs, R., Mustieles, V., Fernandez, M. F., Bengtsen, E., Vogel, U., Hougaard, K. S., & Saber, A. T. (2021) · International Journal of Hygiene and Environmental Health · doi:10.1016/j.ijheh.2021.113855 · Cited by 135 · see citing works
Insulin-Like Growth Factor 2/H19 Methylation at Birth and Risk of Overweight and Obesity in Children
Perkins, E., Murphy, S. K., Murtha, A. P., Schildkraut, J. M., Jirtle, R. L., Demark‐Wahnefried, W., Forman, M. R., Kurtzberg, J., Overcash, F. M., Huang, Z., et al. (2012) · The Journal of Pediatrics · doi:10.1016/j.jpeds.2012.01.015 · Cited by 135 · see citing works
Senut, M.-C., Sen, A., Cingolani, P., Shaik, A., Land, S. J., & Ruden, D. M. (2014) · Toxicological Sciences · doi:10.1093/toxsci/kfu028 · Cited by 135 · see citing works
Prenatal epigenetics diets play protective roles against environmental pollution
Li, S.-Z., Chen, M., Li, Y.-Y., & Tollefsbol, T. (2019) · Clinical Epigenetics · doi:10.1186/s13148-019-0659-4 · Cited by 103 · see citing works
The Impact of External Factors on the Epigenome:In Uteroand over Lifetime
Toraño, E. G., García, M. G., Fernández-Morera, J. L., García, P. N., & Fernández, A. F. (2016) · BioMed Research International · doi:10.1155/2016/2568635 · Cited by 125 · see citing works
Environmental influences on reproductive health: the importance of chemical exposures
Wang, A., Padula, A. M., Sirota, M., & Woodruff, T. J. (2016) · Fertility and Sterility · doi:10.1016/j.fertnstert.2016.07.1076 · Cited by 120 · see citing works
Schneider, J. S., Kidd, S. K., & Anderson, D. W. (2013) · Toxicology Letters · doi:10.1016/j.toxlet.2012.12.004 · Cited by 115 · see citing works
Epigenetic epidemiology: Promises for public health research
Bakulski, K. M., & Fallin, M. D. (2014) · Environmental and Molecular Mutagenesis · doi:10.1002/em.21850 · Cited by 112 · see citing works
Maternal choline supplementation: a nutritional approach for improving offspring health?
Jiang, X., West, A. A., & Caudill, M. A. (2014) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2014.02.001 · Cited by 112 · see citing works
Baïz, N., Slama, R., Béné, M. C., Charles, M.-A. A., Kolopp‐Sarda, M., Magnan, A., Thiébaugeorges, O., Faure, G. C., & Annesi‐Maesano, I. (2011) · BMC Pregnancy and Childbirth · doi:10.1186/1471-2393-11-87 · Cited by 111 · see citing works
Breton, C. V., Yao, J., Millstein, J., Gao, L., Siegmund, K. D., Mack, W. J., Whitfield, L., Lurmann, F. W., Hodis, H. N., Avol, E., et al. (2016) · Environmental Health Perspectives · doi:10.1289/ehp181 · Cited by 109 · see citing works
Effects of Prenatal Exposure to Endocrine Disruptors and Toxic Metals on The Fetal Epigenome
Bommarito, P. A., Martin, E. M., & Fry, R. C. (2017) · Epigenomics · doi:10.2217/epi-2016-0112 · Cited by 105 · see citing works
Programming of respiratory health in childhood
Wright, R. J., & Brunst, K. J. (2013) · Current Opinion in Pediatrics · doi:10.1097/mop.0b013e32835e78cc · Cited by 106 · see citing works
Self-citationPrenatal Smoke Exposure and Genomic DNA Methylation in a Multiethnic Birth Cohort
Flom, J. D., Ferris, J. S., Liao, Y., Tehranifar, P., Belessiotis‐Richards, C., Cho, Y. H., González, K., Santella, R. M., & Terry, M. B. (2011) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-11-0553 · Cited by 104 · see citing works
Epigenetic Basis of Lead-Induced Neurological Disorders
Wang, T., Zhang, J., & Xu, Y. (2020) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph17134878 · Cited by 98 · see citing works
Epigenetic mechanisms in metal toxicity
Fragou, D., Fragou, A., Kouidou, S., Njau, S. N., & Kovatsi, L. (2011) · Toxicology Mechanisms and Methods · doi:10.3109/15376516.2011.557878 · Cited by 97 · see citing works
Association between Prenatal Lead Exposure and Blood Pressure in Children
Zhang, A., Hu, H., Sánchez, B. N., Ettinger, A. S., Park, S. K., Cantonwine, D. E., Schnaas, L., Wright, R. O., Lamadrid‐Figueroa, H., & Téllez‐Rojo, M. M. (2011) · Environmental Health Perspectives · doi:10.1289/ehp.1103736 · Cited by 96 · see citing works
Self-citationBurris, H. H., Braun, J. M., Byun, H., Tarantini, L., Mercado, A., Wright, R. J., Schnaas, L., Baccarelli, A., Wright, R. O., & Téllez‐Rojo, M. M. (2013) · Epigenomics · doi:10.2217/epi.13.24 · Cited by 96 · see citing works
Self-citationEpigenetics and environmental exposures
Stein, R. A. (2011) · Journal of Epidemiology & Community Health · doi:10.1136/jech.2010.130690 · Cited by 94 · see citing works
Global LINE-1 DNA methylation is associated with blood glycaemic and lipid profiles
Pearce, M. S., McConnell, J. C., Potter, C., Barrett, L. M., Parker, L., Mathers, J. C., & Relton, C. L. (2012) · International Journal of Epidemiology · doi:10.1093/ije/dys020 · Cited by 91 · see citing works
Callaghan, B. C., Feldman, D. J., Gruis, K. L., & Feldman, E. L. (2010) · Neurodegenerative Diseases · doi:10.1159/000315405 · Cited by 92 · see citing works
Vaiserman, A. (2015) · Clinical Epigenetics · doi:10.1186/s13148-015-0130-0 · Cited by 91 · see citing works
Activity-dependent synaptic plasticity modulates the critical phase of brain development
Chaudhury, S., Sharma, V., Kumar, V., Nag, T. C., & Wadhwa, S. (2015) · Brain and Development · doi:10.1016/j.braindev.2015.10.008 · Cited by 92 · see citing works
Sánchez, O. F., Lee, J.-Y., Hing, N. Y. K., Kim, S.-E., Freeman, J. L., & Yuan, C. (2016) · Metallomics · doi:10.1039/c6mt00198j · Cited by 88 · see citing works
Metal mining and birth defects: a case-control study in Lubumbashi, Democratic Republic of the Congo
Brusselen, D. V., Kayembe‐Kitenge, T., Mbuyi‐Musanzayi, S., Lubala, T. K., Ngombe, L. K., Obadia, P. M., Mukoma, D. K. W., Herck, K. V., Avonts, D., Devriendt, K., et al. (2020) · The Lancet Planetary Health · doi:10.1016/s2542-5196(20)30059-0 · Cited by 88 · see citing works
Leung, Y., Ouyang, B., Niu, L., Xie, C., Ying, J., Medvedovic, M., Chen, A., Weihe, P., Valvi, D., Grandjean, P., et al. (2018) · Epigenetics · doi:10.1080/15592294.2018.1445901 · Cited by 89 · see citing works
LINE ‐1 hypomethylation in spermatozoa is associated with Bisphenol A exposure
Miao, M., Zhou, X., Li, Y., Zhang, O. G. H., Zhou, Z., Li, T., Yuan, W., Li, R., & Li, D. (2013) · Andrology · doi:10.1111/j.2047-2927.2013.00166.x · Cited by 88 · see citing works
El‐Maarri, O., Walier, M., Behne, F., van Üüm, J., Singer, H., Diaz-Lacava, A. N., Nüsgen, N., Niemann, B., Watzka, M., REINSBERG, J., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0016252 · Cited by 86 · see citing works
Chung, F. F., & Herceg, Z. (2020) · Environmental Health Perspectives · doi:10.1289/ehp6104 · Cited by 86 · see citing works
Epigenetics, Obesity and Early-Life Cadmium or Lead Exposure
Park, S., Skaar, D. A., Jirtle, R. L., & Hoyo, C. (2016) · Epigenomics · doi:10.2217/epi-2016-0047 · Cited by 83 · see citing works
Mei, M., Song, H., Chen, L., Hu, B., Bai, R., Xu, D., Liu, Y., Zhao, Y., & Chen, C. (2018) · Particle and Fibre Toxicology · doi:10.1186/s12989-018-0249-1 · Cited by 80 · see citing works
Gestational Exposure to Urban Air Pollution Related to a Decrease in Cord Blood Vitamin D Levels
Baïz, N., Dargent‐Molina, P., Wark, J. D., Souberbielle, J., Slama, R., Annesi‐Maesano, I., & the EDEN Mother-Child Cohort Study Group (2012) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2012-1943 · Cited by 81 · see citing works
Trojsi, F., Monsurrò, M. R., & Tedeschi, G. (2013) · International Journal of Molecular Sciences · doi:10.3390/ijms140815286 · Cited by 78 · see citing works
Sutton, P., Woodruff, T. J., Perron, J. L., Stotland, N. E., Conry, J. A., Miller, M. D., & Giudice, L. C. (2012) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2012.01.034 · Cited by 79 · see citing works
Appleton, A. A., Jackson, B. P., Karagas, M. R., & Marsit, C. J. (2017) · Epigenetics · doi:10.1080/15592294.2017.1320637 · Cited by 76 · see citing works
Ou, Y., Bloom, M. S., Nie, Z., Han, F., Mai, J., Chen, J., Lin, S., Liu, X., & Zhuang, J. (2017) · Environment International · doi:10.1016/j.envint.2017.05.017 · Cited by 77 · see citing works
Brown, T. A., Lee, J. W., Holian, A., Porter, V., Fredriksen, H., Kim, M.-J., & Cho, Y. H. (2015) · Nanotoxicology · doi:10.3109/17435390.2015.1078852 · Cited by 72 · see citing works
Wu, H., Delgado‐Cruzata, L., Flom, J. D., Perrin, M. C., Liao, Y., Ferris, J. S., Santella, R. M., & Terry, M. B. (2012) · Carcinogenesis · doi:10.1093/carcin/bgs201 · Cited by 71 · see citing works
Li, Y., Xie, C., Murphy, S. K., Skaar, D. A., Nye, M. D., Vidal, A. C., Cecil, K. M., Dietrich, K. N., Puga, A., Jirtle, R. L., et al. (2015) · Environmental Health Perspectives · doi:10.1289/ehp.1408577 · Cited by 71 · see citing works
Sex-Dependent Effects of Developmental Lead Exposure on the Brain
Singh, G., Singh, V., Sobolewski, M., Cory‐Slechta, D. A., & Schneider, J. S. (2018) · Frontiers in Genetics · doi:10.3389/fgene.2018.00089 · Cited by 71 · see citing works
The role of epigenetic dysregulation in the epidemic of allergic disease
Prescott, S. L., & Saffery, R. (2011) · Clinical Epigenetics · doi:10.1007/s13148-011-0028-4 · Cited by 70 · see citing works
Epigenetic marker (LINE-1 promoter) methylation level was associated with occupational lead exposure
Li, C., Yang, X., Xu, M. J., Zhang, J., & Sun, N. (2013) · Clinical Toxicology · doi:10.3109/15563650.2013.782410 · Cited by 71 · see citing works
Delgado‐Cruzata, L., Zhang, W., McDonald, J. A., Tsai, W. Y., Valdovinos, C., Falci, L., Wang, Q., Crew, K. D., Santella, R. M., Hershman, D. L., et al. (2015) · Journal of Nutrition · doi:10.3945/jn.114.202853 · Cited by 69 · see citing works
Winans, B., Nagari, A., Chae, M., Post, C. M., Ko, C.-Y. J., Puga, A., Kraus, W. L., & Lawrence, B. P. (2015) · The Journal of Immunology · doi:10.4049/jimmunol.1402044 · Cited by 67 · see citing works
Sen, A., Cingolani, P., Senut, M., Land, S. J., Mercado‐García, A., Téllez‐Rojo, M. M., Baccarelli, A., Wright, R. O., & Ruden, D. M. (2015) · Epigenetics · doi:10.1080/15592294.2015.1050172 · Cited by 67 · see citing works
Self-citationEnvironmental Exposure to Lead (Pb) and Variations in Its Susceptibility
Kim, J.-A., Lee, Y., & Yang, M. (2014) · Journal of Environmental Science and Health Part C · doi:10.1080/10590501.2014.907461 · Cited by 67 · see citing works
Alu and LINE-1 methylation and lung function in the normative ageing study
Lange, N. E., Sordillo, J. E., Tarantini, L., Bollati, V., Sparrow, D., Vokonas, P., Zanobetti, A., Schwartz, J. D., Baccarelli, A., Litonjua, A. A., et al. (2012) · BMJ Open · doi:10.1136/bmjopen-2012-001231 · Cited by 65 · see citing works
Wang, G., DiBari, J., Bind, E. P., Steffens, A. M., Mukherjee, J., Azuine, R. E., Singh, G. K., Hong, X., Ji, Y., Ji, H., et al. (2019) · JAMA Network Open · doi:10.1001/jamanetworkopen.2019.12343 · Cited by 65 · see citing works
Alvarado-Cruz, I., Alegría‐Torres, J. A., Montes-Castro, N., Jiménez-Garza, O., & Quintanilla‐Vega, B. (2018) · Annals of Global Health · doi:10.29024/aogh.909 · Cited by 66 · see citing works
Zeng, Z., Huo, X., Zhang, Y., Hylkema, M. N., Wu, Y., & Xu, X. (2019) · Environmental Research · doi:10.1016/j.envres.2019.01.007 · Cited by 63 · see citing works
Early life exposure to lead (Pb) and changes in DNA methylation: relevance to Alzheimer’s disease
Bihaqi, S. W. (2019) · Reviews on Environmental Health · doi:10.1515/reveh-2018-0076 · Cited by 63 · see citing works
Castillo, P., Ibanez-Carrasco, F., Guajardo, A., Llanos, M. N., & Ronco, A. M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0044139 · Cited by 62 · see citing works
Maternal lead exposure and risk of congenital heart defects occurrence in offspring
Liu, Z., Yu, Y., Li, X., Wu, A., Mu, M., Li, N., Deng, Y., Jin, X., Li, S., Lin, Y., et al. (2014) · Reproductive Toxicology · doi:10.1016/j.reprotox.2014.11.002 · Cited by 61 · see citing works
Li, C., Xu, M. J., Wang, S., Yang, X., Zhou, S., Zhang, J., Liu, Q., & Sun, Y. (2011) · Toxicology Letters · doi:10.1016/j.toxlet.2011.03.002 · Cited by 60 · see citing works
Leter, G., Consales, C., Eleuteri, P., Uccelli, R., Specht, I. O., Toft, G. V., Moccia, T., Budillon, A., Jönsson, B., Lindh, C. H., et al. (2014) · Environmental and Molecular Mutagenesis · doi:10.1002/em.21874 · Cited by 60 · see citing works
Lead (Pb) exposure induces disturbances in epigenetic status in workers exposed to this metal
Devóz, P. P., Gomes, W. R., de Araújo, M. L., Ribeiro, D. L., Pedron, T., Antunes, L. M. G., Batista, B. L., Barbosa, F., & Barcelos, G. R. M. (2017) · Journal of Toxicology and Environmental Health · doi:10.1080/15287394.2017.1357364 · Cited by 61 · see citing works
Developmental exposure to Pb2+ induces transgenerational changes to zebrafish brain transcriptome
Meyer, D. N., Crofts, E. J., Akemann, C., Gurdziel, K., Farr, R. L., Baker, B. B., Weber, D. N., & Baker, T. R. (2019) · Chemosphere · doi:10.1016/j.chemosphere.2019.125527 · Cited by 55 · see citing works
Bozack, A. K., Rifas‐Shiman, S. L., Coull, B. A., Baccarelli, A., Wright, R. O., Amarasiriwardena, C. J., Gold, D. R., Oken, E., Hivert, M., & Cárdenas, A. (2021) · Clinical Epigenetics · doi:10.1186/s13148-021-01198-z · Cited by 54 · see citing works
Self-citationEcogenetics of lead toxicity and its influence on risk assessment
Mani, M. S., Kabekkodu, S. P., Joshi, M. B., & Dsouza, H. S. (2019) · Human & Experimental Toxicology · doi:10.1177/0960327119851253 · Cited by 55 · see citing works
Cuomo, D., Foster, M., & Threadgill, D. W. (2022) · Environmental Science and Pollution Research · doi:10.1007/s11356-022-19333-5 · Cited by 56 · see citing works
Goodrich, J. M., Sánchez, B. N., Dolinoy, D. C., Zhang, Z., Hernández‐Ávila, M., Hu, H., Peterson, K. E., & Téllez‐Rojo, M. M. (2015) · Epigenetics · doi:10.4161/15592294.2014.989077 · Cited by 54 · see citing works
Self-citationSchwartz, J. D., Bellinger, D. C., & Glass, T. A. (2011) · American Journal of Public Health · doi:10.2105/ajph.2011.300272 · Cited by 52 · see citing works
Subramanyam, M. A., Roux, A. V. D., Pilsner, J. R., Villamor, E., Donohue, K. M., Liu, Y., & Jenny, N. S. (2013) · PLoS ONE · doi:10.1371/journal.pone.0054018 · Cited by 50 · see citing works
Self-citationPrenatal exposure to lead in Spain: Cord blood levels and associated factors
Llop, S., Aguinagalde, X., Vioqué, J., Ibarluzea, J. M., Guxens, M., Casas, M., Murcia, M., Ruiz‐Castell, M., Amurrio, A., Rebagliato, M., et al. (2011) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2011.02.004 · Cited by 50 · see citing works
Health repercussions of environmental exposure to lead: Methylation perspective
Shiek, S. S., Mani, M. S., Kabekkodu, S. P., & Dsouza, H. S. (2021) · Toxicology · doi:10.1016/j.tox.2021.152927 · Cited by 49 · see citing works
DNA Methylation in Schizophrenia Subjects: Gender and <i>MTHFR</i> 677C/T Genotype Differences
Burghardt, K. J., Pilsner, J. R., Bly, M. J., & Ellingrod, V. L. (2012) · Epigenomics · doi:10.2217/epi.12.25 · Cited by 49 · see citing works
Self-citationSingh, G., Singh, V., Wang, Z., Voisin, G., Lefebvre, F., Navenot, J.-M., Evans, B. J., Verma, M., Anderson, D. W., & Schneider, J. S. (2018) · Toxicology Letters · doi:10.1016/j.toxlet.2018.03.021 · Cited by 50 · see citing works
Nye, M. D., King, K. E., Darrah, T. H., Maguire, R. L., Jima, D. D., Huang, Z., Méndez, M. A., Fry, R. C., Jirtle, R. L., Murphy, S. K., et al. (2016) · Current Zoology · doi:10.1093/eep/dvv009 · Cited by 47 · see citing works
Onuzulu, C. D., Rotimi, O. A., & Rotimi, S. O. (2019) · Reviews on Environmental Health · doi:10.1515/reveh-2018-0059 · Cited by 47 · see citing works
Early-Life Lead Exposure: Risks and Neurotoxic Consequences
Bjørklund, G., Tippairote, T., Hangan, T., Chirumbolo, S., & Peana, M. (2023) · Current Medicinal Chemistry · doi:10.2174/0929867330666230409135310 · Cited by 48 · see citing works
Developmental Plasticity, Epigenetics and Human Health
Low, F. M., Gluckman, P. D., & Hanson, M. A. (2012) · Evolutionary Biology · doi:10.1007/s11692-011-9157-0 · Cited by 45 · see citing works
Nakayama, S. M. M., Nakata, H., Ikenaka, Y., Yabe, J., Oroszlany, B., Yohannes, Y. B., Bortey‐Sam, N., Muzandu, K. M., Choongo, K., Kuritani, T., et al. (2019) · Environmental Pollution · doi:10.1016/j.envpol.2019.05.038 · Cited by 46 · see citing works
- Authors
- Pilsner, J. R., Hu, H., Ettinger, A., Sánchez, B. N., Wright, R. O., Cantonwine, D., Lazarus, A., Lamadrid-Figueroa, H., Mercado-García, A., Téllez-Rojo, M. M., & Hernández-Avila, M.
- Affiliations
- University of Michigan (US)
- Brigham and Women's Hospital (US)
- Department of Epidemiology, University of Michigan School of Public Health, Ann Arbor, Michigan, USA
- Division of Program Evaluation and Biostatistics, Center for Evaluation Research and Surveys, National Institute of Public Health, Cuernavaca, Morelos, Mexico
- Division of Environmental Health, Center for Population Health Research, National Institute of Public Health, Mexico City, Mexico
- Ministry of Health, Mexico City, Mexico
- Corresponding author
- Pilsner, J. Richard
- ORCID
- Venue
- Environmental Health Perspectives
- Publisher
- American Chemical Society (ACS)
- Published
- 2009-03-25
- Volume
- 117
- Issue
- 9
- Pages
- 1466-1471
- ISSN
- 0091-6765 (ISSN-L)
- 1552-9924
- PMC
- PMC2737027
- OpenAlex
- W2088501324
- Cited by
- 275
- References
- 53
- Citations by year
- 2026: 5 · 2025: 7 · 2024: 5 · 2023: 12 · 2022: 15 · 2021: 18 · 2020: 14 · 2019: 22 · 2018: 18 · 2017: 15 · 2016: 14 · 2015: 25 · 2014: 26 · 2013: 17 · 2012: 23
- FWCI
- 14.22
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- public-domain
- creativecommons.org/licenses/by/4.0/ (vor, 3201 d)
- Locations
- Environmental Health Perspectives (publishedVersion, public-domain)
- PubMed Central (publishedVersion, public-domain)
- PubMed (publishedVersion)
- Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
- Funders
- U.S. Environmental Protection Agency (R01 ES013744, P42 ES05947, P01 ES012874, 83172501, R01 ES007821, R01 ES014930, RD-83172501)
- Consejo Nacional de Ciencia y Tecnología (P01 ES012874, P42 ES05947, R01 ES007821, R01 ES014930, RD-83172501, 4150M9405, R01 ES013744)
- National Institutes of Health (ES-00002)
- National Institute of Environmental Health Sciences (P 42-ES05947, K23ES000381, R01ES014930, ES05947, P01ES012874, R01ES007821, ES014930, ES013744, ES 007821, P42ES005947, P30ES000002, K01ES014907, R01ES020268, P30-ES00002, ES 00002, RD-83172501, R01ES013744)
- Topics
- Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Heavy Metal Exposure and Toxicity
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Keywords
- prenatal lead exposure, DNA methylation, umbilical cord blood, LINE-1 methylation, fetal programming, epigenetic programming, environmental toxins, developmental toxicity
- MeSH terms
- Base Sequence, Environmental Pollutants, Female, Fetal Blood, Humans, Lead, Mexico, Polymerase Chain Reaction, DNA Primers, Maternal Exposure, DNA Methylation
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