Abstract
Background and objectives
Infant weight patterns predict subsequent weight outcomes. Rapid infant weight gain, defined as a >0.67 increase in weight-for-age z-score (WAZ) between two time points in infancy, increases obesity risk. Higher oxidative stress, an imbalance between antioxidants and reactive oxygen species, has been associated with low birthweight and paradoxically also with later obesity. We hypothesized that prenatal oxidative stress may also be associated with rapid infant weight gain, an early weight pattern associated with future obesity.
Methods
Within the NYU Children’s Health and Environment Study prospective pregnancy cohort, we analyzed associations between prenatal lipid, protein, and DNA urinary oxidative stress biomarkers and infant weight data. Primary outcome was rapid infant weight gain (>0.67 increase in WAZ) between birth and later infancy at the 8 or 12 month visit. Secondary outcomes included: very rapid weight gain (>1.34 increase in WAZ), low (<2500 g) or high (≥4000 g) birthweight, and low (< −1 WAZ) or high (>1 WAZ) 12 month weight.
Results
Pregnant participants consented to the postnatal study (n = 541); 425 participants had weight data both at birth and in later infancy. In an adjusted binary model, prenatal 8-iso-PGF2α, a lipid oxidative stress biomarker, was associated with rapid infant weight gain (aOR 1.44; 95% CI: 1.16, 1.78, p = 0.001). In a multinomial model using ≤0.67 change in WAZ as a reference group, 8-iso-PGF2α was associated with rapid infant weight gain (defined as >0.67 but ≤1.34 WAZ; aOR 1.57, 95% CI: 1.19, 2.05, p = 0.001) and very rapid infant weight gain (defined as >1.34 WAZ; aOR 1.33; 95% CI: 1.02, 1.72, p < 0.05) Secondary analyses detected associations between 8-iso-PGF2α and low birthweight outcomes.
Conclusions
We found an association between 8-iso-PGF2α, a lipid prenatal oxidative stress biomarker, and rapid infant weight gain, expanding our understanding of the developmental origins of obesity and cardiometabolic disease.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$259.00 per year
only $21.58 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
Data availability
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Ward ZJ, Long MW, Resch SC, Giles CM, Cradock AL, Gortmaker SL. Simulation of growth trajectories of childhood obesity into adulthood. N Engl J Med. 2017;377:2145–53.
Zheng M, Lamb KE, Grimes C, Laws R, Bolton K, Ong KK, et al. Rapid weight gain during infancy and subsequent adiposity: a systematic review and meta-analysis of evidence. Obes Rev. 2018;19:321–32.
Bichteler A, Gershoff ET. Identification of children’s BMI trajectories and prediction from weight gain in infancy. Obesity. 2018;26:1050–6.
Ong KK, Ahmed ML, Emmett PM, Preece MA, Dunger DB. Association between postnatal catch-up growth and obesity in childhood: prospective cohort study. BMJ. 2000;320:967–71.
Arisaka O, Ichikawa G, Koyama S, Sairenchi T. Childhood obesity: rapid weight gain in early childhood and subsequent cardiometabolic risk. Clin Pediatr Endocrinol. 2020;29:135–42.
Ong KK, Loos RJF. Rapid infancy weight gain and subsequent obesity: systematic reviews and hopeful suggestions. Acta Paediatr. 2006;95:904–8.
Felder JN, Epel E, Coccia M, Cordeiro A, Laraia B, Adler N, et al. Prenatal maternal objective and subjective stress exposures and rapid infant weight gain. J Pediatr. 2020;222:45–51.
Higdon JV, Frei B. Obesity and oxidative stress: a direct link to CVD? Arterioscler Thromb Vasc Biol. 2003;23:365–7.
Loy SL, Sirajudeen KNS, Hamid, Jan JM. The effects of prenatal oxidative stress levels on infant adiposity development during the first year of life. J Dev Orig Health Dis. 2014;5:142–51.
Weber D, Stuetz W, Bernhard W, Franz A, Raith M, Grune T, et al. Oxidative stress markers and micronutrients in maternal and cord blood in relation to neonatal outcome. Eur J Clin Nutr. 2014;68:215–22.
Vincent HK, Innes KE, Vincent KR. Oxidative stress and potential interventions to reduce oxidative stress in overweight and obesity. Diabetes, Obes Metab. 2007;9:813–39.
Arogbokun O, Rosen E, Keil AP, Milne GL, Barrett E, Nguyen R, et al. Maternal oxidative stress biomarkers in pregnancy and child growth from birth to age 6. J Clin Endocrinol Metab. 2021;106:1427–36.
Ho E, Karimi Galougahi K, Liu CC, Bhindi R, Figtree GA. Biological markers of oxidative stress: applications to cardiovascular research and practice. Redox Biol. 2013;1:483–91.
Martinez MP, Kannan K. Simultaneous analysis of seven biomarkers of oxidative damage to lipids, proteins, and DNA in urine. Environ Sci Technol. 2018;52:6647–55.
Eick SM, Geiger SD, Alshawabkeh A, Aung M, Barrett E, Bush NR, et al. Environmental influences on Child Health Outcomes. Associations between social, biologic, and behavioral factors and biomarkers of oxidative stress during pregnancy: findings from four ECHO cohorts. Sci Total Environ. 2022;835:155596.
Oguntibeju OO. Type 2 diabetes mellitus, oxidative stress and inflammation: examining the links. Int J Physiol Pathophysiol Pharmacol. 2019;11:45–63.
Li H, Yin Q, Li N, Ouyang Z, Zhong M. Plasma markers of oxidative stress in patients with gestational diabetes mellitus in the second and third trimester. Obstet Gynecol Int. 2016;2016:e3865454
Frijhoff J, Winyard PG, Zarkovic N, Davies SS, Stocker R, Cheng D, et al. Clinical relevance of biomarkers of oxidative stress. Antioxid Redox Signal. 2015;23:1144–70.
Trasande L, Ghassabian A, Kahn LG, Jacobson MH, Afanasyeva Y, Liu M, et al. The NYU Children’s Health and Environment Study. Eur J Epidemiol. 2020;35:305–20.
Gallardo JM, Gómez-López J, Medina-Bravo P, Juárez-Sánchez F, Contreras-Ramos A, Galicia-Esquivel M, et al. Maternal obesity increases oxidative stress in the newborn. Obesity. 2015;23:1650–4.
Kim YJ, Hong YC, Lee KH, Park HJ, Park EA, Moon HS, et al. Oxidative stress in pregnant women and birth weight reduction. Reprod Toxicol. 2005;19:487–92.
Koo TK, Li MY. A guideline of selecting and reporting intraclass correlation coefficients for reliability research. J Chiropr Med. 2016;15:155–63.
Roberts LJ, Morrow JD. Measurement of F(2)-isoprostanes as an index of oxidative stress in vivo. Free Radic Biol Med. 2000;28:505–13.
About the Program | National Biomonitoring Program | CDC [Internet]. 2021 [cited 2022 Nov 14]. Available from: https://www.cdc.gov/biomonitoring/about.html.
Hornung RW, Reed LD. Estimation of average concentration in the presence of nondetectable values. Appl Occup Environ Hyg. 1990;5:46–51.
Martinez-Moral MP, Kannan K. How stable is oxidative stress level? An observational study of intra- and inter-individual variability in urinary oxidative stress biomarkers of DNA, proteins, and lipids in healthy individuals. Environ Int. 2019;123:382–9.
O’Brien KM, Upson K, Cook NR, Weinberg CR. Environmental chemicals in urine and blood: improving methods for creatinine and lipid adjustment. Environ Health Perspect. 2016;124:220–7.
Villar J, Cheikh Ismail L, Victora CG, Ohuma EO, Bertino E, Altman DG, et al. International Fetal and Newborn Growth Consortium for the 21st Century (INTERGROWTH-21st). International standards for newborn weight, length, and head circumference by gestational age and sex: the Newborn Cross-Sectional Study of the INTERGROWTH-21st Project. Lancet. 2014;384:857–68.
WHO Multicentre Growth Reference Study Group. WHO Child Growth Standards based on length/height, weight and age. Acta Paediatr Suppl. 2006;450:76–85.
Druet C, Stettler N, Sharp S, Simmons RK, Cooper C, Davey Smith G, et al. Prediction of childhood obesity by infancy weight gain: an individual-level meta-analysis. Paediatric Perinat Epidemiol. 2012;26:19–26.
Wang G, Johnson S, Gong Y, Polk S, Divall S, Radovick S, et al. Weight gain in infancy and overweight or obesity in childhood across the gestational spectrum: a prospective birth cohort study. Sci Rep Nat Publ Group. 2016;6:29867.
Cutland CL, Lackritz EM, Mallett-Moore T, Bardají A, Chandrasekaran R, Lahariya C, et al. Low birth weight: case definition & guidelines for data collection, analysis, and presentation of maternal immunization safety data. Vaccine. 2017;35:6492–6500.
Ouzounian JG, Hernandez GD, Korst LM, Montoro MM, Battista LR, Walden CL, et al. Pre-pregnancy weight and excess weight gain are risk factors for macrosomia in women with gestational diabetes. J Perinatol. 2011;31:717–21.
Mei Z, Grummer-Strawn LM. Standard deviation of anthropometric Z-scores as a data quality assessment tool using the 2006 WHO growth standards: a cross country analysis. Bull World Health Organ. 2007;85:441–8.
Chen SY, Feng Z, Yi X. A general introduction to adjustment for multiple comparisons. J Thorac Dis. 2017;9:1725–9.
Furukawa S, Fujita T, Shimabukuro M, Iwaki M, Yamada Y, Nakajima Y, et al. Increased oxidative stress in obesity and its impact on metabolic syndrome. J Clin Invest. 2004;114:1752–61.
Singhal A. Long-term adverse effects of early growth acceleration or catch-up growth. Ann Nutr Metab. 2017;70:236–40.
Barker D, Osmond C. Infant mortality, childhood nutrition, ischaemic heart disease in England and Wales. Lancet. 1986;327:1077–81.
Cusick SE, Georgieff MK. The role of nutrition in brain development: the golden opportunity of the “First 1000 Days”. J Pediatr. 2016;175:16–21.
Yao D, Chang Q, Wu QJ, Gao SY, Zhao H, Liu YS, et al. Relationship between Maternal central obesity and the risk of gestational diabetes mellitus: a systematic review and meta-analysis of cohort studies. J Diabetes Res. 2020;2020:e6303820.
Cnattingius S, Villamor E, Lagerros YT, Wikström AK, Granath F. High birth weight and obesity—a vicious circle across generations. Int J Obes. 2012;36:1320–4.
Leni Z, Künzi L, Geiser M. Air pollution causing oxidative stress. Curr Opin Toxicol. 2020;20:1–8.
Isong IA, Rao SR, Bind MA, Avendaño M, Kawachi I, Richmond TK. Racial and ethnic disparities in early childhood obesity. Pediatrics. American Academy of Pediatrics; 2018 Jan [cited 2020 Nov 23]. 141. Available from: http://pediatrics.aappublications.org/content/141/1/e20170865.
Ogden CL, Fryar CD, Martin CB, Freedman DS, Carroll MD, Gu Q, et al. Trends in obesity prevalence by race and hispanic origin—1999-2000 to 2017-2018. JAMA. 2020;324:1208–10.
Baker JL, Michaelsen KF, Rasmussen KM, Sørensen TIA. Maternal prepregnant body mass index, duration of breastfeeding, and timing of complementary food introduction are associated with infant weight gain. Am J Clin Nutr. 2004;80:1579–88.
Valvi D, Mendez MA, Garcia-Esteban R, Ballester F, Ibarluzea J, Goñi F, et al. Prenatal exposure to persistent organic pollutants and rapid weight gain and overweight in infancy. Obesity. 2014;22:488–96.
Mendez MA, Garcia -Esteban R, Guxens M, Vrijheid M, Kogevinas M, Goñi F, et al. Prenatal organochlorine compound exposure, rapid weight gain, and overweight in infancy. environmental health perspectives. Environ Health Perspect. 2011;119:272–8.
Halfon N, Forrest CB, Lerner RM, Faustman EM, editors. Handbook of Life Course Health Development. Cham (CH): Springer; 2018 [cited 2022 Feb 23]. Available from: http://www.ncbi.nlm.nih.gov/books/NBK543707/.
Messito MJ, Mendelsohn AL, Katzow MW, Scott MA, Vandyousefi S, Gross RS. Prenatal and pediatric primary care-based child obesity prevention program: a randomized trial. Pediatrics. 2020;146:e20200709.
White O, Roeder N, Blum K, Eiden RD, Thanos PK. Prenatal effects of nicotine on obesity risks: a narrative review. Int J Environ Res Public Health. 2022;19:9477.
Pesch MH, Pont CM, Lumeng JC, McCaffery H, Tan CC. Mother and infant predictors of rapid infant weight gain. Clin Pediatr (Phila). 2019;58:1515–21.
Rotevatn TA, Melendez-Torres GJ, Overgaard C, Peven K, Hyldgaard Nilsen J, Bøggild H, et al. Understanding rapid infant weight gain prevention: a systematic review of quantitative and qualitative evidence. Eur J Public Health. 2020;30:703–12.
Acknowledgements
We thank all of the NYU CHES participants and staff for their important contributions. This work was supported by the institutional funds of NYU Grossman School of Medicine as well as the NIH Office of the Director (UG3/UH3OD023305). CD-L acknowledges support from training grants by the National Center for Advancing Translational Sciences, National Institutes of Health 2KL2TR001446-06 and the Life Course Intervention Research Network (Health Resources and Services Administration) UA6MC32492.
Author information
Authors and Affiliations
Contributions
CD-L conceptualized and designed the study, analyzed data, reviewed the analyses, drafted the initial manuscript, and reviewed and revised the manuscript. LT and AG conceptualized and designed the study, supervised acquisition of data, reviewed the analyses, and reviewed and revised the manuscript. KK contributed substantially to the design of the study, supervised acquisition of the data, reviewed the analyses, and reviewed and revised the manuscript. RSG, RO, and AG substantially contributed to interpretation of data, and reviewed and revised the manuscript for important intellectual content. YA, ML, and LS contributed substantially to data collection and reviewed and revised the manuscript. All authors approved the final manuscript as submitted and agree to be accountable for all aspects of the work.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Additional information
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Duh-Leong, C., Ghassabian, A., Kannan, K. et al. Prenatal oxidative stress and rapid infant weight gain. Int J Obes 47, 583–589 (2023). https://doi.org/10.1038/s41366-023-01302-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/s41366-023-01302-8