Abstract
Persistent organic pollutants (POPs) are compounds that are recalcitrant and ubiquitous that bioaccumulate in human milk (HM) and can impact infant growth and development. We explore the association between POP concentration in HM at 2–50 days postpartum and infant growth and development trajectory throughout the first year of life. A cohort of 68 healthy adult Brazilian women and their infants were followed from 28 to 35 gestational weeks to 12 months postpartum. HM samples were collected between 2 and 50 days postpartum, and POP concentrations were analyzed using gas chromatography with mass spectrometry. Concentrations of POPs >limit of quantification (LOQ) were defined as presence, and concentrations ≤LOQ as an absence. Growth z-scores were analyzed according to WHO growth charts and infant development scores according to Age & Stages Questionnaires at 1 (n = 66), 6 (n = 50), and 12 months (n = 45). Linear mixed effects (LME) models were used to investigate the association of POPs in HM with infant growth and development. Benjamini-Hochberg (BH) correction for multiple testing was performed to reduce the false discovery ratio. P < 0.1 was considered for models with the interaction between POPs and time/sex. After BH correction, adjusted LME models with time interaction showed (1) a positive association between the presence of β hexachlorocyclohexane and an increase in head circumference-for-age z-score (β = 0.003, P = 0.095); (2) negative associations between total POPs (β = −0.000002, P = 0.10), total organochlorine pesticides (β = −0.000002, P = 0.10), and dichlorodiphenyldichloroethylene concentrations in HM (β = −0.000002, P = 0.10) and fine motor scores. No statistical difference between the sexes was observed. Postnatal exposure to organochlorine pesticides in HM shows a positive association with the trajectory of head circumference-for-age z-score and a negative association with the trajectories of fine motor skills scores. Future studies on POP variation in HM at different postpartum times and their effect on infant growth and development should be encouraged.
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Data availability
All datasets used and/or, codebook, and analytic code generated during the current study are available from the corresponding author upon reasonable request pending application and approval.
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Acknowledgements
We gratefully acknowledge all cohort women and infants from the Public Health Center, where the data were collected. We also thank the support of the Carlos Chagas Filho Foundation for Research Support of Rio de Janeiro State-FAPERJ and the National Council for Scientific and Technological Development-CNPq.
Funding
This work was partly supported by the Carlos Chagas Filho Foundation for Research Support of Rio de Janeiro State-FAPERJ [grant nos. E-26/210.190/2014 (200585), E-26/010.002429/2019 (211560), and E-26/200.429/2020] and by the National Council for Scientific and Technological Development-CNPq (grant no. 409676/2016).
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Ana Lorena Ferreira and Gilberto Kac: study conception and design; Ana Lorena Ferreira, Nathalia Freitas-Costa, Amanda Figueredo, and Nadya Alves-Santos: conducted the research data collection; Ana Lorena Ferreira: analyzed the data and performed the statistical analysis and written the first draft of the manuscript; Gilberto Kac: supervision and funding acquisition to research. Ana Lorena Ferreira, Nathalia Freitas-Costa, Samary Freire, Amanda Figueredo, Marina Padilha, Nadya Alves-Santos, and Gilberto Kac contributed to the review and editing, provided a critical evaluation, and approved the final manuscript.
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Supplementary Information
ESM 1
Supplementary Fig. 1 Study theoretical model with a directed acyclic graph for minimal adjustment to the association between POPs in human milk and infant growth. Breastfeeding status indicates exclusively dichotomous yes/no. Note: POPs, persistent organic pollutants; PP-BMI, pre-pregnancy body mass index; GWG, total gestational weight gain; HM, human milk. Minimal adjustment: birth weight, breastfeeding status, total gestational weight gain, gestational age birth, maternal serum leptin, maternal education, PP- BMI. (TIF 888 kb)
ESM 2
Supplementary Fig. 2 Study theoretical model with a directed acyclic graph for minimal adjustment to the association between POPs in human milk and infant development. Breastfeeding status indicates exclusively dichotomous yes/no. Note: POPs, persistent organic pollutants; PP-BMI, pre-pregnancy body mass index; GWG, total gestational weight gain; HM, human milk. Minimal adjustment: birth weight, congenital anomalies, GWG, gestational age birth, gestational energy intake (kcal), maternal education, maternal age, PP-BMI, parity, smoking during pregnancy. (TIF 1080 kb)
ESM 3
Supplementary Fig. 3 Longitudinal linear mixed-effect models for z-scores growth trajectory throughout one (n=66), six (n=50), and 12 months (n=45) of infants’ life. Note: The space between oranges' dashed lines represents the normal range according to the World Health Organization growth chart (2006; 2007). The model coefficients, standard error (SE), and p-value for each z-score are as follows: weight for age: β= 0.001, SE= 0.0003, P=0.012 (A); length for age: β= 0.0001, SE= 0.0003, P=0.844 (B); BMI for age: β= 0.001, SE= 0.0004, P=0.002 (C); weight for length: β= 0.001, SE= 0.0004, P=0.047 (D); head circumference for age: β= 0.0002, SE= 0.0003, P=0.590 (E). (TIFF 10295 kb)
ESM 4
Supplementary Fig. 4 Longitudinal linear mixed-effect models for infant development scores throughout one (n=66), six (n=50), and 12 months (n=45) of infants’ life. Note: Score domains according to Age & Stages Questionnaires (Squires et al. 2009). The model coefficients, standard error (SE), and P for each z-score are as follows: (A) communication: β= 0.043, SE= 0.006, P<0.001; (B) gross motor skills: β= 0.050, SE= 0.006, P<0.001; (C) fine motor skills: β= 0.023, SE= 0.005, P<0.001; (D) personal-social: β= -0.0046, SE= 0.006, P=0.444; (E) problem solving: β= 0.004, SE= 0.0008, P<0.001. (TIFF 10295 kb)
ESM 5
Supplementary Fig. 5 Longitudinal linear mixed-effect models for infant growth z-scores throughout one, six, and 12 months of infants’ life in interaction with sex. Note: Boys: one (n=32), six (n=24), and 12 months (n=21). Girls: one (n=36), six (n=26), and 12 months (n=24). The model coefficients, standard error (SE), and p-value for each z-score are as follows: (A) weight-for-age (β =-0.00003, SE= 0.001, P=0.965), (B) height/length-for-age (β =0.0002, SE= 0.001, P=0.732), (C) BMI-for-age (β =-0.0004, SE= 0.0008, P=0.587), (D) head circumference-for-age (β =0.0009, SE= 0.0006, P=0.154), (E) weight-for-length (β =-0.001, SE= 0.001, P=0.274). (TIFF 774 kb)
ESM 6
Supplementary Fig. 6 Longitudinal linear mixed-effect models for infant development scores throughout one, six, and 12 months of infants’ life in interaction with sex. Note: Score domains according to Age & Stages Questionnaires (Squires et al. 2009). Boys: one (n=32), six (n=24), and 12 months (n=21). Girls: one (n=36), six (n=26), and 12 months (n=24). The model coefficients, standard error (SE), and p-value for each score are as follows: (A) communication (β =-0.00003, SE= 0.012, P= 0.980), (B) gross motor skills (β =-0.002, SE= 0.013, P= 0.878), (C) fine motor skills (β =0.004, SE= 0.010, P= 0.669), (D) problem-solving (β =-0.014, SE= 0.015, P= 0.346), and (E) personal-social (β =0.028, SE= 0.011, P=0.016). (TIFF 706 kb)
ESM 7
Supplementary Fig. 7 Longitudinal linear mixed-effect models for Personal-social infant development domain throughout the first year of infants’ life for (A) boys and (B) girls. Note: Score domains according to Age & Stages Questionnaires (Squires et al. 2009). Boys: one (n=32), six (n=24), and 12 months (n=21). Girls: one (n=36), six (n=26), and 12 months (n=24). The model coefficients, standard error (SE), and p-value: (A) Boys: β=0.0006, SE= 0.0003, P= 0.595; (B) Girls: β=0.0004, SE=0.0002, P= 0.786. (TIFF 17158 kb)
ESM 8
Supplementary Table 1. Linear mixed models between POPs and weight-for-age (WAZ), length-for-age (HAZ), BMI-for-age (BAZ), weight for length (WHAZ) and head circumference-for-age z-scores in the first year of infant life in unadjusted models, with the interaction between POPs concentration and days postpartum (*days) and with interaction adjusted (*days adj.). Supplementary Table 2. Linear mixed models between POPs and communication, gross motor skills, fine motor skills, problem solving and personal-social scores in the first year of infant life in unadjusted models, with the interaction between POPs concentration and days postpartum (*days) and with interaction adjusted (*days adj.).(XLSX 45 kb)
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Ferreira, .L.L., Freitas-Costa, N., da Silva Rosa Freire, S. et al. Association between persistent organic pollutants in human milk and the infant growth and development throughout the first year postpartum in a cohort from Rio de Janeiro, Brazil. Environ Sci Pollut Res 30, 115050–115063 (2023). https://doi.org/10.1007/s11356-023-30316-y
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DOI: https://doi.org/10.1007/s11356-023-30316-y