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Maternal exposure to polycyclic aromatic hydrocarbons during pregnancy and timing of pubertal onset in a longitudinal mother–child cohort in rural Bangladesh

Malin Igra, Annachiara ; Trask, Mercedes ; Rahman, Syed Moshfiqur ; Dreij, Kristian ; Lindh, Christian LU orcid ; Krais, Annette M. LU orcid ; Persson, Lars Åke ; Rahman, Anisur and Kippler, Maria (2024) In Environment International 189.
Abstract

Background: In experimental studies, several polycyclic aromatic hydrocarbons (PAHs) have shown endocrine disrupting properties, but very few epidemiological studies have examined their impact on pubertal development and results have been heterogenous. Objective: To explore if maternal PAH exposure during pregnancy was associated with the offspring's timing of pubertal onset. Methods: We studied 582 mother-daughter dyads originating from a population-based cohort in a rural setting in Bangladesh. Maternal urinary samples, collected in early pregnancy (on average, gestational week 8), were analyzed for monohydroxylated metabolites of phenanthrene (1-OH-Phe, Σ2-,3-OH-Phe, and 4-OH-Phe), fluorene (Σ2-,3-OH-Flu), and pyrene (1-OH-Pyr) using... (More)

Background: In experimental studies, several polycyclic aromatic hydrocarbons (PAHs) have shown endocrine disrupting properties, but very few epidemiological studies have examined their impact on pubertal development and results have been heterogenous. Objective: To explore if maternal PAH exposure during pregnancy was associated with the offspring's timing of pubertal onset. Methods: We studied 582 mother-daughter dyads originating from a population-based cohort in a rural setting in Bangladesh. Maternal urinary samples, collected in early pregnancy (on average, gestational week 8), were analyzed for monohydroxylated metabolites of phenanthrene (1-OH-Phe, Σ2-,3-OH-Phe, and 4-OH-Phe), fluorene (Σ2-,3-OH-Flu), and pyrene (1-OH-Pyr) using liquid chromatography with tandem mass spectrometry (LC-MS/MS). The girls were interviewed on two separate occasions concerning date of menarche, as well as breast and pubic hair development according to Tanner. Associations were assessed using Kaplan-Meier analysis and multivariable-adjusted Cox proportional hazards regression or ordered logistic regression. Results: In early pregnancy, the mothers’ median urinary concentrations of Σ1-,2-,3-,4-OH-Phe, Σ2-,3-OH-Flu, and 1-OH-Pyr were 3.25 ng/mL, 2.0 ng/mL, and 2.3 ng/mL respectively. At the second follow-up, 78 % of the girls had reached menarche, and the median age of menarche was 12.7 ± 0.81 years. Girls whose mothers belonged to the second and third quintiles of ΣOH-Phe metabolites had a higher rate of menarche, indicating a younger menarcheal age (HR 1.39; 95 % CI 1.04, 1.86, and HR 1.41; 95 % CI 1.05, 1.88, respectively), than girls of mothers in the lowest quintile. This trend was not observed in relation to either breast or pubic hair development. None of the other maternal urinary PAH metabolites or the sum of all thereof in early pregnancy were associated with age at menarche or pubertal stage. Conclusions: Indications of non-monotonic associations of prenatal phenanthrene exposure with the daughters’ age of menarche were found, warranting further investigation.

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organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
Fluorene, Menarche, Phenanthrene, Polycyclic aromatic hydrocarbons, Prenatal exposure, Pyrene
in
Environment International
volume
189
article number
108798
publisher
Elsevier
external identifiers
  • scopus:85195814683
  • pmid:38875814
ISSN
0160-4120
DOI
10.1016/j.envint.2024.108798
language
English
LU publication?
yes
id
1b210c06-d90e-4bf7-b8ed-0f7e5d3b7f31
date added to LUP
2024-10-31 10:00:57
date last changed
2025-07-11 08:47:40
@article{1b210c06-d90e-4bf7-b8ed-0f7e5d3b7f31,
  abstract     = {{<p>Background: In experimental studies, several polycyclic aromatic hydrocarbons (PAHs) have shown endocrine disrupting properties, but very few epidemiological studies have examined their impact on pubertal development and results have been heterogenous. Objective: To explore if maternal PAH exposure during pregnancy was associated with the offspring's timing of pubertal onset. Methods: We studied 582 mother-daughter dyads originating from a population-based cohort in a rural setting in Bangladesh. Maternal urinary samples, collected in early pregnancy (on average, gestational week 8), were analyzed for monohydroxylated metabolites of phenanthrene (1-OH-Phe, Σ2-,3-OH-Phe, and 4-OH-Phe), fluorene (Σ2-,3-OH-Flu), and pyrene (1-OH-Pyr) using liquid chromatography with tandem mass spectrometry (LC-MS/MS). The girls were interviewed on two separate occasions concerning date of menarche, as well as breast and pubic hair development according to Tanner. Associations were assessed using Kaplan-Meier analysis and multivariable-adjusted Cox proportional hazards regression or ordered logistic regression. Results: In early pregnancy, the mothers’ median urinary concentrations of Σ1-,2-,3-,4-OH-Phe, Σ2-,3-OH-Flu, and 1-OH-Pyr were 3.25 ng/mL, 2.0 ng/mL, and 2.3 ng/mL respectively. At the second follow-up, 78 % of the girls had reached menarche, and the median age of menarche was 12.7 ± 0.81 years. Girls whose mothers belonged to the second and third quintiles of ΣOH-Phe metabolites had a higher rate of menarche, indicating a younger menarcheal age (HR 1.39; 95 % CI 1.04, 1.86, and HR 1.41; 95 % CI 1.05, 1.88, respectively), than girls of mothers in the lowest quintile. This trend was not observed in relation to either breast or pubic hair development. None of the other maternal urinary PAH metabolites or the sum of all thereof in early pregnancy were associated with age at menarche or pubertal stage. Conclusions: Indications of non-monotonic associations of prenatal phenanthrene exposure with the daughters’ age of menarche were found, warranting further investigation.</p>}},
  author       = {{Malin Igra, Annachiara and Trask, Mercedes and Rahman, Syed Moshfiqur and Dreij, Kristian and Lindh, Christian and Krais, Annette M. and Persson, Lars Åke and Rahman, Anisur and Kippler, Maria}},
  issn         = {{0160-4120}},
  keywords     = {{Fluorene; Menarche; Phenanthrene; Polycyclic aromatic hydrocarbons; Prenatal exposure; Pyrene}},
  language     = {{eng}},
  publisher    = {{Elsevier}},
  series       = {{Environment International}},
  title        = {{Maternal exposure to polycyclic aromatic hydrocarbons during pregnancy and timing of pubertal onset in a longitudinal mother–child cohort in rural Bangladesh}},
  url          = {{http://dx.doi.org/10.1016/j.envint.2024.108798}},
  doi          = {{10.1016/j.envint.2024.108798}},
  volume       = {{189}},
  year         = {{2024}},
}