1Department of Pediatrics, Ewha Womans University College of Medicine, Seoul, Korea
2Department of Environmental Medicine, Ewha Womans University College of Medicine, Seoul, Korea
3Institute of Ewha-SCL for Environmental Health (IESEH), Ewha Womans University College of Medicine, Seoul, Korea
4Department of Human Systems Medicine, College of Medicine, Seoul National University, Seoul, Korea
5System Health & Engineering Major in Graduate School (BK21 Plus Program), Ewha Womans University, Seoul, Korea
*Corresponding author: Hae Soon Kim,
Department of Pediatrics, Ewha Womans University College of Medicine, 260,
Gonghang-daero, Gangseo-gu, Seoul, 07804, Korea, E-mail:
hyesk@ewha.ac.kr
*Corresponding author: Eunhee Ha,
Department of Environmental Medicine, Ewha Womans University College of
Medicine, 25, Magokdong-ro 2-gil, Gangseo-gu, Seoul 07804, Korea, E-mail:
eunheeha@ewha.ac.kr
• Received: February 28, 2024 • Revised: April 21, 2024 • Accepted: April 22, 2024
This is an Open-Access article distributed under the terms of the
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The worldwide incidence of precocious puberty, which is associated with negative
health outcomes, is increasing. Several studies have suggested that
environmental factors contribute to the development of precocious puberty
alongside genetic factors. Some epidemiological studies have provided limited
evidence suggesting an association between exposure to air pollution and changes
in pubertal development. This systematic review aimed to summarize existing
evidence on the association between air pollution exposure and precocious
puberty. Following the Preferred Reporting Items for Systematic reviews and
Meta-Analyses guidelines, we searched two databases (PubMed and Web of Science)
until August 2023. The included studies assessed the association between air
pollutant exposure and the risk of precocious puberty, early menarche, or
pubertal development. Two authors independently performed study selection and
data extraction. A meta-analysis and analysis of the risk of bias were
infeasible due to the limited number of studies and the heterogeneity among
them. The literature search resulted in 184 studies, from which we included six
studies with sample sizes ranging from 437 to 4,074 participants. The studies
reported heterogeneous outcomes. Four studies found that increased exposure to
air pollution was related to earlier pubertal onset. One study was inconclusive,
and another suggested that air pollutant exposure may delay the onset of
thelarche. Most studies suggest that exposure to air pollutants accelerates
pubertal development; however, the results from the available studies are
inconsistent. More extensive and well-designed longitudinal studies are required
for a comprehensive understanding of the association between air pollution and
precocious puberty.
The increasing incidence of precocious puberty is emerging as a significant
medical and social issue worldwide [1,2]. A meta-analysis from
2020 reported a trend of breast development beginning approximately 0.24 years
earlier every decade from 1977 to 2023 [3]. Additionally, there has been a notable decrease in the age of
menarche from the 19th to the 20th century [4]. The onset of puberty is determined by both genetic and
environmental factors [5,6]. Recent studies have highlighted that
non-genetic lifestyle factors, such as adiposity, exposure to
endocrine-disrupting chemicals (EDCs), and air pollution, might influence the
timing of pubertal onset [7]. Furthermore,
several epidemiological studies have found that exposure to ambient air
pollution is linked to an earlier onset of menarche in girls [8,9].
Ambient air pollution consists of a mixture of particulate matter (PM) and
gaseous pollutants that originate from both human activities and natural
sources. This pollution primarily includes sulfur dioxide (SO2),
nitrogen dioxide (NO2), carbon monoxide (CO), and ozone
(O3). PM contains various components such as heavy metals,
polycyclic aromatic hydrocarbons, and EDCs, all of which can interfere with the
endocrine system [10,11]. When inhaled, ambient air pollution
can enter the human bloodstream and be transported to various organs [12], leading to a range of health outcomes,
including endocrine disruption [10]. PM
can interact with estrogen receptors, triggering the release of kisspeptin,
which in turn stimulates the secretion of gonadotropin-releasing hormone,
thereby initiating the onset of puberty [13]. Moreover, fine particulate matter (PM2.5), with a
diameter of less than 2.5 μm, as opposed to particulate matter
(PM10), which has a diameter of less than 10 μm, can
penetrate deeper into the body upon inhalation, potentially causing more severe
adverse effects.
Currently, epidemiological studies that investigate the association between
exposure to air pollution and pubertal development are limited, and their
findings are inconsistent. It is important to note that, to date, no systematic
review has been conducted on the relationship between exposure to air pollution
and pubertal development.
Objectives
This systematic review investigated the impact of exposure to ambient air
pollution on pubertal development and the risk of precocious puberty.
Methods
Ethics statement
Since this research did not involve any direct human participants or
human-derived materials, it did not require approval from an institutional
review board or the obtainment of informed consent.
Study design
We conducted a systematic review following the Preferred Reporting Items for
Systematic Reviews and Meta-Analyses (PRISMA) 2020 guidelines (Fig. 1). The study protocol was registered
with PROSPERO on September 19, 2023 (CRD42023465050). Revisions to the protocol
were necessary as assessing the risk of bias and conducting a meta-analysis
proved infeasible due to the heterogeneity among the included studies.
Fig. 1.
Flow diagram summarizing the process of literature search and
selection. WoS, Web of Science.
Eligibility criteria
To investigate our systematic review, we defined the population, exposures,
comparison, outcomes, and study designs (PECOS) parameters. The details of PECOS
are as follows: a) population: infants, children, adolescents, or pediatric
patients; b) exposure: air pollutants, such as PM2.5,
PM10, SO2, NO, NO2, or O3; c)
comparison: exposure to lower or higher levels of each specific type of air
pollutants in the same population or in a control population; with provision of
a measure of risk (e.g., relative risk [RR], OR, hazard ratio [HR], or mean
difference [MD]); d) outcome: precocious puberty risk, early menarche risk, or
pubertal development stage; and e) study design: human epidemiological studies,
including prospective and retrospective cohort studies, case-control, and
cross-sectional studies. We excluded abstracts, case reports, editorials, animal
studies, in vivo studies, and commentaries.
Information sources
We performed a systematic search of the 1) PubMed and 2) Web of Science (WoS)
databases from their inception to August 23, 2023. Only articles in English were
included.
Search strategy
The search terms for the search strategy can be found in Supplement 1. Duplicate
articles were eliminated using EndNote and the manual method.
Selection process
Two authors (RSL and EJM) independently reviewed the titles and abstracts and
selected potentially eligible articles. Subsequently, the full texts of selected
studies were examined by two authors (RSL and EJM) with the participation of
other authors (JMO, KHK, JHL, HSK, and EHH) to address any disagreements and
reach a consensus.
Data collection process
Two authors (RSL and JMO) extracted the following data of interest in a Microsoft
Excel sheet: first author, year of publication, country, study design, follow-up
period, sample size, population characteristics, exposure details, details on
outcome assessment, and confounders. Furthermore, we also extracted measures of
effect (i.e., RR, OR, HR, MD, and time ratio [TR]) for the association between
air pollution and precocious puberty.
Data synthesis
In our initial protocol for the systematic review, we planned to conduct a
meta-analysis if at least three studies shared similar study designs, analysis
methods, and effect sizes. However, a meta-analysis proved infeasible due to the
limited number of studies (<3) and the diverse range of study designs,
including case-crossover, cohort, and cross-sectional studies. Additionally, the
outcomes varied among the studies, encompassing the risk of precocious puberty,
the risk of early menarche, and stages of pubertal development. Given the
heterogeneity among the included studies, we created a table to outline the
characteristics of the studies and the relationships between the exposures and
outcomes. As a result, we were unable to perform a meta-analysis and instead
provided a descriptive summary.
Results
Study selection
In our systematic search, we identified 184 studies out of the initial 212
(PubMed: 122 and WoS: 90), following the removal of duplicates. Of these, 10
full-text studies were assessed for eligibility, with 6 ultimately being
included [8,9,14–17]. Fig.
1 illustrates the flow diagram of the study selection process. The
studies that were excluded, along with the reasons for their exclusion, are
detailed in Supplement 2.
Characteristics of the included studies
Table 1 summarizes the characteristics of
the six studies. Three studies were designed as cohorts [8,16,17], two were conducted as cross-sectional
studies [9,15], and one was a case-crossover study [14]. These studies were conducted in China, Hong Kong, the
USA, South Korea, Poland, and Germany. The sample sizes ranged from 437 to 4,074
participants, with follow-up durations spanning from 3 to 14 years. Five studies
investigated exposure to ambient air pollutants such as PM2.5,
PM10, SO2, NO, NO2, and O3
[8,9,14–16], whereas one study analyzed
traffic-related metrics [17]. Yang et al.
measured air pollutant levels using inverse distance weighting; Wronka et al.
assessed air quality based on data from the chief inspectorate for environmental
protection; Zhao et al. utilized a land-use regression model; Jung et al. relied
on air monitoring network stations; Huang et al. gathered data from a monitoring
station; and McGuinn et al. used annualized traffic data from the California
Department of Transportation Highway Performance Monitoring System. The outcomes
of these studies varied. Two studies [8,9] focused on the risk of
early menarche as their primary outcome, with the age at menarche being
self-reported. One study [14] examined
the incidence of precocious puberty, defined by a professional pediatrician as
the activation of the hypothalamic-pituitary-gonadal axis function and the onset
of secondary sexual characteristics before the age of 8 in girls and 9 in boys.
The remaining studies [15–17] assessed pubertal development at a
specific age using Tanner staging or measured sex hormone levels.
Table 1.
Characteristics of studies assessing the association between air
pollutant exposure and pubertal development
†The authors assessed children born between 1995 and 1999 when they
reached the age of 10, between 2005 and 2009.
‡The authors assessed children born in 1997 when they reached the age
of 9–12, between 2005 and 2008.
Synthesis of results
Relationship between air pollution exposure and pubertal
development
Table 2 summarizes the findings on the
impact of air pollution on pubertal development, precocious puberty, and age
at menarche across various studies. Four out of six studies [8,9,14,17] indicated that exposure to air
pollution accelerates pubertal development stages and promotes precocious
puberty. Jung et al. found that a 1 μg/m3 increase in
PM10 was associated with a higher risk of early menarche
(OR=1.08; 95% CI, 1.04–1.12) and accelerated age at menarche by 0.046
years (95% CI, −0.064 to −0.027) on a 1-year average. The
authors reported that the results were consistent across the 2-year average
(OR=1.06; 95% CI, 1.02–1.10; 0.038 years; 95% CI, −0.059 to
−0.018) and 3-year model average (OR=1.05; 95% CI, 1.01–1.09;
0.031 years; 95% CI, −0.047 to −0.015). Wronka et al. found
that the risk of early menarche (age below 11) was higher in the group
living in areas with high PM levels. The ORs were calculated as 3.18 (95%
CI, 2.29–4.69) for PM10 and 3.25 (95% CI, 2.34–4.8)
for PM2.5. Yang et al. used a distributed lag nonlinear model to
determine the OR of the lag effect of PM2.5 and PM10
on the incidence of precocious puberty. They reported that the most
significant effects of PM2.5 and PM10 on precocious
puberty were observed in lag 27 (OR=1.72; 95% CI, 1.01–2.92) and lag
16 (OR=1.95; 95% CI, 1.33–2.85), respectively. McGuinn et al. found
that girls living within 150 m of a major road or highway had a higher
likelihood of experiencing early pubarche (TR=0.96; 95% CI,
0.93–0.99), but not thelarche (TR=0.99; 95% CI, 0.97–1.02).
The authors used accelerated failure time models, and calculated TRs, where
a TR of <1.0 indicated an earlier age at pubertal development than
the reference group. In contrast, Huang et al. reported that exposure to
PM10 during the prenatal and infantile periods could delay
thelarche. Exposure to PM10, SO2, NO, and
NO2 was considered as z-scores for comparability, and the
outcomes were the MD in Tanner stage per SD increment in each type of air
pollutant. In girls, higher PM10 exposure in
utero (MD: −0.05; 95% CI, −0.08 to −0.02)
and in infancy (MD: −0.03; 95% CI, −0.06 to −1.2) was
associated with a lower pubertal stage. In boys, higher SO2
exposure in utero (MD: −0.03; 95% CI, −0.05,
−0.01) and during childhood (MD: −0.06; 95% CI, −0.08,
−0.04) were associated with lower pubertal stage. Furthermore, higher
NO2 exposure in utero (MD: −0.03; 95%
CI, −0.04, −0.02) and during childhood (MD: −0.02; 95%
CI, −0.04, −0.01) was associated with a lower pubertal stage.
Zhao et al. found no statistically significant associations between air
pollution exposure and pubertal development as assessed using serum sex
hormone levels.
Table 2.
Relationship between air pollutant exposure and pubertal
development
Age, sex, body mass
index, secondhand smoke exposure, time spent outside and in
front of a screen, physical activity level, season, and time
of the blood sampling, household income, parental education,
maternal age at birth, single parent status
Pubertal stage at
age 11 years assessed with Tanner stage
Mean difference in
Tanner stage
Female In
utero: −0.05 (−0.08 to
−0.02)† Infancy:
−0.03 (−0.06 to −1.2)†
Neighborhood and
household income per person, mother's migration
status, highest parental educational level, age, maternal
age at birth, parity, maternal smoking
NA
SO2
Male In
utero: −0.03 (−0.05 to
−0.01)† Childhood:
−0.06 (−0.08 to −0.04)†
NO
Statistically insignificant
NO2
Male In
utero: −0.03 (−0.04 to
−0.02)† Childhood:
−0.02 (−0.04 to −0.01)†
PM, particulate matter; SO2, sulfur dioxide;
NO2; nitrogen dioxide; CO, carbon monoxide;
O3, ozone; TR, time ratio; NA, not
applicable.
*Low: annual pollutant values and the number of days per year with
exceedances were below the allowable limit; Medium: annual
values below the permissible limit, but with the number of days
exceeding the normal above the limit; High: included zones above
the limit.
†Statistically significant results.
Discussion
Key results
In this systematic review, we found that four out of six studies indicated a
relationship between increased exposure to air pollution and earlier onset of
puberty [8,9,14,17]. One study produced inconclusive results [15], while another suggested that exposure
to air pollutants might delay the onset of thelarche [16].
There has been no prior systematic review examining the effects of air pollution
exposure on pubertal development and precocious puberty. The studies we included
employed various research designs, such as cohort, cross-sectional, and
case-crossover studies, featured different sample sizes, and tracked
participants over varying lengths of time. These studies also investigated
different exposures and outcomes and utilized a range of methods to measure
exposure. We recognize that this diversity in study design could account for the
inconsistent results regarding the impact of air pollution on precocious
puberty. Nevertheless, the authors are inclined to believe that air pollution
adversely affects precocious puberty, based on the accumulating evidence that
air pollutants influence pubertal development through various mechanisms, which
are not yet fully understood.
Interpretation and comparison with previous studies
When chemicals and heavy metals with endocrine-disrupting properties are released
into the air from industrial emissions, vehicle emissions, and waste combustion,
they can bind to PM [18]. Polycyclic
aromatic hydrocarbons and heavy metals in PM, particularly from fossil fuel
combustion, are recognized as endocrine disruptors due to their ability to
activate aryl hydrocarbon, androgen, or estrogen receptors [19]. PM can act on estrogen receptors,
triggering the release of kisspeptin, which subsequently initiates the secretion
of gonadotropin-releasing hormone, thus starting the onset of puberty [13]. Epigenetic disruption caused by PM is
a potential mechanism for triggering puberty through neuroendocrine components
[20]. Moreover, PM can induce
oxidative stress and systemic inflammation upon entering the respiratory tract
[21]. Endocrine disruptors attached
to PM influence hormone synthesis in endocrine glands or disrupt hormone
transport to target organs. Research using mixtures of EDCs found in indoor air
samples has shown that these compounds exhibit estrogenic and androgenic
activities when tested in in vitro assay systems [22]. There is increasing evidence that
certain EDCs are associated with various human health issues, such as
reproductive problems in both females and males, and precocious puberty in
children, as indicated in several previously reported systematic reviews [23–28].
Although the exact mechanisms connecting air pollutants and puberty onset remain
unclear, the presence of EDCs in air, including PM, and their potential impact
on puberty are areas that require active research.
Strengths and limitations of the included studies
These studies stand out for their pioneering research into the relationship
between exposure to air pollutants and pubertal development. McGuinn et al.
[17] conducted the first study to
explore the link between early life proximity to traffic and pubertal
development within a multiethnic cohort. Huang et al. utilized a
population-representative birth cohort and gathered clinical data on pubertal
stages. Jung et al. [9] analyzed data from
the fifth Korea National Health and Nutrition Examination Study, a
representative sample of the South Korean population, and found consistent
results across various models after making adjustments. Wronka et al. [8] carried out the inaugural study in a
European country investigating the connection between air pollutant exposure and
early menarche. Zhao et al. [15] also
drew on data from two relatively large birth cohorts, with numerous relevant
covariates available for adjustment. Yang et al. [14] employed a case-crossover study design and a
distributed nonlinear model to evaluate the association between PM10
and PM2.5 levels and the risk of precocious puberty. Zhao et al.
[15] and Jung et al. [9] considered body mass index as a
confounding factor, acknowledging that nongenetic lifestyle factors such as
adiposity can influence the onset of puberty.
Nonetheless, the included studies have several limitations. First, exposure to
air pollutants was estimated using data averaged for specific geographic areas,
and the limited number of air quality monitoring stations may not provide a
precise representation of individual exposure. Consequently, exposure
misclassification and a lack of individual-level data are possible issues.
Second, some studies were susceptible to recall bias, particularly those relying
on self-reported data such as age at menarche. Additionally, most studies
focused on single pollutant exposure, whereas in reality, humans are exposed to
a complex mixture of air pollutants [29].
Moreover, the study designs varied, encompassing different exposures to air
pollutants, and the outcomes included the incidence of precocious puberty, age
at menarche, and pubertal stage at a specific age. This heterogeneity in study
design and outcomes made it infeasible to conduct a meta-analysis and evaluate
the risk of bias.
Recommendations for future studies and health implications
Future researchers should consider conducting prospective birth cohort studies to
assess the long-term consequences of prenatal and postnatal exposure to air
pollution. This is crucial because EDCs can function as obesogens during
pregnancy, potentially altering fetal programming [30], and air pollution may have similar effects.
Furthermore, to accurately assess individual exposure to air pollution, it is
feasible to use advanced technologies and methods, such as personal monitoring
devices. Expanding the study population to include diverse socioeconomic groups
and geographical locations can enhance the generalizability of the findings.
In vitro research is also necessary to understand the
biological mechanisms underlying the association between air pollution and
pubertal development. Additionally, research should focus on developing
prevention policies and interventions aimed at mitigating the impact of air
pollution. Air pollution is a global concern, and international collaboration
among researchers and institutions worldwide can lead to a more comprehensive
understanding of its effects on health.
Strengths and limitations of this review
To the best of our knowledge, this is the first systematic review to provide
evidence of the impact of air pollution exposure on precocious puberty and
pubertal development. Additionally, all review processes underwent peer review,
adhering to the PRISMA guidelines. However, due to the heterogeneity among the
studies, it was not feasible to conduct a meta-analysis to evaluate the combined
effect of air pollution on the risk of precocious puberty. Future research on
this topic is necessary, and as more studies become available, we aim to gather
sufficient evidence to conduct a meta-analysis.
Conclusion
The evidence suggests that exposure to air pollution may lead to an earlier onset
of puberty, although the results of studies have been inconsistent. To address
this, further longitudinal studies are needed that accurately assess individual
exposure to multiple air pollutants over extended periods. It is crucial to
promote policies aimed at reducing exposure to air pollution. Additionally,
sharing international data and conducting collaborative studies could provide
valuable insights for developing preventive policies concerning exposure to air
pollutants.
Authors' contributions
Project administration: Kim HS, Ha E
Conceptualization: Lee R, Oh J, Mun E, Choi JE, Kim KH, Lee JH, Kim HS, Ha E
Methodology & data curation: Kim HS, Ha E
Funding acquisition: Kim HS, Ha E
Writing – original draft: Lee R
Writing – review & editing: Lee R, Oh J, Mun E, Choi JE, Kim KH,
Lee JH, Kim HS, Ha E
Funding
Eunhee Ha has been a dean of the Ewha Womans University College of Medicine since
August 2021; however, she was not involved in the peer review process or
decision-making. Otherwise, no potential conflict of interest relevant to this
article was reported.
Funding
This study was supported by a project titled “Institute of Ewha-SCL for
Environmental Health (IESEH)’’ and Research of Environmental
Examination Model for Children and Women (No. 1-2022-0205-001-2).
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Environmental factors trigger pubertal development Sofia Malave-Ortiz, Cameron Grant, Natalie D. Shaw Current Opinion in Pediatrics.2025;[Epub] CrossRef
Gender equity in medicine, artificial intelligence, and other
articles in this issue Sun Huh The Ewha Medical Journal.2024;[Epub] CrossRef
Age, sex, body mass
index, secondhand smoke exposure, time spent outside and in
front of a screen, physical activity level, season, and time
of the blood sampling, household income, parental education,
maternal age at birth, single parent status
Pubertal stage at
age 11 years assessed with Tanner stage
Mean difference in
Tanner stage
Female In
utero: −0.05 (−0.08 to
−0.02)† Infancy:
−0.03 (−0.06 to −1.2)†
Neighborhood and
household income per person, mother's migration
status, highest parental educational level, age, maternal
age at birth, parity, maternal smoking
NA
SO2
Male In
utero: −0.03 (−0.05 to
−0.01)† Childhood:
−0.06 (−0.08 to −0.04)†
NO
Statistically insignificant
NO2
Male In
utero: −0.03 (−0.04 to
−0.02)† Childhood:
−0.02 (−0.04 to −0.01)†
PM, particulate matter; SO2, sulfur dioxide;
NO2; nitrogen dioxide; CO, carbon monoxide;
O3, ozone; TR, time ratio; NA, not
applicable.
*Low: annual pollutant values and the number of days per year with
exceedances were below the allowable limit; Medium: annual
values below the permissible limit, but with the number of days
exceeding the normal above the limit; High: included zones above
the limit.
†Statistically significant results.
Table 1.
Characteristics of studies assessing the association between air
pollutant exposure and pubertal development
The authors assessed children born between 1995 and 1999 when they
reached the age of 10, between 2005 and 2009.
The authors assessed children born in 1997 when they reached the age
of 9–12, between 2005 and 2008.
Table 2.
Relationship between air pollutant exposure and pubertal
development
PM, particulate matter; SO2, sulfur dioxide;
NO2; nitrogen dioxide; CO, carbon monoxide;
O3, ozone; TR, time ratio; NA, not
applicable.
Low: annual pollutant values and the number of days per year with
exceedances were below the allowable limit; Medium: annual
values below the permissible limit, but with the number of days
exceeding the normal above the limit; High: included zones above
the limit.
, Jongmin Oh2,3,4
