Association between perfluoroalkyl substance concentrations and blood pressure in adolescents

doi:10.1016/j.envpol.2019.112971

Environmental Pollution

Volume 254, Part A, November 2019, 112971

https://doi.org/10.1016/j.envpol.2019.112971 Get rights and content

Highlights

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2251 adolescents were used to examine associations of polyfluoroalkyl chemicals with blood pressure levels.
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Positive associations were found between blood PFOS and diastolic blood pressure in males.
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Restricted cubic spline models showed no significant associations between PFOS and blood pressure.

Abstract

The effects of exposure to some environmental chemicals on blood pressure have been determined, but the association between non-occupational exposure to perfluoroalkyl substances (PFASs) and blood pressure in adolescents remains unknown. The association between blood pressure and PFAS concentrations was studied by analysing data from 2251 participants filtered from the population enrolled in the National Health and Nutrition Examination Survey (NHANES) from 2003 to 2012. After adjusting for age, sex, race, BMI, cotinine level, dietary intake of calcium, caloric intake, sodium consumption, potassium consumption and sampling year, we estimated the coefficients (betas) and 95% confidence intervals (CIs) for the relationship between PFAS concentrations and blood pressure with multiple linear regression models. Potential non-linear relationships were assessed with restricted cubic spline models. Blood levels of perfluorooctane sulfonic acid (PFOS) had a strong positive association with diastolic blood pressure (DBP) in adolescents in the linear model, while the result was not significant in the non-linear model. No significant association was observed between the concentration of any other PFASs and blood pressure. According to the fully adjusted linear regression model (P = 0.041), the mean DBP values in boys in the higher PFOS quintile were 2.70% greater than the mean DBP values of boys in the lowest PFOS quintile. Furthermore, serum PFOS concentrations predominantly affected blood pressure in male adolescents compared with female adolescents. These results provide epidemiological evidence of PFOS-related increases in DBP. Further research is needed to address related issues.

Graphical abstract

Introduction

Hypertension, or elevated blood pressure, is a global public health problem. According to documents issued by the World Health Organization (WHO), hypertension is defined as a systolic blood pressure (SBP) value ≥ 140 mmHg and/or a diastolic blood pressure (DBP) value ≥ 90 mmHg. The global number of hypertensive patients increased to 1 billion by 2008. In general, the prevalence was higher in males than in females. According to a survey published by the American Medical Association (AMA), the systolic blood pressure of 3.5 billion adults ranges from at least 110–115 mmHg, while 874 million adults have systolic blood pressure values above 140 mmHg (Forouzanfar et al., 2017). In addition, many hypertensive patients remain undiagnosed due to a lack of symptoms in the early stages. Alarmingly, after the American Academy of Pediatrics (AAP) released new practical clinical guidelines in 2017 in which they redefined hypertension as BP ≥ 130/80 mmHg or the reported use of anti-hypertensive medication among adolescents aged 12–19 years, 795 thousand young people were reclassified as hypertensive patients (Jackson et al., 2018). An increase in the prevalence of hypertension among adolescents is expected, with a higher prevalence in males (Rao, 2016). Therefore, determining the risk factors for hypertension is critical, and some new risk factors have been reported in recent years. In addition to the risk factors for adults published by the WHO in 2013, such as ageing, population growth and behaviours, youths who were male, relatively older and obese tended to have high blood pressure (Anyaegbu and Dharnidharka, 2014; Jackson et al., 2018). Additionally, a number of studies revealed that environmental factors are nonnegligible contributors to high blood pressure, especially perfluoroalkyl substances (PFASs) (Li et al., 2013; Lin et al., 2011; Yorifuji et al., 2010).

PFASs are synthetic organic compounds and include perfluorooctanoic acid (PFOA), perfluorooctane sulfonic acid (PFOS), perfluorohexane sulfonic acid (PFHxS), 2-(N-ethyl-perfluorooctane sulfonamido) acetate (EPAH), and 2-(N-methyl-perfluorooctane sulfonamido) acetate (MPAH). PFASs have been widely used in commercial applications and various manufacturing industries, including the manufacture of surfactants, paper, lubricants, textile coatings, and water and oil repellents in cosmetics, clothing, food packaging and furnishings (Lindstrom et al., 2011; Prevedouros et al., 2006). On account of their stable biology, physics and chemistry, PFASs accumulate and can be biomagnified through the trophic chain (Tomy et al., 2004). According to the national biological monitoring survey report, PFOA, PFOS and other perfluorooctanoic acids are emerging as human pollutants, and they are not only commonly detected in surface water, soil, wastewater and indoor environmental sources but also in human blood in vivo. Some studies have reported that PFASs, especially PFOA and PFOS, could harm animals to a certain degree, with effects including neurotoxicity (Salgado et al., 2016), a decrease in the Ser9 phosphorylation of glycogen synthase kinase-3β (Dong et al., 2016), inhibition of the differentiation of neural stem cells (Wan Ibrahim et al., 2013) and development of sex hormone disorders (Chen et al., 2016).

In addition, several studies have demonstrated that PFASs are correlated with hypertension in adults (Bao et al., 2017; Min et al., 2012). A study on young hypertensive patients showed that teenagers diagnosed with hypertension had higher levels of PFASs than those not diagnosed with hypertension, but the study did not further analyse the relationship between PFASs and hypertension (Min et al., 2012). The relationships between hypertension in teenagers and the concentrations of PFASs are still unclear. Therefore, our study focused on the correlations between the concentrations of PFASs and hypertension in adolescents. Interestingly, the results of the study revealed that the concentration of PFOS was positively associated with diastolic blood pressure in adolescent boys.

Section snippets

Subjects

We used publicly available data regarding subjects who were recruited for the National Health and Nutrition Examination Survey (NHANES). The data were from five cycles of the NHANES (2003–2004, 2005–2006, 2007–2008, 2009–2010, and 2011–2012). The NHANES website [https://www.cdc.gov/nchs/nhanes/] presents the detailed survey design, methods and available data. In brief, the NHANES study population is representative of the civilian non-institutionalised U.S. population. Mobile examination centers

Results

The demographics of the study subjects is shown in Table 1. Differential significance was not found in age, race, BMI and PIR.

Table 2 shows the results of the univariate linear regression analyses of the relationships among BP, serum concentrations of PFASs and the potential confounders. Most of the confounders were significantly associated. However, calcium intake and PIR were not significantly associated; thus, we did not include them in the multiple linear regression analysis or the

Discussion

This population-based study was the first to identify the association between low-dose exposure to PFOS and increased DBP in adolescents, especially in males.

However, some studies had conflicting conclusions. Research on the offspring of pregnant rats exposed to diverse chemicals has shown that PFOS is associated with hypertension, especially systolic blood pressure. Male offspring in the PFOS group had higher systolic blood pressure values than those of the controls at 7 weeks of age, while a

Conclusion

Our study found that low-dose exposure to PFOS is related to elevated diastolic blood pressure in male adolescents and that the effects of PFOS on blood pressure exhibited a sex difference. The mechanism underlying the effect of PFOS on hypertension may be related to hepatocytes, hypercholesterolaemia and high peripheral resistance, with decreased levels of thyroid hormones and aldosterone increasing DBP.

Funding

This work was supported by the Maternal and Child Health Research Project of Jiangsu Province (F201755); the China Postdoctoral Science Foundation (2018M630585); the Key Project of Science and Technology Development Fund of Nanjing Medical University (2017NJMUZD060); the National Key Research and Development Program of China (2016YFC1101001, 2017YFC1308105); the Nanjing Medical University School Project (NMUC2018012A); and a Key Project supported by the Medical Science and Technology

Declaration of interests

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

The authors declare the following financial interests/personal relationships which may be considered as potential competing interests:

Disclosure statement

The authors declare that they have no competing interests.

Acknowledgement

Xu C and Mo XM designed the study protocol. Xu C and Ma SY conducted the research and performed the data analysis under the close supervision of Wang ZQ, Zhang YX, Shu YQ and Mo XM. Ma J provided language help. The manuscript was drafted by Ma SY and proofread by Xu C.

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Previous research investigating the correlation between prenatal exposure to per- and polyfluoroalkyl substances (PFAS) and subsequent blood pressure (BP) in offspring has yielded limited and contradictory findings. This study was conducted to investigate the potential relationship between maternal PFAS levels during pregnancy and subsequent BP in early childhood. A total of 129 expectant mothers from the Shanghai Birth Cohort were included in the study. Using high-performance liquid chromatography/tandem mass spectrometry, we measured ten PFAS compounds in maternal plasma throughout the pregnancy. When the children reached the age of 4, we examined their systolic BP (SBP) and diastolic BP (DBP), along with mean arterial pressure (MAP) and pulse pressure (PP). Data interpretation employed multiple linear and logistic regression models, complemented by Bayesian kernel machine regression (BKMR).We found that the majority of PFAS concentrations remained stable during pregnancy. The linear and BKMR models indicated a positive relationship between the PFAS mixture in maternal plasma and offspring's DBP and MAP, with perfluorohexanesulphonic acid (PFHxS) having the most significant influence (PFHxS and DBP [first trimester:β=3.03, 95%CI: (1.01,5.05); second trimester: β=2.35, 95%CI: (0.94,3.75); third trimester: β=2.57, 95%CI:(0.80,4.34)]; MAP [first trimester:β=2.55, 95%CI: (0.64,4.45); second trimester: β=2.28, 95%CI: (0.95,3.61); third trimester: β=2.35, 95%CI:(0.68,4.01)]). Logistic regression highlighted an increased risk of prehypertension and hypertension in offspring with higher maternal PFHxS concentrations during all three trimesters [first trimester: OR=2.53, 95%CI:(1.11,5.79), second trimester: OR=2.05, 95%CI:(1.11,3.78), third trimester: OR=3.08, 95%CI:(1.40,6.79)]. A positive correlation was identified between the half-lives of PFAS and the odds ratio (OR) of prehypertension and hypertension in childhood (β=0.139, P=0.010). In conclusion, this research found maternal plasma PFAS concentrations to be positively associated with BP in offspring, with PFHxS showing the most significant influence. This correlation remained consistent throughout pregnancy, and this effect was proportional to the half-lives of PFAS.
Analytical methods employed in the identification and quantification of per- and polyfluoroalkyl substances in human matrices - A scoping review
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Persistent organic pollutants (POPs) represent a possible hazard for the ecosystems, with adverse outcomes on wildlife and humans. POPs have always received interest from the scientific community, and they have also been subject to legal restrictions worldwide on their application and commercialization. Among the broad spectrum of POPs, per- and polyfluoroalkyl substances (PFASs) are considered emerging contaminants due to their potential effect on the ecosystem and human health. These contaminants are widely employed in countless applications, from surfactants and building materials to food packaging. On the other hand, their chemical structure gives them the ability to interact with the environment, causing possible toxic effects for humans and environment. Human biomonitoring is a necessary instrument to indagate the impact of PFASs on human health: in recent years several studies have found detectable levels of PFASs in several biological matrices in humans (blood, hair, nails, and urine).
Here, we review the most recent scientific literature concerning analytical methods employed in the identification and quantification of PFASs focusing on biological matrices. It has been noted that liquid chromatography coupled with mass spectrometry is the main analytical instrumentation employed, while blood and/or serum samples are the main employed human matrices whereas the use of non-invasive matrices is still at the beginning. Various issues directly related to human metabolism of PFASs and the effective amount of PFAS absorbed from the environment still need to be investigated.
Exposure to a mixture of per-and polyfluoroalkyl substances modulates pulmonary expression of ACE2 and circulating hormones and cytokines
2022, Toxicology and Applied Pharmacology
Genetic and environmental factors impact on the interindividual variability of susceptibility to communicable and non-communicable diseases. A class of ubiquitous chemicals, Per- and polyfluoroalkyl substances (PFAS) have been linked in epidemiological studies to immunosuppression and increased susceptibility to viral infections, but possible mechanisms are not well elucidated. To begin to gain insight into the role of PFAS in susceptibility to one such viral infection, Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), male and female C57BL/6 J mice were exposed to control water or a mixture of 5 PFAS (PFOS, PFOA, PFNA, PFHxS, Genx) for 12 weeks and lungs were isolated for examination of expression of SARS-CoV-2-related receptors Angiotensin-Converting Enzyme 2 (ACE2) and others. Secondary analyses included circulating hormones and cytokines which have been shown to directly or indirectly impact on ACE2 expression and severity of viral infections. Changes in mRNA and protein expression were analyzed by RT-qPCR and western blotting and circulating hormones and cytokines were determined by ELISA and MESO QuickPlex. The PFAS mixture decreased Ace2 mRNA 2.5-fold in male mice (p < 0.0001), with no significant change observed in females. In addition, TMPRSS2, ANPEP, ENPEP and DPP4 (other genes implicated in COVID-19 infection) were modulated due to PFAS. Plasma testosterone, but not estrogen were strikingly decreased due to PFAS which corresponded to PFAS-mediated repression of 4 representative pulmonary AR target genes; hemoglobin, beta adult major chain (Hbb-b1), Ferrochelatase (Fech), Collagen Type XIV Alpha 1 Chain (Col14a1), 5’-Aminolevulinate Synthase 2 (Alas2). Finally, PFAS modulated circulating pro and anti-inflammatory mediators including IFN-γ (downregulated 3.0-fold in females; p = 0.0301, 2.1-fold in males; p = 0.0418) and IL-6 (upregulated 5.6-fold in males; p = 0.030, no change in females). In conclusion, our data indicate long term exposure to a PFAS mixture impacts mechanisms related to expression of ACE2 in the lung. This work provides a mechanistic rationale for important future studies of PFAS exposure and subsequent viral infection.
Associations of serum PFOA and PFOS levels with incident hypertension risk and change of blood pressure levels
2022, Environmental Research
Citation Excerpt :
The potential biological pathways may include impaired vasodilation due to oxidative stress. However, all these were cross-sectional studies and potential reverse causality could not be excluded (Averina et al., 2021; Pitter et al., 2020; Bao et al., 2017; Ma et al., 2019; Min et al., 2012; Christensen et al., 2016; Geiger et al., 2014). Our results unexpectedly discovered an inverse association between serum PFOS concentration and incident hypertension risk.
Evidence on the associations of perfluorooctanoic acid (PFOA) and perfluorooctane sulfonate (PFOS) with hypertension or blood pressure (BP) levels was limited and inconsistent. The present prospective study aims to evaluate the longitudinal associations of serum levels of PFOA and PFOS with incident hypertension risk and change of blood pressure levels. At baseline 1080 participants (mean age 62 years, 58.9% females) free of hypertension, cardiovascular disease, diabetes, and cancer were followed up for nearly 5 years. Baseline serum levels of PFOA and PFOS were measured with ultra-performance liquid chromatography-tandem mass spectrometry (UPLC-MS). Hypertension was defined as any of (1) self-reported physician-diagnosed hypertension (2) use of hypotension drugs (3) measured systolic BP ≥ 140 mmHg or diastolic BP ≥ 90 mmHg. Change of BP was evaluated as a difference between twice measurements (BP at follow-up visit－BP at baseline). After adjustment for multiple covariates, serum PFOS levels were negatively correlated with risk of hypertension [RR per lg-unit = 0.94 (95% CI: 0.88, 0.99)] and change of systolic BP [β = −1.48 (95% CI: −2.56, −0.41)]. The highest vs lowest quartiles of PFOS concentration was negatively associated with hypertension risk. Compared with Q1, the RRs (95% CIs) for Q2, Q3, and Q4 were 0.83 (0.67–0.98), 0.81 (0.67–0.97), and 0.81(0.67–0.97), respectively (p for trend = 0.016). The negative associations remained in females but not in males (p for interaction = 0.44). No significant association of PFOA with hypertension risk was observed. Further studies are needed to validate our findings.
Perfluoroalkyl substance mixtures and cardio-metabolic outcomes in highly exposed male workers in the Veneto Region: A mixture-based approach.
2022, Environmental Research
Citation Excerpt :
Conversely, there was no previous published study on the association between PFAS concentrations and blood pressure in occupationally exposed individuals. Available data derived from studies on populations with background levels of exposure (Liao et al., 2020; Lin et al., 2019; Ma et al., 2019; Min et al., 2012) or on highly exposed individuals (Bao et al., 2017; Pitter et al., 2020d), still relatively limited and with contradictory results. An increase in SBP was often associated with higher concentrations of PFOA (Liao et al., 2020; Lin et al., 2019; Min et al., 2012), PFOS (Bao et al., 2017; Min et al., 2012) and PFHxS (Min et al., 2012); while a positive association between PFAS and DBP was found only for PFOS (Liao et al., 2020; Ma et al., 2019) and PFNA (Min et al., 2012).
Perfluoroalkyl substances (PFAS) have been consistently associated with cardio-metabolic traits. Occupational exposures to multiple PFAS with health outcomes have been poorly investigated. The aim of the present study was to examine these associations among former workers involved in PFAS production.
We considered 232 male ex-employees who had worked in a factory (Trissino, Veneto Region, Italy), which produced PFAS and other chemicals during 1968–2018. Out of twelve serum PFAS, only four (PFOA, PFOS, PFHxS, and PFNA) were quantifiable in at least 50% of samples. Non-fasting serum total cholesterol (TC), high-density lipoprotein cholesterol (HDL-C), low-density lipoprotein cholesterol (LDL-C), systolic blood pressure (SBP) and diastolic blood pressure (DBP) were measured. The associations between serum PFAS mixture and considered outcomes were assessed through linear regression mixed models and Weighted Quantile Sum (WQS) regression, adjusting for potential confounders.
PFOA was detected at the highest level, with a median concentration (in ng/mL) of 80.8 (min-max: 0.35–13,033), followed by PFOS (median: 8.55, min-max: 0.35–343), PFHxS (median: 6.8, min-max: 0.35–597) and PFNA (median: 0.8, min-max: 0.35–5). We observed that each A quartile increase in the WQS index was positively associated with the levels of TC (β: 8.41, 95% IC: 0.78–16.0), LDL-C (β: 8.02, 95% IC: 1–15.0) and SBP (β: 3.21, 95% IC: 0.82–5.60). No association of serum PFAS concentration on HDL cholesterol and DBP emerged. WQS analyses revealed a major contribution of PFNA and PFHxS for the cholesterol levels, although PFOA reported the highest concentration. PFOA and PFOS emerged as chemicals of concern regarding the association with SBP.
The results showed a clear association between serum PFAS levels and markers of cardiovascular risk and support the importance of clinical surveillance of cardiovascular risk factors in population with a high exposure to PFAS, especially in the occupational setting.
Association of maternal exposure to perfluoroalkyl and polyfluroalkyl substances with infant growth from birth to 12 months: A prospective cohort study
2022, Science of the Total Environment
Citation Excerpt :
Animal studies have linked maternal PFASs exposure to several impaired developmental outcomes, including pregnancy loss, compromised postnatal survival, delays in postnatal growth and development (Case et al., 2001; Grasty et al., 2005; Lau et al., 2006; Lau et al., 2007; Luebker et al., 2005). Population-based studies have shown that maternal PFASs exposure are associated with decreased birth weight, ponderal index, and head circumference (Apelberg et al., 2007; Blake and Fenton, 2020; Kishi et al., 2015; Li et al., 2017; Liew et al., 2018; Ma et al., 2019; Starling et al., 2017), as well as adiposity/overweight after birth, especially for children and adolescents aged 5 to 19 years (Braun et al., 2016; Halldorsson et al., 2012; Lauritzen et al., 2018), with less evidence on the nutritional status in early infancy (Braun et al., 2021; Shoaff et al., 2018). Compared to older children, infants who developed rapidly during the first 12 months of life after delivery (WHO Multicentre Growth Reference Study Group, 2006) may be more susceptible to intrauterine PFASs exposure.
Although maternal perfluoroalkyl and polyfluroalkyl substances (PFASs) were associated with adverse birth outcomes, much less is known about their impact on infant growth during early infancy.
We investigated the association between maternal PFASs exposure and infant growth during the first 12 months of life.
Participating 2395 pregnancies were recruited from Shanghai Birth Cohort between 2013 and 2016. Ten PFASs were quantified from maternal plasma collected during early pregnancy (median, 15 gestational weeks). We measured infant length, weight, and head circumference at birth, 42 days, 6 months, and 12 months. Linear mixed regression model was used to estimate the associations between PFAS concentrations and repeated measurements of infant growth. Effect modification by infant sex was estimated.
Elevated perfluoroheptanoic acid (PFHpA) concentration was negatively associated with infant length-for-age Z score (LAZ) (β = −0.06, 95% confidence interval (CI): −0.11, −0.01) during the first year. Adverse associations were also observed for perfluorobutane sulfonate (PFBS) and weight-for-length Z score (WFL) (β = −0.02, 95% CI: −0.04, −0.00) and BMI-for-age Z score (BAZ) (β = −0.02, 95% CI: −0.04, −0.00). However, perfluorododecanoic acid (PFDoA) was positively associated with WFL (β = 0.03, 95% CI: 0.00, 0.06) and BAZ (β = 0.03, 95% CI: 0.00, 0.06). The adverse association of PFHpA and LAZ was more pronounced among males (β = −0.06; 95% CI: −0.11, −0.00) than females (β = 0.06; 95% CI: 0.01, 0.12).
In our study, negative associations were found for maternal PFHpA exposure and infant LAZ, PFBS and WFL and BAZ. Meanwhile, maternal PFDoA exposure was positively related with WFL and BAZ. The adverse association of maternal PFHpA exposure and infant LAZ was more pronounced among males. The results should be interpreted with caution, further prospective cohort studies with longitudinal and detailed measures are warranted to confirm these findings.

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^☆: This paper has been recommended for acceptance by Eddy Y. Zeng.

¹: These authors contributed equally to the present study and should be regarded as joint first authors.

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Association between perfluoroalkyl substance concentrations and blood pressure in adolescents☆

Highlights

Abstract

Graphical abstract

Introduction

Section snippets

Subjects

Results

Discussion

Conclusion

Funding

Declaration of interests

Disclosure statement

Acknowledgement

Pediatr. Clin. N. Am.

Sci. Total Environ.

Environ. Pollut.

Bull. Environ. Contam. Toxicol.

Aquat. Toxicol.

Sci. Total Environ.

Chemosphere

Sci. Total Environ.

Chemosphere

Toxicology

Toxicol. Lett.

Toxicol. Lett.

Toxicol. Appl. Pharmacol.

Environ. Res.

Toxicol. Appl. Pharmacol.

Environ. Res.

Environ. Int.

Thyroid disruption by perfluorooctane sulfonate (PFOS) and perfluorooctanoate (PFOA)

J. Endocrinol. Investig.

Perfluorooctane sulfonate (PFOS) impairs the proliferation of C17.2 neural stem cells via the downregulation of GSK-3beta/beta-catenin signaling

J. Appl. Toxicol.

Global burden of hypertension and systolic blood pressure of at least 110 to 115 mm Hg, 1990-2015

J. Am. Med. Assoc.