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A review of cardiovascular effects and underlying mechanisms of legacy and emerging per- and polyfluoroalkyl substances (PFAS)

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Abstract

Cardiovascular disease (CVD) poses the leading threats to human health and life, and their occurrence and severity are associated with exposure to environmental pollutants. Per- and polyfluoroalkyl substances (PFAS), a group of widely used industrial chemicals, are characterized by persistence, long-distance migration, bioaccumulation, and toxicity. Some PFAS, particularly perfluorooctane sulfonic acid (PFOS), perfluorooctanoic acid (PFOA) and perfluorohexanesulfonic acid (PFHxS), have been banned, leaving only legacy exposure to the environment and human body, while a number of novel PFAS alternatives have emerged and raised concerns, such as polyfluoroalkyl ether sulfonic and carboxylic acid (PFESA and PFECA) and sodium p-perfluorous nonenoxybenzene sulfonate (OBS). Overall, this review systematically elucidated the adverse cardiovascular (CV) effects of legacy and emerging PFAS, emphasized the dose/concentration-dependent, time-dependent, carbon chain length-dependent, sex-specific, and coexposure effects, and discussed the underlying mechanisms and possible prevention and treatment. Extensive epidemiological and laboratory evidence suggests that accumulated serum levels of legacy PFAS possibly contribute to an increased risk of CVD and its subclinical course, such as cardiac toxicity, vascular disorder, hypertension, and dyslipidemia. The underlying biological mechanisms may include oxidative stress, signaling pathway disturbance, lipid metabolism disturbance, and so on. Various emerging alternatives to PFAS also play increasingly prominent toxic roles in CV outcomes that are milder, similar to, or more severe than legacy PFAS. Future research is recommended to conduct more in-depth CV toxicity assessments of legacy and emerging PFAS and explore more effective surveillance, prevention, and treatment strategies, accordingly.

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Abbreviations

AHR:

Aryl hydrocarbon receptor

AGTR1:

Angiotensin II receptor 1

BA:

Bulbus arteriosus

BBB:

Blood brain barrier

BMP2:

Bone morphogenetic protein 2

BP:

Blood pressure

BPA:

Bisphenol A

BTB:

Blood–testis barrier

CAD:

Coronary artery disease

CD36:

Cluster of differentiation 36

CHD:

Congenital heart disease

CIMT:

Common carotid artery intima–media thickness

Cnx-43:

Connexin-43

CV:

Cardiovascular

CVD:

Cardiovascular disease

DBP:

Diastolic blood pressure

DA:

Dorsal aorta

DLAV:

Dorsal longitudinal anastomotic vessel

dpf:

Days postfertilization

ED:

Embryonic day

EMPs:

Endothelial microparticles

ESC-CMs:

Embryonic stem cell-derived cardiomyocytes

FAs:

Fatty acids

FTCA:

Fluorotelomer carboxylic acids

GD:

Gestation day

GJ:

Gap junction

HBMECs:

Human brain microvascular endothelial cells

HDL-C:

High-density lipoprotein cholesterol

HFPO-DA (GenX):

Hexafluoropropylene oxide dimer acid

HK:

High-molecular-weight kininogen

HMVECs:

Human microvascular endothelial cells

HRECs:

Human retinal endothelial cells

HUVECs:

Human umbilical vein endothelial cells

ICaL:

L-type Ca2+ current

iNOS:

Inducible nitric oxide synthase

ISV:

Intersegmental vessel

KKS:

Kallikrein–kinin system

LC:

L-Carnitine

LC50 :

50% Lethal concentrations

LDL-C:

Low-density lipoprotein cholesterol

LV:

Left ventricular

MAM:

Mitochondria-associated endoplasmic reticulum membrane

MePOSAA:

2-(N-methyl-perfluorooctane sulfonamido) acetate

MMP9:

Matrix metalloproteinase 9

NHANES:

National health and nutrition examination survey

NF-κB:

Nuclear factor κ-light chain-enhancer of activated B cells

OBS:

Sodium p-perfluorous nonenoxybenzene sulfonate

OxPC:

Oxidized phosphatidylcholine

OxPL:

Oxidized phospholipids

PCB:

Polychlorinated biphenyl

PCV:

Posterior cardinal vein

PFAS:

Per- and polyfluoroalkyl substances

PFDA:

Perfluorodecanoic acid

PFDoA:

Perfluorododecanoic acid

PFHpS:

Perfluoroheptanoic acid

PFHxS:

Perfluorohexanesulfonic acid

PFNA:

Perfluorononanoic acid

PFOA:

Perfluorooctanoic acid

PFOS:

Perfluorooctane sulfonic acid

PFOSA:

Perfluorooctane sulfonamide

PFUnDA:

Perfluoroundecanoic acid

PIVUS:

Prospective Investigation of the Vasculature in Uppsala Seniors

PMPs:

Platelet microparticles

PPAR:

Peroxisome proliferator-activated receptor

PPK:

Plasma prekallikrein

PVD:

Peripheral vascular disease

ROS:

Reactive oxygen species

RV:

Right ventricular

SBP:

Systolic blood pressure

STAT5B:

Signal transducer and activator of transcription 5B

SV:

Sinus venosus

TC:

Total cholesterol

TET:

Translocation methylcytosine dioxygenases

TG:

Triglyceride

TJ:

Tight junction

VEGFR2:

Vascular endothelial growth factor receptor 2

VLDL-C:

Very-low-density lipoprotein cholesterol

6:2 Cl-PFESA (F-53B):

6:2 Polyfluoroether sulfonate chloride

ΔΨm:

Mitochondrial membrane potential

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Acknowledgement

This work was supported by the National Natural Science Foundation of China (22006084); Hubei Key Laboratory of Environmental and Health Effects of Persistent Toxic Substances (PTS2019-05; PTS2019-06); and graphical abstract was modified from Servier Medical Art (http://smart. servier.com/).

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  1. Zeng-Jin Wen and Yi-Jing Wei have contributed equally to this work.

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  1. Institute for Translational Medicine, The Affiliated Hospital of Qingdao University, College of Medicine, Qingdao University, Qingdao, China

    Zeng-Jin Wen, Yi-Jing Wei, Yi-Fei Zhang & Yin-Feng Zhang

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ZJW, YJW, and YFZ searched the literature; YFZ provided inspiration and guidance for writing; ZJW and YJW wrote the manuscript; ZJW prepared all the figures and tables. All the authors read and approved the final manuscript. ZJW and YFZ revised and presented the final submit materials.

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Wen, ZJ., Wei, YJ., Zhang, YF. et al. A review of cardiovascular effects and underlying mechanisms of legacy and emerging per- and polyfluoroalkyl substances (PFAS). Arch Toxicol 97, 1195–1245 (2023). https://doi.org/10.1007/s00204-023-03477-5

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