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Per- and polyfluoroalkyl substances and incident diabetes in midlife women: the Study of Women’s Health Across the Nation (SWAN)

Diabetologia volume 65, pages 1157–1168 (2022)Cite this article

Abstract

Aims/hypothesis

Diabetogenic effects of per- and polyfluoroalkyl substances (PFAS) have been suggested. However, evidence based on prospective cohort studies is limited. We examined the association between serum PFAS concentrations and incident diabetes in the Study of Women’s Health Across the Nation Multi-Pollutant Study (SWAN-MPS).

Methods

We included 1237 diabetes-free women aged 45–56 years at baseline (1999–2000) who were followed up to 2017. At each follow-up visit, women with incident diabetes were identified by the presence of one or more of the following conditions: (1) use of a glucose-lowering medication at any visit; (2) fasting glucose ≥7 mmol/l on two consecutive visits while not on steroids; and (3) any two visits with self-reported diabetes and at least one visit with fasting blood glucose ≥7 mmol/l. Serum concentrations of 11 PFAS were quantified by online solid-phase extraction–HPLC–isotope dilution–tandem MS. Seven PFAS with high detection rates (>96%) (n-perfluorooctanoic acid [n-PFOA], perfluorononanoic acid [PFNA], perfluorohexane sulfonic acid [PFHxS], n-perfluorooctane sulfonic acid [n-PFOS], sum of perfluoromethylheptane sulfonic acid isomers [Sm-PFOS], 2-[N-methyl-perfluorooctane sulfonamido] acetic acid [MeFOSAA] and 2-[N-ethyl-perfluorooctane sulfonamido] acetic acid) were included in data analysis. Cox proportional hazards models were used to compute HRs and 95% CIs. Quantile-based g-computation was used to evaluate the joint effects of PFAS mixtures.

Results

After adjustment for race/ethnicity, site, education, smoking status, alcohol consumption, total energy intake, physical activity, menopausal status and BMI, the HR (95% CI) comparing the lowest with the highest tertile was 1.67 (1.21, 2.31) for n-PFOA (ptrend = 0.001), 1.58 (1.13, 2.21) for PFHxS (ptrend = 0.003), 1.36 (0.97, 1.90) for Sm-PFOS (ptrend = 0.05), 1.85 (1.28, 2.67) for MeFOSAA (ptrend = 0.0004) and 1.64 (1.17, 2.31) for the sum of four common PFAS (n-PFOA, PFNA, PFHxS and total PFOS) (ptrend = 0.002). Exposure to seven PFAS as mixtures was associated with an HR of 2.62 (95% CI 1.12, 6.20), comparing the top with the bottom tertiles for all seven PFAS.

Conclusions/interpretation

This study suggests that PFAS may increase diabetes risk in midlife women. Reduced exposure to these ‘forever and everywhere chemicals’ may be an important preventative approach to lowering population-wide diabetes risk.

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Abbreviations

CDC:

Centers for Disease Control and Prevention

EtFOSAA:

2-(N-ethyl-perfluorooctane sulfonamido) acetic acid

IPW:

Inverse probability weighting

LOD:

Limit of detection

MeFOSAA:

2-(N-methyl-perfluorooctane sulfonamido) acetic acid

MPS:

Multi-Pollutant Study

NHS-II:

Nurses’ Health Study-II

n-PFOA:

Linear PFOA

n-PFOS:

Linear PFOS

PFAS:

Per- and polyfluoroalkyl substances

PFDA:

Perfluorodecanoic acid

PFDoDA:

Perfluorododecanoic acid

PFHxS:

Perfluorohexane sulfonic acid

PFNA:

Perfluorononanoic acid

PFOA:

Perfluorooctanoic acid

PFOS:

Perfluorooctane sulfonic acid

PFUnDA:

Perfluoroundecanoic acid

PPAR:

Peroxisome proliferator-activated receptor

Sb-PFOA:

Sum of branched PFOA isomers

Sm-PFOS:

Sum of perfluoromethylheptane sulfonic acid isomers

SWAN:

Study of Women’s Health Across the Nation

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Acknowledgements

We thank all the women who participated in SWAN. We also thank the late Xiaoyun Ye at CDC for her support in PFAS assessment. We thank the study staff and principal investigators at each of the following sites.

Clinical centres: University of Michigan, Ann Arbor, MI (C. Karvonen-Gutierrez, S. Harlow, M. Sowers); Massachusetts General Hospital, Boston, MA (J. Finkelstein, R. Neer); Rush University, Rush University Medical Center, Chicago, IL (H. Kravitz, L. Powell); University of California, Davis/Kaiser (E. Gold); University of California, Los Angeles (G. Greendale); Albert Einstein College of Medicine, Bronx, NY (C. Derby, R. Wildman, N. Santoro); University of Medicine and Dentistry, New Jersey Medical School, Newark, NJ (G. Weiss); and the University of Pittsburgh, Pittsburgh, PA (K. Matthews).

National Institutes of Health (NIH) Program Office: National Institute on Aging, Bethesda, MD (C. Dutta, W. Rossi, S. Sherman, M. Ory); National Institute of Nursing Research, Bethesda, MD (Program Officers).

Central Laboratory: Central Ligand Assay Satellite Services, University of Michigan, Ann Arbor, MI (D. McConnell).

CDC Laboratory: Division of Laboratory Sciences, National Center for Environmental Health, Centers for Disease Control and Prevention, Atlanta, GA.

SWAN Repository: University of Michigan, Ann Arbor, MI (S. Harlow, D. McConnell, M. Sowers).

Coordinating Center: University of Pittsburgh, Pittsburgh, PA (M. Mori Brooks, K. Sutton-Tyrrell); New England Research Institutes, Watertown, MA (S. McKinlay).

Steering Committee: S. Johnson, C. Gallagher.

Data availability

SWAN provides access to public-use datasets that include data from SWAN screening, the baseline visit and follow-up visits (https://agingresearchbiobank.nia.nih.gov/). To preserve participant confidentiality, some, but not all, of the data used for this manuscript are contained in the public-use datasets. A link to the public-use datasets is also located on the SWAN website: http://www.swanstudy.org/swan-research/data-access/. Investigators who require assistance accessing the public use dataset may contact the SWAN Coordinating Center at the following e-mail address: swanaccess@edc.pitt.edu.

Funding

SWAN has grant support from the NIH, US Department of Health and Human Services (DHHS), through the National Institute on Aging (NIA), the National Institute of Nursing Research (NINR) and the NIH Office of Research on Women’s Health (ORWH) (grants U01NR004061, U01AG012505, U01AG012535, U01AG012531, U01AG012539, U01AG012546, U01AG012553, U01AG012554, U01AG012495 and U19AG063720). The study was also supported by the SWAN Repository (U01AG017719). This publication was supported in part by the National Center for Research Resources and the National Center for Advancing Translational Sciences, NIH, through UCSF-CTSI grant no. UL1 RR024131. This study was also supported by grants from the National Institute of Environmental Health Sciences (NIEHS) R01-ES026578, R01-ES026964 and P30-ES017885, and by the CDC/National Institute for Occupational Safety and Health (NIOSH) grant T42-OH008455. The content of this article is solely the responsibility of the authors and does not necessarily represent the official views of the NIA, NINR, ORWH or the NIH. The findings and conclusions of this report are those of the authors and do not necessarily represent the official position of the CDC. Use of trade names is for identification only and does not imply endorsement by the CDC, the Public Health Service or the DHHS.

Authors’ relationships and activities

The authors declare that there are no relationships or activities that might bias, or be perceived to bias, their work.

Contribution statement

SKP was involved in the design of the analysis plan and wrote the manuscript. XW and ND conducted data analyses and critically revised the manuscript. CAKG, WHH, BM, AMC and SDH were involved in the design of the analysis plan, contributed to interpretation of the data, and critically revised the manuscript. All authors read and approved the final version of the paper. SKP is the guarantor of this work and had full access to all the data in the study and takes responsibility for the contents of the manuscript.

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Authors and Affiliations

  1. Department of Epidemiology, School of Public Health, University of Michigan, Ann Arbor, MI, USA

    Sung Kyun Park, Xin Wang, Ning Ding, Carrie A. Karvonen-Gutierrez, William H. Herman & Siobán D. Harlow

  2. Department of Environmental Health Sciences, School of Public Health, University of Michigan, Ann Arbor, MI, USA

    Sung Kyun Park

  3. Division of Laboratory Sciences, National Center for Environmental Health, Centers for Disease Control and Prevention, Atlanta, GA, USA

    Antonia M. Calafat

  4. Department of Internal Medicine, School of Medicine, University of Michigan, Ann Arbor, MI, USA

    William H. Herman

  5. Department of Biostatistics, School of Public Health, University of Michigan, Ann Arbor, MI, USA

    Bhramar Mukherjee

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  1. Sung Kyun Park
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Park, S.K., Wang, X., Ding, N. et al. Per- and polyfluoroalkyl substances and incident diabetes in midlife women: the Study of Women’s Health Across the Nation (SWAN). Diabetologia 65, 1157–1168 (2022). https://doi.org/10.1007/s00125-022-05695-5

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Keywords

  • Diabetes
  • Midlife women
  • Per- and polyfluoroalkyl substances
  • PFAS
  • Prospective cohort