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The Navigation Guide—Evidence-Based Medicine Meets Environmental Health: Systematic Review of Human Evidence for PFOA Effects on Fetal Growth
Open accessAbstract
Background: The Navigation Guide methodology was developed to meet the need for a robust method of systematic and transparent research synthesis in environmental health science. We conducted a case study systematic review to support proof of concept of the method. Objective: We applied the Navigation Guide systematic review methodology to determine whether developmental exposure to perfluorooctanoic acid (PFOA) affects fetal growth in humans. Methods: We applied the first 3 steps of the Navigation Guide methodology to human epidemiological data: 1) specify the study question, 2) select the evidence, and 3) rate the quality and strength of the evidence. We developed a protocol, conducted a comprehensive search of the literature, and identified relevant studies using prespecified criteria. We evaluated each study for risk of bias and conducted meta-analyses on a subset of studies. We rated quality and strength of the entire body of human evidence. Results: We identified 18 human studies that met our inclusion criteria, and 9 of these were combined through meta-analysis. Through meta-analysis, we estimated that a 1-ng/mL increase in serum or plasma PFOA was associated with a –18.9 g (95% CI: –29.8, –7.9) difference in birth weight. We concluded that the risk of bias across studies was low, and we assigned a “moderate” quality rating to the overall body of human evidence. Conclusion: On the basis of this first application of the Navigation Guide systematic review methodology, we concluded that there is “sufficient” human evidence that developmental exposure to PFOA reduces fetal growth. Citation: Johnson PI, Sutton P, Atchley DS, Koustas E, Lam J, Sen S, Robinson KA, Axelrad DA, Woodruff TJ. 2014. The Navigation Guide—evidence-based medicine meets environmental health: systematic review of human evidence for PFOA effects on fetal growth. Environ Health Perspect 122:1028–1039; http://dx.doi.org/10.1289/ehp.1307893
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“such methods have only recently been developed and utilized in environmental health sciences [23–30].”
From A Systematic Review and Meta-Analysis of Multiple Airborne Pollutants and Autism Spectrum Disorder (2016) · cites this paper as [30]
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“This observation is consistent with our previous systematic reviews, [24, 27, 28, 30]”
From A Systematic Review and Meta-Analysis of Multiple Airborne Pollutants and Autism Spectrum Disorder (2016) · cites this paper as [30]
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Gomis, M. I., Vestergren, R., Nilsson, H., & Cousins, I. T. (2016) · Environmental Science & Technology · doi:10.1021/acs.est.6b01477 · Cited by 52
Yan, S., Zhang, H., Wang, J., Zheng, F. Y., & Dai, J. (2015) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2015.06.043 · Cited by 49
Rayasam, S. D. G., Koman, P. D., Axelrad, D. A., Woodruff, T. J., & Chartres, N. (2022) · Environmental Science & Technology · doi:10.1021/acs.est.2c02079 · Cited by 51
Self-citationYan, B., Wang, J., & Liu, J. (2021) · Water Research · doi:10.1016/j.watres.2021.117371 · Cited by 53
Critical Appraisal of Studies Using Laboratory Animal Models
O'Connor, A. M. C., & Sargeant, J. M. (2014) · ILAR Journal · doi:10.1093/ilar/ilu038 · Cited by 54
“Formal transparent approaches to this combination are available but have infrequently been applied to laboratory animal studies and are not reviewed here (Guyatt et al. 2008, 2011; Johnson et al. 2014; Koustas et al. 2014; Lam et al. 2014; Woodruff and Sutton 2014).”
MethodAutomated screening of research studies for systematic reviews using study characteristics
Tsafnat, G., Glasziou, P., Karystianis, G., & Coiera, E. (2018) · Systematic Reviews · doi:10.1186/s13643-018-0724-7 · Cited by 44
Suman, T. Y., & Kwak, I. (2025) · Journal of Hazardous Materials · doi:10.1016/j.jhazmat.2025.137249 · Cited by 49
Luo, Y., Li, X., Li, J., Gong, X., Wu, T., Li, X., Li, Z., Zhai, Y., Yuan, W., Wang, Y., et al. (2024) · Environmental Science & Technology · doi:10.1021/acs.est.4c00453 · Cited by 50
Liu, Y., Li, N., Papandonatos, G. D., Calafat, A. M., Eaton, C. B., Kelsey, K. T., Chen, A., Lanphear, B. P., Cecil, K. M., Kalkwarf, H. J., et al. (2020) · Environmental Science & Technology · doi:10.1021/acs.est.0c06088 · Cited by 63
Pega, F., Norris, S., Backes, C., Bero, L., Descatha, A., Gagliardi, D., Godderis, L., Loney, T., Modenese, A., Morgan, R., et al. (2019) · Environment International · doi:10.1016/j.envint.2019.105039 · Cited by 44
“As in the Navigation Guide systematic review framework (Johnson et al., 2014), RoB heat maps are used as a visual summary of RoB across domains for individual studies (for an example see Figure 3 on p1033 in da Costa et al.”
MethodSelf-citationPoothong, S., Lundanes, E., Thomsen, C., & Haug, L. S. (2017) · Analytica Chimica Acta · doi:10.1016/j.aca.2016.12.043 · Cited by 44
Prenatal exposures to perfluoroalkyl acids and serum lipids at ages 7 and 15 in females
Maisonet, M., Näyhä, S., Lawlor, D. A., & Marcus, M. (2015) · Environment International · doi:10.1016/j.envint.2015.05.001 · Cited by 47
“Knowledge on the role of prenatal exposures to PFAA is still developing, but growing evidence suggests inverse associations of prenatal exposures of PFAA with fetal growth (Johnson et al., 2014) and a positive association with risk of overweight at age 20 (Halldorsson et al.”
BackgroundGribble, M. O., Bartell, S. M., Kannan, K., Wu, Q., Fair, P. A., & Kamen, D. L. (2015) · Environmental Research · doi:10.1016/j.envres.2015.03.012 · Cited by 43
Liang, D., Taibl, K. R., Dunlop, A. L., Barr, D. B., Ryan, P. B., Everson, T. M., Huels, A., Tan, Y., Panuwet, P., Kannan, K., et al. (2023) · Environmental Science & Technology · doi:10.1021/acs.est.3c04561 · Cited by 46
Waterfield, G., Rogers, M., Grandjean, P., Auffhammer, M., & Sunding, D. L. (2020) · Environmental Health · doi:10.1186/s12940-020-00591-0 · Cited by 56
Potential Developmental and Reproductive Impacts of Triclocarban: A Scoping Review
Rochester, J. R., Bolden, A. L., Pelch, K. E., & Kwiatkowski, C. F. (2017) · Journal of Toxicology · doi:10.1155/2017/9679738 · Cited by 51
Systematic comparison of study quality criteria
Lynch, H. N., Goodman, J. E., Tabony, J. A., & Rhomberg, L. R. (2015) · Regulatory Toxicology and Pharmacology · doi:10.1016/j.yrtph.2015.12.017 · Cited by 48
Gestational Exposure to Perfluorooctanoic Acid (PFOA): Alterations in Motor Related Behaviors
Goulding, D. R., White, S. S., McBride, S. J., Fenton, S. E., & Harry, G. J. (2017) · NeuroToxicology · doi:10.1016/j.neuro.2016.11.008 · Cited by 42
“…identified an association between maternal PFOA exposure and birth weight, Lam et al. (2014) reported an association with reduced birth weight following a meta-analysis of 9 human studies combined with 8 mouse studies that showed an association with reduced birth weight (Koustas et al., 2014).”
InfluentialEnvironmental toxicants and placental function
Bloom, M. S., Varde, M., & Newman, R. (2022) · Best Practice & Research Clinical Obstetrics & Gynaecology · doi:10.1016/j.bpobgyn.2022.09.003 · Cited by 49
Blake, B. E., Rickard, B. P., & Fenton, S. E. (2022) · Frontiers in Toxicology · doi:10.3389/ftox.2022.881347 · Cited by 46
Cope, H. A., Blake, B. E., Love, C. A., McCord, J. P., Elmore, S. A., Harvey, J. B., Chappell, V. A., & Fenton, S. E. (2021) · Emerging contaminants · doi:10.1016/j.emcon.2021.10.004 · Cited by 47
Wikström, S., Hussein, G., Karlsson, A. L., Lindh, C. H., & Bornehag, C.-G. (2021) · Scientific Reports · doi:10.1038/s41598-021-82748-6 · Cited by 41
Rokoff, L. B., Rifas‐Shiman, S. L., Coull, B. A., Cárdenas, A., Calafat, A. M., Ye, X., Gryparis, A., Schwartz, J. D., Sagiv, S. K., Gold, D. R., et al. (2018) · Environmental Health · doi:10.1186/s12940-018-0363-4 · Cited by 42
“A meta-analysis of nine studies found a 19 g (95% CI: -30, − 8) lower birth weight for each ng/mL increment in cord serum or maternal plasma PFOA concentration [10].”
MethodSystematic reviews: Separating fact from fiction
Haddaway, N., & Bilotta, G. S. (2015) · Environment International · doi:10.1016/j.envint.2015.07.011 · Cited by 45
“…unfamiliar to somedisciplines, including environmental health and chemical risk assessment, for which there have only been a handful of SRs attempted so far (e.g. Adams et al., 2014; Alderman et al., 2012; Johnson et al., 2014; Liu et al., 2015; Schinasi and Leon, 2014; Shah and Balkhair, 2011).”
BackgroundHofmann, A., Mishra, J. S., Yadav, P., Dangudubiyyam, S. V., Blesson, C. S., & Kumar, S. (2023) · Journal of Environmental Science and Public Health · doi:10.26502/jesph.96120197 · Cited by 52
“…to be particularly susceptible to PFAS effects, as highlighted by the reported link between PFAS exposure during pregnancy and adverse outcomes such as low birth weight [11, 12], increased maternal weight gain [13], gestational hypertension [14], preeclampsia [15, 16], and gestational diabetes.”
BackgroundChaney, C., & Wiley, K. S. (2023) · Environmental Research · doi:10.1016/j.envres.2023.115714 · Cited by 51
Barton‐Maclaren, T. S., Wade, M. G., Basu, N., Bayen, S., Grundy, J. E., Marlatt, V. L., Moore, R., Parent, L., Parrott, J. L., Grigorova, P., et al. (2021) · Environmental Research · doi:10.1016/j.envres.2021.112225 · Cited by 55
Gyllenhammar, I., Benskin, J. P., Sandblom, O., Berger, U., Ahrens, L., Lignell, S., Wiberg, K., & Glynn, A. W. (2019) · Environmental Science & Technology · doi:10.1021/acs.est.9b01746 · Cited by 54
Taniyasu, S., Yeung, L. W. Y., Lin, H., Yamazaki, E., Eun, H., Lam, P. K. S., & Yamashita, N. (2021) · Chemosphere · doi:10.1016/j.chemosphere.2021.132440 · Cited by 46
Schümann, M., Lilienthal, H., & Hölzer, J. (2021) · Regulatory Toxicology and Pharmacology · doi:10.1016/j.yrtph.2021.104868 · Cited by 58
Nielsen, C., Andersson-Hall, U. K., Lindh, C. H., Ekström, U., Xu, Y., Li, Y., Holmäng, A. B., & Jakobsson, K. (2020) · Environmental Health · doi:10.1186/s12940-020-00626-6 · Cited by 45
Lilienthal, H., Dieter, H. H., Hölzer, J., & Wilhelm, M. (2017) · International Journal of Hygiene and Environmental Health · doi:10.1016/j.ijheh.2017.03.001 · Cited by 39
Vela-Soria, F., García-Villanova, J., Mustieles, V., de Haro, T., Antignac, J., & Fernández, M. F. (2020) · Talanta · doi:10.1016/j.talanta.2020.121577 · Cited by 45
Manea, S., Salmaso, L., Lorenzoni, G., Mazzucato, M., Russo, F., Mantoan, D., Martuzzi, M., Fletcher, T., & Facchin, P. (2020) · Environmental Research · doi:10.1016/j.envres.2020.109282 · Cited by 49
Lee, E.-S., Han, S., & Oh, J. (2015) · Reproductive Toxicology · doi:10.1016/j.reprotox.2015.10.020 · Cited by 41
Chang, C.-J., Barr, D. B., Zhang, Q., Dunlop, A. L., Smarr, M. M., Kannan, K., Panuwet, P., Tangpricha, V., Shi, L., Liang, D., et al. (2021) · Environmental Research · doi:10.1016/j.envres.2021.111713 · Cited by 37
Hölzer, J., Lilienthal, H., & Schümann, M. (2021) · Regulatory Toxicology and Pharmacology · doi:10.1016/j.yrtph.2021.104862 · Cited by 48
Endocrine-Disrupting Chemicals in Human Fetal Growth
Street, M. E., & Bernasconi, S. (2020) · Prime Archives in Molecular Biology · doi:10.37247/pamb.1.2020.42 · Cited by 35
Prenatal and postnatal transfer of perfluoroalkyl substances from mothers to their offspring
Liu, Y., Li, A., An, Q., Liu, K., Zheng, P., Yin, S., & Liu, W.-P. (2021) · Critical reviews in environmental science and technology · doi:10.1080/10643389.2021.1886556 · Cited by 35
“Plenty of literature reported adverse effects of PFASs on the health of infants, such as small for gestational age (Govarts et al., 2018), low birth weight (Johnson et al., 2014), less gut microbiome diversity (Iszatt et al., 2019), thyroid function disorders (de Cock et al., 2014) among others.”
BackgroundEffects of In Utero Exposure to Perfluorooctane Sulfonate on Placental Functions
Wan, H. T., Wong, A. Y.-M., Feng, S., & Wong, C. K. C. (2020) · Environmental Science & Technology · doi:10.1021/acs.est.0c06569 · Cited by 34
Chen, Z., Tian, H., Li, H., Li, J., Hong, R., Feng, S., Wang, C., & Gu, C. (2019) · Chemosphere · doi:10.1016/j.chemosphere.2019.07.032 · Cited by 47
Costa, O., Íñiguez, C., Manzano-Salgado, C. B., Amiano, P., Murcia, M., Casas, M., Irizar, A., Basterrechea, M., Beneíto, A., Schettgen, T., et al. (2019) · Environment International · doi:10.1016/j.envint.2019.05.024 · Cited by 41
Metadata
- Authors
- Johnson, P. I., Sutton, P., Atchley, D. S., Koustas, E., Lam, J., Sen, S., Robinson, K. A., Axelrad, D. A., & Woodruff, T. J.
- Affiliations
- University of California, San Francisco (US)
- Environmental Protection Agency (US)
- Department of Epidemiology and Biostatistics, University of California, San Francisco, San Francisco, California, USA
- Johns Hopkins University (US)
- Corresponding author
- Johnson, Paula I.
- Venue
- Environmental Health Perspectives
- Publisher
- American Chemical Society (ACS)
- Published
- 2014-06-25
- Volume
- 122
- Issue
- 10
- Pages
- 1028-1039
- ISSN
- 0091-6765 (ISSN-L)
- 1552-9924
- PMC
- PMC4181929
- OpenAlex
- W4243002209
- Cited by
- 449
- References
- 131
- Citations by year
- 2026: 29 · 2025: 31 · 2024: 36 · 2023: 43 · 2022: 32 · 2021: 50 · 2020: 68 · 2019: 34 · 2018: 31 · 2017: 42 · 2016: 25 · 2015: 20 · 2014: 8
- FWCI
- 2.88
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- public-domain
- creativecommons.org/licenses/by/4.0/ (vor, 1283 d)
- Locations
- Environmental Health Perspectives (publishedVersion, public-domain)
- PubMed Central (publishedVersion, public-domain)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- U.S. Department of Energy
- U.S. Environmental Protection Agency (RD-83543301)
- New York Community Trust
- Heinz Endowments
- Johnson Family Foundation
- Rose Foundation for Communities and the Environment
- Kaiser Permanente
- Office of Research and Development
- Oak Ridge Institute for Science and Education
- University of California, San Francisco
- National Center For Environmental Assessment
- National Institute of Environmental Health Sciences (ES018135, P01ES022841, ES022841, P20ES018135)
- Topics
- Physical Sciences › Environmental Science › Environmental Chemistry › Per- and polyfluoroalkyl substances research
- Social Sciences › Decision Sciences › Statistics, Probability and Uncertainty › Meta-analysis and systematic reviews
- Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Health, Environment, Cognitive Aging
- Keywords
- perfluorooctanoic acid, fetal growth, birth weight, early life exposure, environmental health, risk of bias, perfluorinated compounds
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