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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Systematic review methods have only recently been developed and utilized in environmental health sciences.
“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]
The observation that author cooperation was necessary to complete the meta-analysis is consistent with the authors' previous systematic reviews.
“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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“…volume 122 | number 10 | October 2014 1029 there have been inconsistent conclusions about the evidence of an association between PFOA and fetal growth (DeWitt et al. 2009; Hekster et al. 2003; Jensen and Leffers 2008; Kennedy et al. 2004; Kudo and Kawashima 2003; Lau et al. 2004, 2007; Lindstrom…”
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Abbott, B. D., Wolf, C. J., Schmid, J., Das, K. P., ZEHR, R. D. J., Helfant, L., Nakayama, S. F., Lindstrom, A. B., Strynar, M. J., & Lau, C. S. (2007) · Toxicological Sciences · doi:10.1093/toxsci/kfm110 · Cited by 262 · see citing works
The GRADE approach and Bradford Hill's criteria for causation
Schünemann, H., Hill, S., Guyatt, G., Akl, E. A., & Ahmed, F. (2011) · Journal of Epidemiology and Community Health · doi:10.1136/jech.2010.119933 · Cited by 262 · see citing works
Midasch, O., Drexler, H., Hart, N., Beckmann, M. W., & Angerer, J. (2007) · International Archives of Occupational and Environmental Health · doi:10.1007/s00420-006-0165-9 · Cited by 260 · see citing works
Animal Research: Reporting <i>In Vivo</i> Experiments: The ARRIVE Guidelines
Kilkenny, C., Browne, W., Cuthill, I. C., Emerson, M., & Altman, D. G. (2010) · The Journal of Gene Medicine · doi:10.1002/jgm.1473 · Cited by 256 · see citing works
Emergency medicine animal research: does use of randomization and blinding affect the results?
Bebarta, V., Luyten, D., & Heard, K. (2003) · Academic Emergency Medicine · doi:10.1111/j.1553-2712.2003.tb00056.x · Cited by 244 · see citing works
Kim, S., Choi, K., Ji, K., Seo, J., Kho, Y., Park, J., Kim, S., Park, S., Hwang, I., Jeon, J.-M., et al. (2011) · Environmental Science and Technology · doi:10.1021/es202408a.s001 · Cited by 243 · cited 1×
“The existence of unmeasured confounders will always be possible with observational studies, but we decided to not let this under mine our ability to make a statement about the available data.”
BackgroundWhite, S., Calafat, A., Kuklenyik, Z., Villanueva, L. R., Zehr, R. D., Helfant, L., Strynar, M., Lindstrom, A., Thibodeaux, J. R., Wood, C., et al. (2006) · Toxicological Sciences · doi:10.1093/toxsci/kfl177 · Cited by 229 · see citing works
Maisonet, M., Terrell, M. L., Mcgeehin, M., Christensen, K., Holmes, A. K., Calafat, A., & Marcus, M. (2012) · Environmental Health Perspectives · doi:10.1289/ehp.1003096 · Cited by 228 · cited 10× · see citing works
“One exception was Maisonet et al. (2012) (see Supplemental Material, Table S13), for which we designated a higher risk of bias for fetal growth measures other than birth weight because of a large amount of missing data for outcomes other than birth weight in that study.”
BackgroundMethodInfluentialDeterminants of Fetal Exposure to Polyfluoroalkyl Compounds in Baltimore, Maryland
Apelberg, B. J., Goldman, L. R., Calafat, A. M., Herbstman, J. B., Kuklenyik, Z., Heidler, J., Needham, L. L., Halden, R. U., & Witter, F. R. (2007) · Environmental Science & Technology · doi:10.1021/es0700911 · Cited by 221 · cited 8× · see citing works
“Study PFOA increase PFOA range (ng/mL) Covariates Apelberg et al. 2007 ln ng/mL 0.3–7.1 ga Apelberg et al. 2007 ln ng/mL 0.3–7.1 ga, ma, bmi, race, par, smk, sex, ht, wtg, dia, hyp Apelberg et al. 2007 25th to 75th percentile 1.2–2.1 ga Apelberg et al. 2007 25th to 75th percentile 1.2–2.1 ga, ma, bmi, race, par, smk,…”
BackgroundMethodInfluentialLam, J., Koustas, E., Sutton, P., Johnson, P. I., Atchley, D. S., Sen, S., Robinson, K. A., Axelrad, D. A., & Woodruff, T. J. (2014) · Environmental Health Perspectives · doi:10.1289/ehp.1307923 · Cited by 214 · cited 3× · see citing works
“…of applying the Navigation Guide method ology to the non human evidence are presented in another review (Koustas et al. 2014), and the results of applying the Navigation Guide methodology to integrate the human and non human evidence streams are presented in a third review (Lam et al. 2014).”
BackgroundMethodInfluentialSelf-citationSawaya, G., Guirguis-Blake, J., Lefevre, M., Harris, R., & Petitti, D. (2007) · Annals of Internal Medicine · doi:10.7326/0003-4819-147-12-200712180-00007 · Cited by 207 · cited 4× · see citing works
“We used criteria and considerations used by IARC (2006), the U.S. Preventive Services Task Force (Sawaya et al. 2007), and the U.S. EPA (1991, 1996) for the type of evidence considered for each of these strength of evidence categories.”
BackgroundMethodInfluentialWolf, C. J., Fenton, S., Schmid, J., Calafat, A., Kuklenyik, Z., Bryant, X. A., Thibodeaux, J. R., Das, K., White, S., Lau, C., et al. (2006) · Toxicological Sciences · doi:10.1093/toxsci/kfl159 · Cited by 199 · see citing works
Perfluorinated Compounds in Umbilical Cord Blood and Adverse Birth Outcomes
Chen, M.-H., Ha, E., Wen, T.-W., Su, Y.-D., Lien, G., Chen, C.-Y., Chen, P.-C., & Hsieh, W. S. (2012) · PLoS ONE · doi:10.1371/journal.pone.0042474 · Cited by 191 · cited 11× · see citing works
“These later publica tions (Chen et al. 2012; Maisonet et al. 2012; Whitworth et al. 2012) were included in our metaanalysis, showing consistent results and an overall reduction in birth weight associated with PFOA exposure.”
BackgroundMethodResultInfluentialThe reproductive toxicology of ammonium perfluorooctanoate (APFO) in the rat
Butenhoff, J. L., Kennedy, G. L., Frame, S. R., O’Connor, J. C., & York, R. G. (2004) · Toxicology · doi:10.1016/j.tox.2003.11.005 · Cited by 188 · see citing works
Hagenaars, A., Vergauwen, L., Coen, W. D., & Knapen, D. (2010) · Chemosphere · doi:10.1016/j.chemosphere.2010.10.076 · Cited by 188 · see citing works
Boberg, J., Metzdorff, S., Wortziger, R., Axelstad, M., Brokken, L., Vinggaard, A., Dalgaard, M., & Nellemann, C. (2008) · Toxicology · doi:10.1016/j.tox.2008.05.020 · Cited by 185 · see citing works
Improving the translational hit of experimental treatments in multiple sclerosis
Vesterinen, H. M., Sena, E. S., ffrench-Constant, C., Williams, A., Chandran, S., & Macleod, M. R. (2010) · Multiple Sclerosis Journal · doi:10.1177/1352458510379612 · Cited by 182 · see citing works
Fetal growth indicators and perfluorinated chemicals: a study in the Danish National Birth Cohort.
Fei, C.-Y., Mclaughlin, J., Tarone, R., & Olsen, J. (2008) · American Journal of Epidemiology · doi:10.1093/aje/kwn095 · Cited by 168 · cited 3× · see citing works
“The Fei et al. study (2007) was the only study that was included in the meta-analysis and was assigned “high” risk of bias for “conflict of interest.”
BackgroundMethodPerfluorooctanoic Acid Exposure and Pregnancy Outcome in a Highly Exposed Community
Savitz, D., Stein, C. R., Bartell, S., Elston, B., Gong, J., Shin, H.-M., & Wellenius, G. (2012) · Epidemiology · doi:10.1097/ede.0b013e31824cb93b · Cited by 163 · cited 13× · see citing works
“…ga, bmi, par, smk Nolan et al. 2009 Low to mid exposure NA ga, ga2, ga3, ma, race, sex, SES Nolan et al. 2009 Low to high exposure NA ga, ga2, ga3, ma, race, sex, SES Savitz et al. 2012b, study II 25th to 75th IQR (ln PFOA) 1.92 ga, ma, par, edu, smk, exposyr, state Savitz et al. 2012b, study II…”
BackgroundMethodResultInfluentialKim, S.-K., Lee, K. T., Kang, C. S., Tao, L., Kannan, K., Kim, K.-R., Kim, C.-K., Lee, J.-S., Park, P., Yoo, Y. W., et al. (2011) · Environmental Pollution · doi:10.1016/j.envpol.2010.09.008 · Cited by 162 · see citing works
Krauth, D., Woodruff, T. J., & Bero, L. (2013) · Environmental Health Perspectives · doi:10.1289/ehp.1206389 · Cited by 160 · cited 2× · see citing works
“We also included the funding source and declared conflicts of interest as a potential source of bias based on empirical data from studies conducted on phar macological treatments that reported evidence of bias associated with funding source (Krauth et al. 2013; Lundh et al. 2012).”
MethodSelf-citationPrenatal Exposure to PFOS or PFOA Alters Motor Function in Mice in a Sex-Related Manner
Onishchenko, N., Fischer, C., Ibrahim, W. N. W., Negri, S., Spulber, S., Cottica, D., & Ceccatelli, S. (2011) · Neurotoxicity research · doi:10.1007/s12640-010-9200-4 · Cited by 152 · see citing works
Maternal exposure to perfluorinated acids and fetal growth
Hamm, M. P., Cherry, N. M., Chan, E., Martin, J. W., & Burstyn, I. (2010) · Journal of Exposure Science & Environmental Epidemiology · doi:10.1038/jes.2009.57 · Cited by 151 · cited 9× · see citing works
“…None Hamm et al. 2010 ln ng/mL < LOD–18 ga, ma, race, grav, mwt, matht, smk, sex Hamm et al. 2010 ng/mL < LOD–18 ga, ma, race, grav, mwt, matht, smk, sex Hamm et al. 2010 1st to 2nd tertile (ng/mL) < LOD– < 1.1 to 1.1–2.1 ga, ma, race, grav, mwt, matht, smk, sex Hamm et al. 2010 1st to 3rd…”
BackgroundMethodResultInfluentialReporting of conflicts of interest in meta-analyses of trials of pharmacological treatments
Roseman, M. (2011) · JAMA · doi:10.1001/jama.2011.257 · Cited by 145 · see citing works
Developmental Origins of Health and Disease: List of contributors
Gluckman, P., & Hanson, M. (2006) · Cambridge University Press eBooks · doi:10.1017/cbo9780511544699 · Cited by 142 · see citing works
White, S., Stanko, J., Kato, K., Calafat, A., Hines, E., & Fenton, S. (2011) · Environmental Health Perspectives · doi:10.1289/ehp.1002741 · Cited by 138 · cited 1× · see citing works
“…the evidence of an association between PFOA and fetal growth (DeWitt et al. 2009; Hekster et al. 2003; Jensen and Leffers 2008; Kennedy et al. 2004; Kudo and Kawashima 2003; Lau et al. 2004, 2007; Lindstrom et al. 2011; Olsen et al. 2009; Post et al. 2012; Steenland et al. 2010; White et al. 2011).”
BackgroundWoodruff, T. J., Sutton, P., & The Navigation Guide Work Group (2011) · Health Affairs · doi:10.1377/hlthaff.2010.1219 · Cited by 134 · see citing works
Self-citationThe effect of prenatal perfluorinated chemicals exposures on pediatric atopy.
Wang, I., Hsieh, W. S., Chen, C.-Y., Fletcher, T., Lien, G., Chiang, H. L., Chiang, C., Wu, T.-N., & Chen, P.-C. (2011) · Environmental Research · doi:10.1016/j.envres.2011.04.006 · Cited by 126 · cited 2× · see citing works
“In addition, by contacting authors of one of the included studies (Wang et al. 2011), we were alerted to an additional study on the same cohort under review at the time (Chen et al. 2012) and were able to include that study in the metaanalysis.”
BackgroundPerfluorinated compounds in relation to birth weight in the Norwegian Mother and Child Cohort Study.
Whitworth, K. W., Haug, L., Baird, D., Becher, G., Hoppin, J., Skjærven, R., Thomsen, C., Eggesbø, M., Travlos, G., Wilson, R., et al. (2012) · American Journal of Epidemiology · doi:10.1093/aje/kwr459 · Cited by 112 · cited 12× · see citing works
“…2009 ng/mL ND–5.3 ma, ga Whitworth et al. 2012 ng/mL median (IQR) = 2.2(1.6–3.0) ga, ma, bmi, par Whitworth et al. 2012 1st to 2nd quartile < 1.65 to 1.65–2.24 ga, ma, bmi, par Whitworth et al. 2012 1st to 3rd quartile < 1.65 to 2.25–3.03 ga, ma, bmi, par Whitworth et al. 2012 1st to 4th…”
BackgroundResultInfluentialSavitz, D., Stein, C. R., Elston, B., Wellenius, G., Bartell, S., Shin, H.-M., Vieira, V., & Fletcher, T. (2012) · Environmental Health Perspectives · doi:10.1289/ehp.1104752 · Cited by 102 · cited 12× · see citing works
“…ga, bmi, par, smk Nolan et al. 2009 Low to mid exposure NA ga, ga2, ga3, ma, race, sex, SES Nolan et al. 2009 Low to high exposure NA ga, ga2, ga3, ma, race, sex, SES Savitz et al. 2012b, study II 25th to 75th IQR (ln PFOA) 1.92 ga, ma, par, edu, smk, exposyr, state Savitz et al. 2012b, study II…”
BackgroundMethodResultInfluentialPerfluorooctanoate: Placental and lactational transport pharmacokinetics in rats.
Hinderliter, P., Mylchreest, E., Gannon, S. A., Butenhoff, J., & Kennedy, G. (2005) · Toxicology · doi:10.1016/j.tox.2005.03.010 · Cited by 101 · see citing works
Nolan, L. A., Nolan, J. M., Shofer, F., Rodway, N., & Emmett, E. (2008) · Reproductive Toxicology · doi:10.1016/j.reprotox.2008.11.001 · Cited by 96 · cited 1× · see citing works
“Maternal age and gestational age may be correlated with PFOA exposure and fetal growth (Fei et al. 2007; Halldorsson et al. 2012; Ode et al. 2013).”
BackgroundWhite, S., Kato, K., Jia, L. T., Basden, B. J., Calafat, A., Hines, E., Stanko, J., Wolf, C. J., Abbott, B., & Fenton, S. (2008) · Reproductive Toxicology · doi:10.1016/j.reprotox.2008.11.054 · Cited by 88 · see citing works
Determinants of maternal and fetal exposure and temporal trends of perfluorinated compounds
Ode, A., Rylander, L., Lindh, C. H., Källén, K., Jönsson, B., Gustafsson, P., Olofsson, P., Ivarsson, S. A., & Rignell‐Hydbom, A. (2013) · Environmental Science and Pollution Research · doi:10.1007/s11356-013-1573-5 · Cited by 88 · cited 1× · see citing works
“Maternal age and gestational age may be correlated with PFOA exposure and fetal growth (Fei et al. 2007; Halldorsson et al. 2012; Ode et al. 2013).”
BackgroundFenton, S., Reiner, J. L., Nakayama, S., Delinsky, A. D., Stanko, J., Hines, E., White, S., Lindstrom, A., Strynar, M., & Petropoulou, S.-S. E. (2009) · Reproductive Toxicology · doi:10.1016/j.reprotox.2009.02.012 · Cited by 80 · see citing works
Umbilical cord blood levels of perfluoroalkyl acids and polybrominated flame retardants.
Arbuckle, T., Kubwabo, C., Walker, M., Davis, K. A., Lalonde, K., Kosarac, I., Wen, S.-W., & Arnold, D. (2013) · International Journal of Hygiene and Environmental Health · doi:10.1016/j.ijheh.2012.03.004 · Cited by 75 · see citing works
DEVELOPMENTAL ORIGINS OF HEALTH AND DISEASE
Gilbert-Barness, E. F. (2007) · Fetal and Pediatric Pathology · doi:10.1080/15513810701394736 · Cited by 68 · see citing works
Effects of perfluorooctanoic acid (PFOA) exposure to pregnant mice on reproduction.
Yahia, D., el-Nasser, M. A., Abedel-Latif, M., Tsukuba, C., Yoshida, M., Sato, I., & Tsuda, S. (2010) · Journal of Toxicological Sciences · doi:10.2131/jts.35.527 · Cited by 67 · see citing works
Preclinical studies of human disease: time to take methodological quality seriously.
van der Worp, H. B., & Macleod, M. R. (2011) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2011.04.008 · Cited by 65 · see citing works
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Perflurooctanoic acid induces developmental cardiotoxicity in chicken embryos and hatchlings.
Jiang, Q.-X., Lust, R., Strynar, M., Dagnino, S., & DeWitt, J. (2012) · Toxicology · doi:10.1016/j.tox.2012.01.005 · Cited by 64 · see citing works
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Boyles, A., Harris, S. F., Rooney, A. A., & Thayer, K. (2011) · Epidemiology · doi:10.1097/ede.0b013e318225ba48 · Cited by 60 · see citing works
Spachmo, B., & Arukwe, A. (2012) · Aquatic Toxicology · doi:10.1016/j.aquatox.2011.07.018 · Cited by 58 · see citing works
Guest Editorial: Biomarkers of Perfluorinated Chemicals and Birth Weight
Savitz, D. (2007) · Environmental Health Perspectives · doi:10.1289/ehp.10923 · Cited by 50 · see citing works
Neurobehavioral Teratogenicity of Perfluorinated Alkyls in an Avian Model
Pinkas, A., Slotkin, T. A., Brick-Turin, Y., Van der Zee, E. A., & Yanai, J. (2010) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2009.11.004 · Cited by 48 · see citing works
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O'Brien, J., Crump, D., Mundy, L. J., Chu, S.-G., McLaren, K., Vongphachan, V., Letcher, R., & Kennedy, S. (2009) · Toxicology Letters · doi:10.1016/j.toxlet.2009.07.004 · Cited by 43 · see citing works
Bellinger, D. (2012) · Neurotoxicology · doi:10.1016/j.neuro.2012.04.003 · Cited by 36 · see citing works
York, R. G., Kennedy, G., Olsen, G., & Butenhoff, J. (2010) · Toxicology · doi:10.1016/j.tox.2010.03.005 · Cited by 30 · see citing works
Evidence-based translational medicine.
Howells, D., & Macleod, M. (2013) · Stroke · doi:10.1161/strokeaha.113.000469 · Cited by 26 · see citing works
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Disturbance of perfluorooctanoic acid on development and behavior in Drosophila larvae
Wang, J.-S., Li, Y., Liu, Y., Zhang, H., & Dai, J. (2010) · Environmental Toxicology and Chemistry · doi:10.1002/etc.237 · Cited by 19 · see citing works
Are developmentally exposed C57BL/6 mice insensitive to suppression of TDAR by PFOA?
Hu, Q., Strynar, M., & DeWitt, J. (2010) · Journal of Immunotoxicology · doi:10.3109/1547691x.2010.520045 · Cited by 13 · see citing works
Flagged first, then by citations
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SYRCLE’s risk of bias tool for animal studies
Hooijmans, C. R., Rovers, M. M., de Vries, R. B., Leenaars, M., Ritskes-Hoitinga, M., & Langendam, M. W. (2014) · BMC Medical Research Methodology · doi:10.1186/1471-2288-14-43 · Cited by 4,415 · see citing works
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“The authors noted similarities in experimental studies (Johnson et al. 2014; Koustas et al. 2014) and concluded that there was “sufficient” human and corroborative toxicology evidence of a detrimental effect of PFOA on birth weight (Johnson et al. 2014; Koustas et al. 2014; Lam et al. 2014).”
BackgroundResultEDC-2: the endocrine society's second scientific statement on endocrine-disrupting chemicals
Gore, A. C., Chappell, V. A., Fenton, S. E., Flaws, J. A., Nadal, A., Prins, G. S., Toppari, J., & Zoeller, R. T. (2015) · Endocrine Reviews · doi:10.1210/er.2015-1010 · Cited by 2,407 · see citing works
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Risk to human health related to the presence of perfluoroalkyl substances in food
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Early Life Exposure to Endocrine Disrupting Chemicals and Childhood Obesity and Neurodevelopment
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Obesity Pathogenesis: An Endocrine Society Scientific Statement
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Key Characteristics of Carcinogens as a Basis for Organizing Data on Mechanisms of Carcinogenesis
Smith, M. T., Guyton, K., Gibbons, C., Fritz, J. M., Portier, C., Rusyn, I., DeMarini, D., Caldwell, J., Kavlock, R., Lambert, P., et al. (2015) · Environmental Health Perspectives · doi:10.1289/ehp.1509912 · Cited by 599 · see citing works
“Progress in the systematic evaluation of published evidence on the adverse health effects of environmental agents has been made through application of methods developed by evidence-based medicine (Koustas et al. 2014).”
MethodHeat exposure and cardiovascular health outcomes: a systematic review and meta-analysis.
Liu, J.-W., Varghese, B., Hansen, A., Zhang, Y., Driscoll, T. G., Morgan, G. G., Dear, K., Gourley, M., Capon, A., & Bi, P. (2022) · Lancet Planetary Health · doi:10.1016/s2542-5196(22)00117-6 · Cited by 550 · see citing works
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Blake, B. E., & Fenton, S. E. (2020) · Toxicology · doi:10.1016/j.tox.2020.152565 · Cited by 499 · see citing works
“…estimates corresponding to the predicted reduction in birth weight in humans [−18.9 g birth weight per 1 ng PFOA/mL maternal serum, 95% CI: −29.8, −7.9; (Johnson et al. 2014)] and in mice [−23.0 mg birth weight per 1 mg PFOA/kg maternal body weight/day, 95% CI: −29.0, −16.0; (Koustas et al. 2014)].”
BackgroundResultInfluentialWoodruff, T. J., & Sutton, P. (2014) · Environmental Health Perspectives · doi:10.1289/ehp.1307175 · Cited by 427 · see citing works
“(Johnson et al. 2014; Koustas et al. 2014; Lam et al. 2014).”
BackgroundInfluentialSelf-citationLiu, J., Varghese, B. M., Hansen, A., Xiang, J., Zhang, Y., Dear, K., Gourley, M., Driscoll, T., Morgan, G., Capon, A., et al. (2021) · Environment International · doi:10.1016/j.envint.2021.106533 · Cited by 406 · see citing works
“As recommended elsewhere regarding the strength of evidence sourced from observational studies (Johnson et al., 2014), we began with a baseline of moderate for the quality of body of evidence.”
BackgroundMethodRappazzo, K., Coffman, E., & Hines, E. (2017) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph14070691 · Cited by 405 · see citing works
“The assigned scores and justification of the scores were evaluated by the other two reviewers (Kristen M. Rappazzo and Erin P. Hines), and any disagreements were resolved by selecting the most conservative judgment, as outlined by Johnson, Sutton, Atchley, Koustas, Lam, Sen, Robinson, Axelrad and Woodruff [19].”
Koustas, E., Lam, J., Sutton, P., Johnson, P. I., Atchley, D. S., Sen, S., Robinson, K. A., Axelrad, D. A., & Woodruff, T. J. (2014) · Environmental Health Perspectives · doi:10.1289/ehp.1307177 · Cited by 349 · see citing works
Self-citationEnvironmental pollutants and child health-A review of recent concerns.
Vrijheid, M., Casas, M., Gascon, M., Valvi, D., & Nieuwenhuijsen, M. (2016) · International Journal of Hygiene and Environmental Health · doi:10.1016/j.ijheh.2016.05.001 · Cited by 344 · see citing works
Mamsen, L. S., Björvang, R. D., Mucs, D., Vinnars, M.-T., Papadogiannakis, N., Lindh, C. H., Andersen, C. Y., & Damdimopoulou, P. (2019) · Environment International · doi:10.1016/j.envint.2019.01.010 · Cited by 338 · see citing works
Rickard, B. P., Rizvi, I., & Fenton, S. E. (2022) · Toxicology · doi:10.1016/j.tox.2021.153031 · Cited by 334 · see citing works
Phillips, N., Craig, N. H., & Steel, D. (2020) · Solutions Manual for Guide to Energy Management, International Version · doi:10.1109/dsn.2013.6575296 · Cited by 312
Per- and polyfluorinated substances (PFASs): Environmental challenges
Krafft, M. P., & Riess, J. G. (2015) · Current Opinion in Colloid & Interface Science · doi:10.1016/j.cocis.2015.07.004 · Cited by 294 · see citing works
Perfluoroalkyl and polyfluoroalkyl substances and human fetal growth: A systematic review
Bach, C., Bech, B., Brix, N., Nøhr, E., Bonde, J. P. E., & Henriksen, T. (2015) · Critical Reviews in Toxicology · doi:10.3109/10408444.2014.952400 · Cited by 282 · see citing works
“Estrogen has been demonstrated to be important in promoting fetal growth (Kaijser et al. 2000).”
BackgroundGRADE: Assessing the quality of evidence in environmental and occupational health
Morgan, R., Thayer, K., Bero, L., Bruce, N., Falck-Ytter, Y., Ghersi, D., Guyatt, G., Hooijmans, C., Langendam, M., Mandrioli, D., et al. (2016) · Environment International · doi:10.1016/j.envint.2016.01.004 · Cited by 273 · see citing works
“Work to-date from the Navigation Guide, NTP, and WHO show the GRADE framework is sufficiently flexible to support use now (Johnson et al., 2013, 2014; Koustas et al., 2014; Lam et al., 2014; NTP, 2015; WHO, 2014a); however, areas for further method assessment have been identified.”
BackgroundMethodInfluentialSelf-citationA Systematic Review and Meta-Analysis of Multiple Airborne Pollutants and Autism Spectrum Disorder
Lam, J., Sutton, P., Kalkbrenner, A., Windham, G., Halladay, A., Koustas, E., Lawler, C., Davidson, L., Daniels, N., Newschaffer, C., et al. (2016) · PLOS ONE · doi:10.1371/journal.pone.0161851 · Cited by 247 · see citing works
“We assumed an initial rating of “moderate” quality to the human bodies of evidence (observational studies), based on previously described rationale [26] and consistent with previous case studies [27, 28, 30], based on consideration of both the values and limitations of observational data in assessing associations betw…”
InfluentialSelf-citationPFAS Environmental Pollution and Antioxidant Responses: An Overview of the Impact on Human Field
Bonato, M., Corrà, F., Bellio, M., Guidolin, L., Tallandini, L., Irato, P., & Santovito, G. (2020) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph17218020 · Cited by 243 · see citing works
Eick, S., Thepaksorn, E. K. H., Izano, M., Cushing, L., Wang, Y.-Z., Smith, S., Gao, S., Park, J.-S., Padula, A., DeMicco, E., et al. (2020) · Environmental Health · doi:10.1186/s12940-020-00654-2 · Cited by 238 · see citing works
Self-citationAnenberg, S., Haines, S., Wang, E., Nassikas, N., & Kinney, P. (2020) · Environmental Health · doi:10.1186/s12940-020-00681-z · Cited by 231 · see citing works
Molecular mechanisms of PFOA-induced toxicity in animals and humans: Implications for health risks.
Li, K., Gao, P., Xiang, P., Zhang, X.-X., Cui, X.-Y., & Ma, L. (2017) · Environment International · doi:10.1016/j.envint.2016.11.014 · Cited by 231 · see citing works
“Based on the Navigation Guide Systematic Review Methodology, Johnson et al. (2014) andKoustas et al. (2014) believe that there are sufficient evidence to link fetal developmental exposure to PFOA and reduction in fetal growth in both humans and animals.”
Apel, P., Angerer, J., Wilhelm, M., & Kolossa-Gehring, M. (2017) · International Journal of Hygiene and Environmental Health · doi:10.1016/j.ijheh.2016.09.007 · Cited by 227 · see citing works
Prenatal Perfluoroalkyl Substance Exposure and Child Adiposity at 8 Years of Age: The HOME Study
Braun, J. M., Chen, A.-M., Romano, M., Calafat, A., Webster, G. M., Yolton, K., & Lanphear, B. (2015) · Obesity · doi:10.1002/oby.21258 · Cited by 223 · see citing works
Lam, J., Koustas, E., Sutton, P., Johnson, P. I., Atchley, D. S., Sen, S., Robinson, K. A., Axelrad, D. A., & Woodruff, T. J. (2014) · Environmental Health Perspectives · doi:10.1289/ehp.1307923 · Cited by 214 · see citing works
Self-citationVerner, M., Loccisano, A., Morken, N., Yoon, M., Wu, H., Mcdougall, R., Maisonet, M., Marcus, M., Kishi, R., Miyashita, C., et al. (2015) · Environmental Health Perspectives · doi:10.1289/ehp.1408837 · Cited by 210 · see citing works
“In addition, the value we used to represent the data from the Washino et al. (2009) study was adjusted for more factors than was the one used by Johnson et al. (2014), and the value we used was closer to the null.”
MethodResultInfluentialBlake, B., Cope, H. A., Hall, S. M., Keys, R. D., Mahler, B., McCord, J. P., Scott, B. E., Stapleton, H., Strynar, M., Elmore, S., et al. (2020) · Environmental Health Perspectives · doi:10.1289/ehp6233 · Cited by 201 · see citing works
“Based on a systematic review of the literature and meta-analysis, the shift in birth weight associated with PFOA exposure has been estimated to be − 18 : 9 g birth weight per 1-ng = mL increase in serum PFOA [95% con fi dence interval (CI): − 29 : 8, − 7 : 9] (Johnson et al. 2014).”
Developmental PBDE Exposure and IQ/ADHD in Childhood: A Systematic Review and Meta-analysis
Lam, J., Lanphear, B., Bellinger, D., Axelrad, D., McPartland, J., Sutton, P. M., Davidson, L., Daniels, N., Sen, Ś., & Woodruff, T. (2017) · Environmental Health Perspectives · doi:10.1289/ehp1632 · Cited by 194 · see citing works
“Weassigned an initial rating of “moderate” quality to human observational studies based on the previously described rationale (Johnson et al. 2014; Koustas et al. 2014; Vesterinen et al. 2014; Woodruff and Sutton 2014), and then we considered potential adjustments (“downgrades” or “upgrades”) to…”
BackgroundMethodInfluentialSelf-citationHazardous waste and health impact: a systematic review of the scientific literature
Fazzo, L., Minichilli, F., Santoro, M., Ceccarini, A., Seta, M. D., Bianchi, F., Comba, P., & Martuzzi, M. (2016) · Environmental Health · doi:10.1186/s12940-017-0311-8 · Cited by 174 · see citing works
Obesity II: Establishing causal links between chemical exposures and obesity
Heindel, J., Howard, S., Agay-Shay, K., Arrebola, J., Audouze, K., Babin, P. J., Barouki, R., Bansal, A., Blanc, E. B., Cave, M., et al. (2022) · Biochemical Pharmacology · doi:10.1016/j.bcp.2022.115015 · Cited by 173 · see citing works
DeLuca, N. M., Minucci, J. M., Mullikin, A., Slover, R., & Cohen Hubal, E. A. (2022) · Environment International · doi:10.1016/j.envint.2022.107149 · Cited by 167 · see citing works
Chartres, N., Cooper, C. B., Bland, G. D., Pelch, K. E., Gandhi, S., BakenRa, A., & Woodruff, T. J. (2024) · Environmental Science and Technology · doi:10.1021/acs.est.3c09524 · Cited by 166 · see citing works
Self-citationDimitrova, A., Ingole, V., Basagaña, X., Ranzani, O., Milà, C., Ballester, J., & Tonne, C. (2021) · Environment International · doi:10.1016/j.envint.2020.106170 · Cited by 164 · see citing works
A review of per- and polyfluorinated alkyl substance impairment of reproduction
Chambers, W. S., Hopkins, J. G., & Richards, S. M. (2021) · Frontiers in Toxicology · doi:10.3389/ftox.2021.732436 · Cited by 164 · see citing works
“Johnson et al. (2014) found an association between lower birth weights and exposure to PFOA, noting an 18.9 g decrease in birth weight for every ng/mL increase in serum PFOA level.”
BackgroundInfluentialChang, C.-J., Barr, D., Ryan, P., Panuwet, P., Smarr, M., Liu, K. H., Kannan, K., Yakimavets, V., Tan, Y.-R., Ly, V., et al. (2021) · Environment International · doi:10.1016/j.envint.2021.106964 · Cited by 154 · see citing works
Li, J., Pega, F., Ujita, Y., Brisson, C., Clays, E., Descatha, A., Ferrario, M., Godderis, L., Iavicoli, S., Landsbergis, P. A., et al. (2020) · Environment International · doi:10.1016/j.envint.2020.105739 · Cited by 195 · see citing works
“Some further refinements of the Navigation Guide method may be warranted (Goodman et al., 2017), but it has been successfully applied in several completed and ongoing systematic reviews (Johnson et al., 2016, 2014; Koustas et al., 2014; Lam et al., 2016a, 2014, 2017, 2016b; Vesterinen et al., 2014).”
MethodSelf-citationMaternal serum levels of perfluoroalkyl substances in early pregnancy and offspring birth weight
Wikström, S., Lin, P., Lindh, C. H., Shu, H., & Bornehag, C.-G. (2019) · Pediatric Research · doi:10.1038/s41390-019-0720-1 · Cited by 152 · see citing works
“In a systematic review of 18 studies (2014), Johnson et al.4 concluded that there is “sufficient” human evidence that prenatal exposure to PFOA reduces fetal growth.”
BackgroundEndocrine-Disrupting Chemicals in Human Fetal Growth
Street, M., & Bernasconi, S. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21041430 · Cited by 146 · see citing works
Early life exposure to per- and polyfluoroalkyl substances (PFASs): a critical review
Winkens, K., Vestergren, R., Berger, U., & Cousins, I. T. (2017) · Emerging Contaminants · doi:10.1016/j.emcon.2017.05.001 · Cited by 145 · see citing works
Hall, S. M., Zhang, S., Hoffman, K., Miranda, M. L., & Stapleton, H. M. (2022) · Chemosphere · doi:10.1016/j.chemosphere.2022.133873 · Cited by 144 · see citing works
Starling, A. P., Adgate, J. L., Hamman, R. F., Kechris, K., Calafat, A. M., Ye, X., & Dabelea, D. (2017) · Environmental Health Perspectives · doi:10.1289/ehp641 · Cited by 142 · see citing works
“Perfluoroalkyl and polyfluoroalkyl substances (PFAS) are widespread and persistent environmental contaminants detected in many populations worldwide, including among pregnant women and infants (Cariou et al. 2015; Jiang et al. 2014; Kato et al. 2014; Manzano-Salgado et al. 2015; Okada et al. 2013).”
BackgroundGreen, M. P., Harvey, A., Finger, B., & Tarulli, G. (2020) · Environmental Research · doi:10.1016/j.envres.2020.110694 · Cited by 142 · see citing works
Review: Evolution of evidence on PFOA and health following the assessments of the C8 Science Panel.
Steenland, K., Fletcher, T., Stein, C. R., Bartell, S., Darrow, L., López-Espinosa, M.-J., Ryan, P., & Savitz, D. (2020) · Environment International · doi:10.1016/j.envint.2020.106125 · Cited by 139 · see citing works
Transfer of perfluoroalkyl substances from mother to fetus in a Spanish birth cohort
Manzano-Salgado, C. B., Casas, M., Lopez-Espinosa, M.-J., Ballester, F., Basterrechea, M., Grimalt, J. O., Jiménez, A.-M., Kraus, T., Schettgen, T., Sunyer, J., et al. (2015) · Environmental Research · doi:10.1016/j.envres.2015.07.020 · Cited by 139 · see citing works
Polycyclic aromatic hydrocarbons and female reproductive health: A scoping review.
Bolden, A., Rochester, J., Schultz, K., & Kwiatkowski, C. (2017) · Reproductive Toxicology · doi:10.1016/j.reprotox.2017.07.012 · Cited by 136 · see citing works
“Scoping reviews are extremely useful and powerful tools for stimulating evidence-based hypotheses that can be tested using systematic review, however, they do not themselves generate answers to research questions [41-44].”
BackgroundPrenatal exposure to perfluoroalkyl substances and birth outcomes in a Spanish birth cohort
Manzano-Salgado, C. B., Casas, M., Lopez-Espinosa, M.-J., Ballester, F., Iñiguez, C., Martinez, D., Costa, O., Santa-Marina, L., Pereda-Pereda, E., Schettgen, T., et al. (2017) · Environment International · doi:10.1016/j.envint.2017.09.006 · Cited by 134 · see citing works
“Prenatal PFOA exposure has been associated with reduced birth weight in animal and human studies, whereas for PFOS the evidence is less consistent (reviewed by Bach et al., 2015a; Johnson et al., 2014; Lam et al., 2014).”
InfluentialJohnson, P. I., Koustas, E., Vesterinen, H., Sutton, P. M., Atchley, D. S., Kim, A., Campbell, M. A., Donald, J. M., Sen, Ś., Bero, L., et al. (2016) · Environment International · doi:10.1016/j.envint.2016.03.009 · Cited by 130 · see citing works
“As with our previous PFOA case study (Koustas et al., 2014) the majority of the included animal studies were “probably high risk of bias”, particularly for the “allocation concealment” and “blinding” domains.”
BackgroundMethodResultInfluentialSelf-citationNegri, E., Metruccio, F., Guercio, V., Tosti, L., Benfenati, E., Bonzi, R., la Vecchia, C., & Moretto, A. (2017) · Critical Reviews in Toxicology · doi:10.1080/10408444.2016.1271972 · Cited by 127 · see citing works
“A systematic review of the toxicological and epidemiological evidence of PFOA effects on fetal growth published up to May 2012 concluded that “developmental exposure to PFOA adversely affects human health based on sufficient evidence of decreased fetal growth in both human and non-human mammalian species” (Johnson et…”
BackgroundMethodInfluentialSymeonides, C., Aromataris, E., Mulders, Y. R., Dizon, J., Stern, C., Barker, T., Whitehorn, A. S., Pollock, D., Marin, T., & Dunlop, S. A. (2024) · Annals of Global Health · doi:10.5334/aogh.4459 · Cited by 123 · see citing works
Mamsen, L., Jönsson, B., Lindh, C. H., Olesen, R. H., Larsen, A., Ernst, E., Kelsey, T., & Andersen, C. (2017) · Science of the Total Environment · doi:10.1016/j.scitotenv.2017.04.058 · Cited by 123 · see citing works
Review of developmental origins of health and disease publications in environmental epidemiology.
Heindel, J., Skalla, L., Joubert, B. R., Dilworth, C., & Gray, K. (2017) · Reproductive Toxicology · doi:10.1016/j.reprotox.2016.11.011 · Cited by 123 · see citing works
DeLuca, N. M., Angrish, M., Wilkins, A., Thayer, K., & Cohen Hubal, E. A. (2021) · Environment International · doi:10.1016/j.envint.2020.106308 · Cited by 122 · see citing works
Cumulative Chemical Exposures During Pregnancy and Early Development
Mitro, S. D., Johnson, T., & Zota, A. R. (2015) · Current Environmental Health Reports · doi:10.1007/s40572-015-0064-x · Cited by 120 · see citing works
Are perfluorooctane sulfonate alternatives safer? New insights from a birth cohort study
Chu, C., Zhou, Y., Li, Q.-Q., Bloom, M. S., Lin, S., Yu, Y.-J., Chen, D., Yu, H.-Y., Hu, L.-W., Yang, B.-Y., et al. (2020) · Environment International · doi:10.1016/j.envint.2019.105365 · Cited by 117 · see citing works
Gyllenhammar, I., Berger, U., Sundström, M., McCleaf, P., Eurén, K., Eriksson, S., Ahlgren, S., Lignell, S., Aune, M., Kotova, N., et al. (2015) · Environmental Research · doi:10.1016/j.envres.2015.05.019 · Cited by 116 · see citing works
“Similar effects have been suggested in epidemiological studies of populations with both high and low exposure, but the causality of the findings are still unclear (Bach et al., 2015; Grandjean et al. 2012; Johnson et al., 2014; Olsen et al., 2009b; Steenland et al., 2010).”
ResultWashington, J. W., Rankin, K., Libelo, E. L., Lynch, D. G., & Cyterski, M. (2019) · Science of The Total Environment · doi:10.1016/j.scitotenv.2018.10.071 · Cited by 114 · see citing works
Perfluoroalkyl acids and their precursors in indoor air sampled in children's bedrooms
Winkens, K., Koponen, J., Schuster, J., Shoeib, M., Vestergren, R., Berger, U., Karvonen, A. M., Pekkanen, J., Kiviranta, H., & Cousins, I. T. (2017) · Environmental Pollution · doi:10.1016/j.envpol.2016.12.010 · Cited by 113 · see citing works
“, 2013) and have been shown to display an array of toxicological effects mostly in animal studies (e.g. Stahl et al., 2011; Lau et al., 2004; Kennedy et al., 2004; Vaughn et al., 2013; Johnson et al., 2014; Olsen et al., 2009).”
BackgroundSagiv, S., Rifas-Shiman, S., Fleisch, A., Webster, T., Calafat, A., Ye, X.-Y., Gillman, M., & Oken, E. (2017) · American Journal of Epidemiology · doi:10.1093/aje/kwx332 · Cited by 113 · see citing works
“(20) estimated a reduction in term birth weight of 18.”
BackgroundVandenberg, L. N., Ågerstrand, M., Beronius, A., Beausoleil, C., Bergman, A., Bero, L., Bornehag, C.-G., Boyer, C. S., Cooper, G., Cotgreave, I., et al. (2016) · Environmental Health · doi:10.1186/s12940-016-0156-6 · Cited by 113 · see citing works
“Element Explanation Example for perfluorooctanoic acid (PFOA) and birth weight in animals (adapted from [54]) Example for perfluorooctanoic acid (PFOA) and birth weight in humans (adapted from [53])”
BackgroundSelf-citationZota, A., Geller, R. J., Romano, L. E., Coleman-Phox, K., Adler, N., Parry, E., Wang, M.-M., Park, J.-S., Elmi, A., Laraia, B., et al. (2018) · Environment International · doi:10.1016/j.envint.2018.02.044 · Cited by 112 · see citing works
Woods, M., Lanphear, B., Braun, J. M., & McCandless, L. (2017) · Environmental Health · doi:10.1186/s12940-017-0332-3 · Cited by 111 · see citing works
Webster, G. M., Rauch, S., Marie, N., Mattman, A., Lanphear, B., & Venners, S. (2015) · Environmental Health Perspectives · doi:10.1289/ehp.1409589 · Cited by 111 · see citing works
Descatha, A., Sembajwe, G. N., Pega, F., Ujita, Y., Baer, M., Boccuni, F., Tecco, C. D., Duret, C., Evanoff, B., Gagliardi, D., et al. (2020) · Environment International · doi:10.1016/j.envint.2020.105746 · Cited by 145 · see citing works
“…(Higgins et al., 2011) and the US Agency for Healthcare Research and Quality (Viswanathan et al., 2008), and has been successfully applied in several completed and ongoing systematic reviews (Johnson et al., 2016, 2014; Koustas et al., 2014; Lam et al., 2014, 2017, 2016a; Vesterinen et al., 2014).”
BackgroundMorgan, R. L., Thayer, K. A., Santesso, N., Holloway, A. C., Blain, R., Eftim, S. E., Goldstone, A. E., Ross, P., Guyatt, G., & Schünemann, H. J. (2018) · Environment International · doi:10.1016/j.envint.2018.08.018 · Cited by 106 · see citing works
Hulshof, C. T. J., Pega, F., Neupane, S., Colosio, C., Daams, J. G., Prakash, K. C., Kuijer, P., Mandić‐Rajčević, S., Masci, F., van der Molen, H. F., et al. (2021) · Environment International · doi:10.1016/j.envint.2020.106349 · Cited by 131 · see citing works
Fromme, H., Wöckner, M., Roscher, E., & Völkel, W. (2017) · International Journal of Hygiene and Environmental Health · doi:10.1016/j.ijheh.2016.12.014 · Cited by 104 · see citing works
Serum Perfluorooctanoic Acid and Birthweight: An Updated Meta-analysis With Bias Analysis
Steenland, K., Barry, V., & Savitz, D. (2018) · Epidemiology · doi:10.1097/ede.0000000000000903 · Cited by 101 · see citing works
Climate Change and Cardiovascular Health: A Systematic Review.
Kazi, D. S., Katznelson, E., Liu, C.-L., Al-Roub, N. M., Chaudhary, R. S., Young, D., McNichol, M., Mickley, L., Kramer, D. B., Cascio, W. E., et al. (2024) · JAMA cardiology · doi:10.1001/jamacardio.2024.1321 · Cited by 98 · see citing works
Goudarzi, H., Araki, A., Itoh, S., Sasaki, S., Miyashita, C., Mitsui, T., Nakazawa, H., Nonomura, K., & Kishi, R. (2016) · Environmental Health Perspectives · doi:10.1289/ehp142 · Cited by 97 · see citing works
The Devil they Knew: Chemical Documents Analysis of Industry Influence on PFAS Science
Gaber, N., Bero, L., & Woodruff, T. (2022) · Annals of Global Health · doi:10.5334/aogh.4013 · Cited by 96 · see citing works
Self-citationMandrioli, D., Schlünssen, V., Ádám, B., Cohen, R. A., Colosio, C., Chen, W., Fischer, A., Godderis, L., Göen, T., Ivanov, I. D., et al. (2018) · Environment International · doi:10.1016/j.envint.2018.06.005 · Cited by 107 · see citing works
Kang, H., Choi, K., Lee, H.-S., Kim, D.-H., Park, N.-Y., Kim, S., & Kho, Y. (2016) · Environmental Research · doi:10.1016/j.envres.2016.04.017 · Cited by 110 · see citing works
Shaffer, R., Sellers, S. P., Baker, M. G., Kalman, R. D. B., Frostad, J., Suter, M. K., Anenberg, S., Balbus, J., Basu, N., Bellinger, D., et al. (2019) · Environmental Health Perspectives · doi:10.1289/ehp5496 · Cited by 94 · see citing works
Effect of Air Pollution on Heart Failure: Systematic Review and Meta-Analysis
Jia, Y., Lin, Z.-N., He, Z., Li, C.-Y., Zhang, Y.-J., Wang, J.-Y., Liu, F.-C., Li, J.-X., Huang, K.-Y., Cao, J., et al. (2023) · Environmental Health Perspectives · doi:10.1289/ehp11506 · Cited by 92 · see citing works
Li, M., Zeng, X.-W., Qian, Z., Vaughn, M., Sauvé, S., Paul, G., Lin, S., Lu, L., Hu, L.-W., Yang, B.-Y., et al. (2017) · Environment International · doi:10.1016/j.envint.2017.03.006 · Cited by 92 · see citing works
Andersen, H., David, A., Freire, C., Fernández, M., D'Cruz, S., Reina-Pérez, I., Fini, J., & Bláha, L. (2022) · Environmental Research · doi:10.1016/j.envres.2022.113935 · Cited by 91 · see citing works
Metabolomics of Childhood Exposure to Perfluoroalkyl Substances: A Cross-Sectional Study
Kingsley, S. L., Walker, D. I., Calafat, A. M., Chen, A., Papandonatos, G. D., Xu, Y., Jones, D. P., Lanphear, B. P., Pennell, K. D., & Braun, J. M. (2019) · Metabolomics · doi:10.1007/s11306-019-1560-z · Cited by 90 · see citing works
Environmental exposure to perchlorate: A review of toxicology and human health
Pleus, R., & Corey, L. M. (2018) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2018.09.001 · Cited by 90 · see citing works
Dong, Z.-M., Wang, H., Yu, Y., Li, Y.-B., Naidu, R., & Liu, Y.-J. (2019) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2019.02.061 · Cited by 89 · see citing works
Paulo, M. S., Ádám, B., Akagwu, C., Akparibo, I., Al‐Rifai, R. H., Bazrafshan, S., Gobba, F., Green, A. C., Ivanov, I., Kežić, S., et al. (2019) · Environment International · doi:10.1016/j.envint.2018.09.039 · Cited by 108 · see citing works
“…of the Navigation Guide method may be warranted (Goodman et al., 2017), but it has been successfully applied in several completed and ongoing systematic reviews (Johnson et al., 2016, 2014; Koustas et al., 2014; Lam et al., 2017, 2015, 2014; Rooney et al., 2016; Vesterinen et al., 2015).”
MethodPFAS concentration during pregnancy in relation to cardiometabolic health and birth outcomes
Gardener, H., Sun, Q., & Grandjean, P. (2020) · Environmental Research · doi:10.1016/j.envres.2020.110287 · Cited by 86 · see citing works
“A uthor M anuscript A uthor M anuscript A uthor M anuscript A uthor M anuscript Mechanisms underlying an association between PFAS exposure and fetal growth remain poorly understood, though PFAS exposure has been associated with low weight at birth in animal models (Koustas et al, 2014).”
BackgroundExposures to chemical mixtures during pregnancy and neonatal outcomes: The HOME study.
Kalloo, G., Wellenius, G., McCandless, L., Calafat, A., Sjödin, A., Romano, M., Karagas, M., Chen, A.-M., Yolton, K., Lanphear, B., et al. (2019) · Environment International · doi:10.1016/j.envint.2019.105219 · Cited by 86 · see citing works
A primer on systematic reviews in toxicology
Hoffmann, S., de Vries, R. B. M., Stephens, M. L., Beck, N. B., Dirven, H. A. A. M., Fowle, J. R., Goodman, J. E., Hartung, T., Kimber, I., Lalu, M. M., et al. (2017) · Archives of Toxicology · doi:10.1007/s00204-017-1980-3 · Cited by 85 · see citing works
“…application of systematic review methodology to toxicological issues has focused primarily on questions regarding the impact of chemicals on human health, e.g., for perfluorooctanoic acid (PFOA) (Johnson et al. 2014; Koustas et al. 2014) or metals (Navas-Acien et al. 2007; Meyer-Baron et al. 2009).”
BackgroundMethodInfluentialEick, S. M., Goin, D. E., Chartres, N., Lam, J., & Woodruff, T. J. (2020) · Systematic Reviews · doi:10.1186/s13643-020-01490-8 · Cited by 82 · see citing works
Self-citationEarly pregnancy serum levels of perfluoroalkyl substances and risk of preeclampsia in Swedish women
Wikström, S., Lindh, C. H., Shu, H., & Bornehag, C.-G. (2019) · Scientific Reports · doi:10.1038/s41598-019-45483-7 · Cited by 82 · see citing works
Effects of high temperatures and heatwaves on dengue fever: a systematic review and meta-analysis
Damtew, Y. T., Tong, M., Varghese, B., Anikeeva, O., Hansen, A., Dear, K., Zhang, Y., Morgan, G. G., Driscoll, T. G., Capon, T., et al. (2023) · EBioMedicine · doi:10.1016/j.ebiom.2023.104582 · Cited by 81 · see citing works
Hulshof, C. T. J., Colosio, C., Daams, J. G., Ivanov, I. D., Prakash, K. C., Kuijer, P., Leppink, N., Mandić‐Rajčević, S., Masci, F., van der Molen, H. F., et al. (2018) · Environment International · doi:10.1016/j.envint.2018.09.053 · Cited by 95 · see citing works
“…may be warranted (Goodman et al., 2017), but it has been successfully applied in several completed and ongoing systematic reviews (Johnson et al., 2014; Koustas et al., 2014; Lam et al., 2014; Vesterinen et al., 2014; Johnson et al., 2016; Lam et al., 2016b; Lam et al., 2017; Lam et al., 2016a).”
BackgroundMethodQiao, L., Gao, L., Zheng, M., Xia, D., Li, J.-G., Zhang, L., Wu, Y.-N., Wang, R., Cui, L., & Xu, C. (2018) · Environmental Science and Technology · doi:10.1021/acs.est.8b02839 · Cited by 81 · see citing works
Endocrine-Disrupting Chemicals & Reproductive Health
Zlatnik, M. (2016) · Journal of midwifery & women's health · doi:10.1111/jmwh.12500 · Cited by 81 · see citing works
Gui, S.-Y., Chen, Y.-N., Wu, K.-J., Liu, W., Wang, W.-J., Liang, H.-R., Jiang, Z.-X., Li, Z.-L., & Hu, C.-Y. (2022) · Frontiers in Public Health · doi:10.3389/fpubh.2022.855348 · Cited by 80 · see citing works
“(51) aimed to examine associations of PFOA with multiple birth outcomes (BW, BL, PI, WC) but was quite inadequate in the number of included studies.”
BackgroundMethodInfluentialPerfluoroalkyl substances in older male anglers in Wisconsin.
Christensen, K., Raymond, M. R., Thompson, B. A., & Anderson, H. (2016) · Environment International · doi:10.1016/j.envint.2016.03.012 · Cited by 78 · see citing works
Knapke, E. T., Magalhães, D. D. P., Dalvie, M. A., Mandrioli, D., & Perry, M. (2021) · Toxicology · doi:10.1016/j.tox.2021.153017 · Cited by 75 · see citing works
The Role of Endocrine Disrupting Chemicals in Gestation and Pregnancy Outcomes
Puche-Juárez, M., Toledano, J. M., Moreno-Fernández, J., Gálvez-Ontiveros, Y., Rivas, A., Díaz-Castro, J., & Ochoa, J. J. (2023) · Nutrients · doi:10.3390/nu15214657 · Cited by 74 · see citing works
“Other studies have reached the conclusion that developmental exposure to PFOA negatively affects fetal growth and birth weight [160].”
BackgroundKashino, I., Sasaki, S., Okada, E., Matsuura, H., Goudarzi, H., Miyashita, C., Okada, E., Ito, Y. M., Araki, A., & Kishi, R. (2020) · Environment International · doi:10.1016/j.envint.2019.105355 · Cited by 74 · see citing works
Does air pollution modify temperature-related mortality? A systematic review and meta-analysis.
Hu, X., Han, W., Wang, Y.-X., Aunan, K., Pan, X.-C., Huang, J., & Li, G. (2022) · Environmental Research · doi:10.1016/j.envres.2022.112898 · Cited by 73 · see citing works
- 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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