Grantee Research Project Results
Final Report: The UCSF Pregnancy Exposures to Environmental Chemicals (PEEC) Children's Center
EPA Grant Number: R835433Center: Center for Integrative Research on Childhood Leukemia and the Environment - 2015
Center Director: Metayer, Catherine
Title: The UCSF Pregnancy Exposures to Environmental Chemicals (PEEC) Children's Center
Investigators: Woodruff, Tracey J.
Institution: University of California - San Francisco
EPA Project Officer: Hahn, Intaek
Project Period: June 1, 2013 through May 31, 2018 (Extended to May 31, 2019)
Project Amount: $3,312,848
RFA: Children's Environmental Health and Disease Prevention Research Centers (with NIEHS) (2012) RFA Text | Recipients Lists
Research Category: Children's Health , Human Health
Objective:
Overall: Our Center's objectives were to: (1) develop novel techniques for early identification of harmful chemical exposures; (2) understand the impact of these exposures on seminal aspects of early human development; (3) translate these findings into prevention-oriented health care and environmental policies; and (4) inspire career choice in environmental health science and science-policy research. Specifically, our goal was to integrate and advance new scientific tools to improve understanding of exposures and effects of environmental chemicals during pregnancy. We focused on endocrine disrupting chemicals (EDCs) exposures, in particular polybrominated diphenyl ethers (PBDEs) and perfluorinated chemicals (PFCs), during the prenatal period as it is a time of critical development that sets the stage for later child health. Our Center has three interconnected research projects and a community outreach and engagement core that is overseen by an administrative core.
Project 1: Modeling the Effects of EDCs on Early Stages of Human Placental Development
Project Investigators: Susan Fisher, Michael McMaster
Project 1 brought together a team of basic scientists to test the hypothesis that exposure to PBDE (BDE-47) or PFC (perfluorooctanoic acid (PFOA)) alter fundamental aspects of human placentation. In doing so, we proposed to develop a cell culture model that can be used to explore the effects on placentation of other environmental chemicals of concern. The placenta plays an important role in regulating prenatal development and adverse effects on the placenta can lead to subsequent effects on infant, as manifested through effects on birthweight, and child health. This project built on the Fisher group's expertise in using cell culture models to study seminal aspects of human placental development. The goal of the project was to map, at high resolution, the effects of these chemicals on the transcriptome (Aim 1), the epigenome (Aim 2) and the functional consequences of the alterations we observe (Aim 3). In Aim 1, we used our in vitro model of human placentation and an unbiased approach, RNA-seq, to understand the pathways in which BDE-47 and/or PFOA are working in terms of effects on trophoblast function. Aim 2 used the same experimental design to carry out a comprehensive analysis of the effects of these chemicals on histone modifications and DNA methylation. Finally, in Aim 3, we studied the functions of molecules that are targets of the environmental chemicals of interest and which we suspect play important roles in human placental development. These experiments employed functional and molecular analyses that allow us to phenotype human trophoblast cells and their defining properties in relation to environmental chemical exposures.
Project 2: Mid-Gestational Exposure to EDCs and Effects on Placental Development
Project Investigators: Tracey Woodruff, Joshua Robinson, Michael McMaster, Saunak Sen
Our project tested the hypotheses that 1) exposures to endocrine disrupting chemicals, such as polybrominated diphenyl ethers (PBDEs) and perfluorinated chemicals (PFCs), can accumulate differently in human fetuses than in pregnant women during gestation and 2) these chemical exposures negatively impact placental development and function, an important outcome that can adversely affect in utero growth, prenatal development, birth weight, and thus, childhood and adult health. This project integrated research between project 1 and project 3 by: using the findings from project 1's in vitro experiments to investigate in vivo relationships between chemical exposures and molecular and morphological markers of effects on placental development; and evaluating associated markers with pathways linked to adverse pregnancy outcomes that were investigated in project 3. The specific aims of this project were to: (1) Compare maternal serum, placenta and fetal liver PBDE levels, and to evaluate a broad range of chemicals in maternal serum and maternal urine, through traditional and novel biomonitoring approaches; and (2) Evaluate the relationship between placental disruption measured via molecular and morphological markers and exposure to PBDEs, PFCs and Organophosphate Flame Retardants.
Project 3: Effects of EDCs and Chronic Psychosocial Stress of Fetal Growth
Project Investigators: Rachel Morello‐Frosh, Marya Zlatnik, Naomi Stotland, Tracey Woodruff
This project examined the hypothesis that prenatal exposures to endocrine disrupting chemicals (EDCs) affect fetal growth outcomes such as birth weight and small for gestational age (SGA), and that these adverse effects are magnified by chronic psychosocial stress. We conducted a prospective study in an economically and ethnically diverse group of pregnant women from two UCSF hospitals: San Francisco General Hospital, which serves predominantly low-income women of color who do not have health insurance, and Mission Bay Hospital, which serves an economically and ethnically diverse population, including women of higher socioeconomic status. We evaluated exposure to two important types of environmental exposures: 1) EDCs - polybrominated diphenyl ethers (PBDEs) and perfluorinated chemicals (PFCs); and 2) chronic psychosocial stress, using objective measures (telomere length in umbilical cord leukocytes and corticotrophin releasing hormone (CRH) levels in maternal plasma) and subjective measures of participants perceived stress (e.g. work stress, social stress, perceived racism, major negative life events, neighborhood conditions, social support, and religion). Accordingly, our specific aims were to: (1) evaluate the relationship between prenatal PBDE and PFC exposures and birth weight; (2) evaluate the relationship between measures of chronic psychosocial stress in the maternal-fetal unit and birth weight outcomes; and (3) assess whether exposure to chronic psychosocial stress in the maternal-fetal unit modifies the relationship between PBDE and PFC exposures and birth weight outcomes.
Core A: Community Outreach and Translation Core (COTC)
Project Investigators: Naomi Stotland, Patrice Sutton, Robert Gould, Tracey Woodruff
The goal of our COTC was to transform the Center's research findings into healthy pregnancies and thus healthy children. To put the science into action, the COTC connected the Center's researchers to an existing and expanding community of affected patients, the public, children's health stakeholders, environmental and clinical scientists, and reproductive and pediatric health care providers. Accordingly the goals of the COTC were to: (1) communicate the science broadly through collecting, integrating, and disseminating the Center's research findings and recommendations for preventing harmful exposures using a wide range of standard and innovative technology-based strategies; (2) harness the evolving science to health care through increasing health professionals' knowledge and awareness of the science and build their capacity to identify and prevent harmful environmental exposures. We focused on reproductive health professionals because they are uniquely positioned to impact exposures during pregnancy- the critical window of human development that was the focus of our research. Our goals were to embed environmental health science in each stage of training and education; and (3) advance prevention-based decision-making by accelerating uptake of the Navigation Guide- a foundational systematic review method for synthesizing existing science about environmental toxics that provides simple, transparent summaries of the evidence that can be used in clinical practice guidelines or other evidence-based recommendations for prevention.
Core B: Administrative Core
Project Investigators: Tracey Woodruff, Naomi Stotland
Our Administrative Core provided the organizational structure needed to manage our Center. More specifically it: 1) managed all meetings internally and externally and oversaw the interactions with stakeholders and the external advisory committee; 2) facilitated the communication and interactions within and outside of the Center including working with our COTC to ensure communications were accurate, timely and appropriate for clinicians and our other stakeholders; 3) facilitated the career development and mentoring of the Faculty Development Investigator (FDI) and junior researchers; and 4) monitored the progress toward achieving the Center's goals.
Summary/Accomplishments (Outputs/Outcomes):
Overall:
As detailed in the final project summaries submitted with this report and in line with the overall mission of NIEHS/EPA Children's Centers, the UCSF PEEC Children's Center studied how complex interactions between the environment chemicals, social factors, and other influences affected children's health via effects on prenatal development. The results of Project 1 found that the placenta may be particularly susceptible to PBDE exposures, altering cytotrophoblasts (CTBs) function and underlying molecular pathways (cytotrophoblasts are key cells that play an important role in implantation and development of the placenta, which is critical to fetal health). Observed perturbations in CTBs may be appropriate biomarkers of PBDE placental toxicity that can be evaluated in vivo. In carrying out this work, we demonstrated how to utilize a primary human CTB model to interrogate environmental chemicals in their ability to cause placental toxicity. Project 2 identified how environmental chemicals accumulate differently in human fetuses than in pregnant women during mid-gestation, and how chemical exposures can negatively impact placental development and function, an important outcome that can adversely affect in utero growth, prenatal development, birth weight, and thus, childhood and adult health. The racial/ethnic and economic diversity of our Project 3 study population of pregnant women enabled us to produce unprecedented data that integrates measurements of prenatal exposures to chemicals and chronic stressors as well as biomarkers of maternal and newborn stress response. This has helped advance scientific understanding about how social and environmental factors affect the health and well-being of pregnant women and their newborns. Our Community Outreach Translation Core (COTC) collaborated with many community partners, health professionals, and organizations to inform and advance science for public health protection. We reached over 5,000 health professionals through talks and CME lectures to diverse, local medical and public health practitioners, pediatricians, obstetric/gynecologists, and members of the Pediatrics Environmental Health Specialty Units (PEHSUs). In addition, we successfully integrated environmental health curriculum within the UCSF medical school education and reached students in Nursing, Pharmacy and Dentistry through other course offerings. We have successful gained recognition of the environment as an important determinant of reproductive and prenatal health in women's health professional societies, including American Congress of Obstetricians and Gynecologists (ACOG), the American Society for Reproductive Medicine (ASRM) and the International Federation of Gynecologists and Obstetricians (FIGO). We have improved the basis of decision making for environmental chemicals through demonstration and dissemination of our Navigation Guide systematic review methodology. Systematic reviews are now used by multiple state, federal, and international authoritative bodies. Further, all UCSF PEEC projects have mentored and trained postdoctoral researchers and junior faculty, as explained in the final project summaries, thereby fostering the next generation of environmental health scientists. Finally, our outreach and dissemination has been extremely successfully, we have given over 200 talks and published 53 peer-reviewed publications.
Project 1: Modeling the Effects of EDCs on Early Stages of Human Placental Development
Over the course of this project, we made tremendous progress in developing the cytotrophoblasts (CTBs) model for toxicological investigations and provided proof in the applicability of the model to test environmental chemicals for their ability to induce placental toxicity. In Years 1-2, using our CTB model system, we 1) characterized baseline conditions on cellular, molecular, and functional levels; 2) developed relevant quantitative functional assays (invasion, migration) for toxicological testing; 3) evaluated the toxicokinetics of BDE-47; 4) determined timing and dosage parameters for compound testing; and 5) demonstrated the high sensitivity of BDE-47 vs. other environmental chemicals of concern (e.g., BPA). In Years 2-3, we performed global transcriptomic (Affymetrix GeneChip Human Gene 2.0 ST Arrays) and methylation (Affymetrix GeneChip Human Gene 2.0 ST Arrays) analyses of the effects of BDE-47 exposure in our CTB model system, and in Years 4-5, we analyzed, interpreted, validated, and summarized the results. These novel assessments provided insight into the potential impacts of environmental chemical exposures on placental development.
In these analyses, we identified BDE-47 to alter human CTBs on functional and molecular levels. For example, a subcytotoxic/relevant concentration (1µM) of BDE-47 induced significant changes in genes linked to morphogenesis, steroid metabolism, inflammation, cell motility, and vascular remodeling, and alterations preceded impairment in function (CTB migration, invasion) observed at a higher concentration (5µM). Validated targets, including IL6 and MMP1, which play roles in placentation and disease, which can serve as correlates of BDE-47 exposure and placental toxicity in future projects (evaluated in project 2 of our center). In parallel with our transcriptomic assessments, we profiled the CpG methylome of BDE-47 and vehicle exposed CTBs following a 24h duration. We identified 758 CpGs as differentially methylated (DM) with BDE-47 exposure (p ≤ 0.005; change ≥ 2.5%). In general, BDE-47 increased global CpG methylation (↑ 0.8% average change across all CpGs); these observations were heightened when the analysis was limited to BDE-47 DM CpGs (↑3.4%). Ninety-three percent of DM CpGs were found to increase in methylation with BDE-47 exposure (708/758 total). On average, methylation changes due to BDE-47 were similar whether exposures were initiated at 3h or 15h (y=0.90x, R2=0.69). Within the BDE-47 DM CpG subset, we identified underrepresentation of CpGs proximal to promoter regions and enriched for intergenic regions. GO analyses of genes near BDE-47 DM CpGs indicated enrichment of pathways involved in hormone response, cellular projection, signaling, ROS-response, morphogenesis, and vesicle transport. We identified an enrichment of DM CpGs on chromosomes 10 and 11. These analyses pointed us towards finding a variable DM CpG cluster on Ch. 11p15.5 known to play a critical role in gestational development and poised to be sensitive to environmental exposures. Interestingly, in general, BDE-47-induced changes in DNA methylation did not correlate with mRNA expression levels; only three genes whose promoters were DM had mRNA levels that were also responsive to BDE-47. Using a primary human CTB model, we demonstrated that PBDEs induced alterations at functional and molecular levels in relevant cells for placentation, suggesting that these environmental contaminants could adversely impact human placental development and contribute to pregnancy complications of placental origin. Large -omic analyses suggested large-scale changes underlying BDE-47 toxicity. These results provided us with a framework to conduct larger toxicological studies utilizing the CTB model.
As related to Aim 3, we continued to validate molecules altered by BDE-47 that have suspected important roles in placental development. Due to the addition of robust proteomic datasets involving BDE-47 and PFOA exposed CTBs, we have focused on targets identified to be disrupted on the protein level to guide these analyses (see below in supplement). Our analyses have led to the novel characterization of proteins (e.g., SQSTM1, NOTUM, PDLIM1, NID1) in the human placenta during mid-gestation.
In addition, utilizing the CTB model, we extended our assessments to other compounds that may alter placental development and CTB differentiation. In a concentration-dependent manner, we found that PFOA induces cytotoxicity and significantly alters CTB invasion, at subcytotoxic concentrations, similar to BDE-47, implicating these cells as a vulnerable population for both exposures. We recently submitted RNA extracts of CTBs exposed to PFOA as well as other environmental pollutants (e.g., lead, cadmium, naled) to the University of California, Berkeley (UCB) Genome Center for RNA sequencing analyses using outside funds. These analyses, which extended from the P01, will provide insight into the potential shared and unique targets of BDE-47 and PFOA (and other environmental contaminants) underlying placental toxicity.
Project 2: Mid-Gestational Exposure to EDCs and Effects on Placental Development
Over the course of this project, we made significant progress in expanding our biomonitoring methods and methods to evaluate molecular and morphological markers of placental development. We successfully collected 130 matched sets of maternal serum, fetal liver, and placenta. Placenta samples were fixed in formalin for future immunohistochemistry analyses. Our collaborators at Department of Toxic Substances (DTSC), Drs. Myrto Petreas and June‐ Soo Park developed new methods for PBDE analysis in serum, liver, and placenta and measured PBDEs in the 130 matched sets of maternal serum, placenta, and fetal liver, finding widespread exposures to PBDEs. We found a dramatic decline of about 45% in PBDE levels of BDE-47, -99 measured in California pregnant women between 2008/09-2011/12, but the levels plateaued between 2011/12-2014. The declines were likely due to phase outs nationally and a ban in California of PBDEs. However, their persistence in the environment could be contributing to the leveling off of exposures. Dr. June-Soo Park also measured organophosphate flame retardants (OPFR) in maternal urine in our 130 study participants. Dr. Roy Gerona completed methods for suspect screening analysis of environmental organic acids (organic compounds that have at least one dissociable proton, focusing on chemicals used in commerce) in maternal serum using LC‐QTOF/MS. This proof of concept approach screened for about 700 environmental organic acids in maternal samples, finding about 65 suspect chemicals detected in greater than 75% of samples (manuscript published in Journal of Exposure Science and Environmental Epidemiology). Dr. Roy Gerona also completed laboratory analysis of PFCs in maternal serum.
Based on findings in Project I, which evaluated the effects of BDE-47 on functional and transcriptomic levels in 2nd trimester human primary cytotrophoblasts; we identified potential biomarkers of PBDE exposure in the placental tissue. We selected four of these targets to further interrogate as potential biomarkers of PBDE exposure in vivo: , MMP1 and PLAC4, molecules with suspected roles in placental development; and HMGCS1 and SCD, members of the cholesterol/fatty acid biosynthesis pathway. We also added proposed biomarkers of pre-eclampsia (GH2, PLAC1) and negative controls/molecules not altered by PBDEs in vitro (NOTUM, EFEMP1) to our analyses. Using antigen-specific antibodies, we independently evaluated the localized expression of each of these targets within a subset of placentas (n=12), pre-identified to be in the upper (>10%) or bottom (>90%) percentiles of ∑PBDE burden within our sample set. Two sections from each placenta were probed and scored blindly by two investigators to determine the relative expression of each marker using a semi-automated method that we developed to quantify relative immunofluorescence intensity within regions of the maternal-fetal interface. We analyzed six regions in total: 1) CTBs invading into the decidua (interstitial invasion); 2) decidual cells; 3) CTBs of the proximal and distal column, 4) villous trophoblasts (STBs and CTBs), 5) mesenchymal cells within the floating villous, and 6) CTBs invading the maternal artery (endovascular invasion). All sections were co-stained with cytokeratin (CK), a marker of CTB populations, and 4',6-diamidino-2-phenylindole (Dapi), a DNA nuclear binding molecule. Specific patterns were observed. For example, SCD was expressed highest in the floating villous CTBs, whereas PLAC4 was predominately expressed in the villous core mesenchyme, interstitial CTBs, and decidua. Relative intensity values for each of the eight biomarkers were summarized. We observed good agreement between investigators (r=0.8) and across technical replicates (r=0.7). Staining patterns varied across individual placentas. Ongoing studies aim to examine correlations via k-means clustering and regression analyses to test relationships between expression profiles of these targets (and potential morphological pathologies) with ∑PBDE concentration levels in maternal serum and placenta, and between PFAS and OPFRs.
Finally, our P01 collaborators have recently published important methodological work using matrix linear models (MLM) as a novel approach for analyzing multi-dimensional high throughput chemical genetic screening data. This new methodology will provide a practical and scalable computational foundation for future research involving the statistical analysis of complex high throughput data on environmental chemicals and biological indicators of toxicity.
Project 3: Effects of EDCs and Chronic Psychosocial Stress of Fetal Growth
We surpassed our enrollment goal by enrolling and completing data collection on 510 diverse research participants for Project 3; please see table for demographic characteristics of our study population. We collected 507 2nd trimester maternal serum samples, 502 2nd trimester maternal urine samples, 205 3rd trimester maternal urine samples, 362 3rd trimester maternal serum samples, and 333 umbilical cord blood samples. Our collaborators at California Department of Toxic Substances, Drs. Myrto Petreas and June-Soo Park, completed PBDE and PFAS analysis on maternal serum. The Fisher lab completed CRH analysis on 497 2nd trimester maternal plasma samples and the Blackburn Lab completed telomere analysis on 330 cord whole blood samples. Since receiving data in fall 2018 on environmental chemical exposures and biomarkers of chronic stress, we have been conducting data analysis and preparing manuscripts for publication.
The Project 3 cohort has been able to continue enrolling participants as part of the NIH Environmental Influences on Child Health Outcomes (ECHO) Program in collaboration with the University of Illinois IKIDS cohort (Schantz, PI). Many of our PEEC Project 3 participants agreed to enroll into the ECHO-wide Program and we are now following and assessing their offspring through four years of age. To date, 334 of the original Project 3 cohort are continuing as part of the ECHO-wide Program.
Core A: Community Outreach and Translation Core (COTC)
Communicate the Science Broadly Our COTC developed a comprehensive strategy to disseminate environmental health research broadly and effectively using both traditional, academic-focused methods (i.e., peer-reviewed publications and presentations at research meetings and symposia) as well as social (blogs, twitter, etc.) and other (TV, radio, print, online) media. Our creative materials are readily available on our website (https://prhe.ucsf.edu) and through the NIEHS Partnerships in Environmental Public Health (PEPH). All That Matters, our series of patient-centered brochures in English and Spanish providing advice on preventing home, food, pesticide, and workplace exposure to toxic chemicals have been distributed tens of thousands times in print and electronic format. On average, we distribute about 2500 print versions of Toxic Matters annually, and have tracked approximately 2400 electronic downloads per year, for a total distribution of roughly 4900 copies per year - or a combined total of about 24,500 Toxic Matters brochures throughout the duration of this grant. Finally, our video lectures on the links between the environment and patient health - presented by the foremost leading reproductive health professionals in the U.S. -have been disseminated and viewed on UCTV over 400,000 times to date.
Harness The Evolving Science To Health Care Training future clinicians and leaders in environmental health is arguably the most "upstream" approach in preventing environmental chemical exposures, as patients largely rely on the advice of their physicians to inform their behaviors and decisions. However, most physicians are untrained in environmental health and unprepared to answer their patients' questions. In response, we have engaged and educated UCSF graduate students and practicing health professionals in environmental health. Throughout the life of this grant, we have made significant advances in integrating environmental health in the educational foundation for 2nd year UCSF medical students. For the past seven years, Dr. Woodruff has given an annual reproductive environmental health lecture as part of the Bridges curriculum, and for the past two years, we have created and implemented a weeklong environmental health curriculum that expands on students' basic familiarity with environmental health, addresses concepts such as clinical appraisal and decision making in the face of uncertainty, and underscores the critical role of the environment in health equity. Both the lecture and weeklong curriculum are mandatory, reaching approximately 170 medical students/year. In addition, we created and implemented an environmental health elective course available to students in the schools of Medicine, Nursing, Pharmacy, and Dentistry, which has reached over 350 students since its inception 7 years ago. While much of our work has focused on educating medical students, we have also focused significant energy in educating practicing health professionals about environmental health. Our team has provided approximately 90 talks - including CME lectures - to diverse local medical and public health practitioners, pediatricians, obstetric/gynecologists, and members of the PEHSU, reaching over 5,000 health professionals.
We have focused on the importance of engaging health professional organizations in advancing environmental health education among their constituents. At the start of this project, we completed the landmark publication the American Congress of Obstetricians and Gynecologists (ACOG) and the American Society for Reproductive Medicine (ASRM) Committee Opinion, Exposure to Toxic Environmental Agents and a companion white paper in September 2013. The Opinion recognized that "patient exposure to toxic environmental chemicals and other stressors is ubiquitous, and preconception and prenatal exposure to toxic environmental agents can have a profound and lasting effect on reproductive health across the life course." The ACOG/ASRM Opinion, which legitimated efforts by health professionals to take action to prevent exposure to toxic chemicals, is a major milestone in our efforts to institutionalize environmental health among health professionals.
This was followed by a 2nd landmark opinion with the International Federation of Gynecologists and Obstetricians (FIGO) on preventing exposures to toxic chemicals and we are now working on more fully integrating environmental health into the Ob/Gyn professional community. FIGO is the leading global voice of reproductive health professionals and FIGO's Member Societies include over 120 countries/territories. Since 2016, we have supported the Reproductive and Developmental Environmental Health (RDEH) Working Group, a workgroup under FIGO. RDEH focuses on capacity building and training, and collaborative research to answer the many knowledge gaps related to the effects of environmental exposures on reproductive capacity and reproductive and developmental outcomes. In early 2019, we supported the establishment of an official RDEH committee within FIGO, reflecting a larger recognition in the organization that environmental health is an inextricable part of maternal and child health.
Advance Prevention-Based Decision-Making Another major activity of our COTC is the advancement and institutionalization of the Navigation Guide, the first ever systematic review methodology for evaluating environmental health science that results in a bottom-line summary of the science. Our work on the Navigation Guide has propelled the field forward and firmly established systematic review methods in environmental health. During the grant time period, we facilitated the meetings of the Navigation Guide Working group as a key method for disseminating the methods and work of systematic reviews. The Navigation Guide Working group consists of about 120 academics and researchers, government scientists and officials, and clinicians from around the world; we have met 23 times during the course of the grant via webinar. We have also conducted extensive outreach and education to increase knowledge and awareness of the method in clinical and decision-making arenas (see list of publications and talks). The National Academy of Sciences recommended systematic reviews in general and the Navigation Guide specifically, as exemplary of scientific approaches for systematic reviews in environmental health in three different reports (Review of the Environmental Protection Agency's State-of-the-Science Evaluation of Nonmonotonic Dose-Response Relationships as they Apply to Endocrine Disruptors (2014), Review of EPA's Integrated Risk Information System (IRIS) Process, Application of Systematic Review (2014), Methods in an Overall Strategy for Evaluating Low-Dose Toxicity from Endocrine Active Chemicals (2017)).
In 2016, our team convened a Navigation Guide meeting of leaders across multiple disciplines. At this meeting we discussed how to advance methods to address key issues in benefits analysis for toxic chemicals, and how to utilize the outcome of the meeting to educate and motivate needed changes in practice with the goal of advancing the scientific basis of decision-making around environmental chemicals. This was a monumental meeting resulting in an important publication (McGartland A, Revesz R, Axelrad DA, Dockins C, Sutton P, Woodruff TJ. Estimating the health benefits of environmental regulations. Science. 2017;357(6350):457-8. Epub 2017/08/05. doi: 10.1126/science.aam8204. PubMed PMID: 28774918; PMCID: PMC6675588) that has significantly advanced the use of systematic review methods in environmental health.
Also in 2017, the EPA mandated systematic reviews for chemical evaluations as part of the newly reformed TSCA. In 2018, we advised the International Agency for Research on Cancer (IARC) on the most current methods for evidence evaluation, and in 2019, IARC used the principles and methods of systematic review to update and strengthen its evaluation process. Finally, also in 2019, the WHO and the International Labor Organization (ILO) announced that they are using the Navigation Guide, to evaluate the burden of disease on 10 pairs of occupational risk factors and health outcomes globally. The project involves over 100 scientists globally and will be the first to comprehensively review the evidence on occupational risk factors, including psychosocial factors, and estimate the burden of death and disease. This along with other uptake by authoritative bodies demonstrates an important global recognition of our work.
Over the course of this grant, the focus of our work has shifted from demonstrating systematic review in environmental health work to scaling and capacity-building through implementation, outreach, training and dissemination for NGOs, academia, industry and government. We have both published peer-reviewed research papers establishing the empirical basis of systematic reviews in environmental health and trained or provided guidance in systematic review to over 200 scientists.
Core B: Administrative Core
Internal Meetings and Communication
PEEC PIs and staff met regularly during scheduled monthly meetings. The meetings included progress and data presentations for each project and consisted of a mix of in-person meetings and webinars. The Administrative Core (Core B) was allotted time at each meeting to address program related topics such as Quality Assurance, Children's Environmental Health Center meetings, External Advisory Committee meeting preparation and to distribute other administrative information to PIs and staff.
Children's Environmental Health Center (CEHC) Calls and Annual Meeting
Monthly CEHC calls were led by the Center's PI, Dr. Tracey Woodruff, and Project Director/Center Evaluator, Annemarie Charlesworth. These meetings included all CEHC members and PEEC PIs. Additionally, Dr. Tracey Woodruff attended the NIEHS/EPA Children's Centers Annual Meetings; however, in October 2017, the NIEHS/EPA Children's Centers Annual Grantee Meeting was held in San Francisco and the majority of faculty and staff working on PEEC was able to attend.
External Advisory Committee
The PEEC External Advisory Committee (EAC) met in person at the beginning of the grant project to give advice the work of the Center, then met virtually as a group in 2016. After that, EAC members participated in project-specific webinars each year of the grant where each project would meet individually with EAC members, project leads, and research staff. The intent of the smaller meetings was to leverage the expertise of certain EAC members with the research questions associated with each project. During the EAC meeting, project leads delivered a comprehensive presentation on accomplishments, current obstacles, and future directions, which was followed by a discussion with EAC members, advising on challenges and suggestions for future research. A full report, including feedback from a post-meeting evaluation was conducted by Center Evaluator, Annemarie Charlesworth, and was compiled for our internal records. This report was used to drive the continuation of our work for the next year.
Quality Assurance
QAPP was performed at the beginning of each year and again at the close of the funding period. The Center Quality Assurance Manager performed on-site audits with the McMaster lab (Project 1), the PRHE ab at San Francisco General Hospital (Projects 2 & 3), The Gerona Lab (Projects 2 & 3), and the Park lab at the Department for Toxic Substances Control (DTSC) in Berkeley (Projects 2 & 3).
QAPP audits consisted of introduction meetings, a demonstration of sample/data collection and storage, a visual inspection of training materials, standard operating procedures and certifications, and a systems audit checklist for laboratory management systems and sample collection quality, which were reviewed with project PIs and staff and updated for accuracy.
Contact and Communication with NIEHS and EPA
The Center maintained continuous communication with EPA and NIEHS in addition to participating in the monthly CEHC calls and attending the annual Children's Centers Grantee Meeting. Dr. Woodruff communicated with NIEHS and EPA program officers regularly during in-person meetings, email exchanges, and telephone calls during the course of this project period. In addition, we completed quarterly highlights forms starting in May 2017 as required by NIEHS.
Opportunities for Training and Professional Development
As noted previously, we spent significant time training and mentoring students, postdoctoral scholars, and junior faculty in environmental health. Dr. Woodruff mentored four postdocs, Dr. Morello-Frosch mentored three postdocs, Dr. Fisher mentored one, and Dr. Robinson mentored one. Dr. Woodruff is a co-mentor, along with Dr. Susan Fisher (primary mentor), of Dr. Joshua Robinson. Dr. Robinson started working on this project as a postdoc and successfully received an NIEHS funded K99, Pathways to Independence Grant entitled, "Polybrominated Diphenyl Ether Effects on Human Neuronal Development." After his postdoc, he was recruited to be a junior faculty member at UCSF and he was subsequently named the Faculty Development Investigator (FDI). Dr. Robinson actively worked on Research Projects 1 and 2. In addition, Dr. Woodruff continues to mentor junior faculty member Amy Padula, who was recruited into a faculty position with support from our P01. Dr. Padula worked on Project 3 and is now a Co-Investigator on the ECHO Program at UCSF. Finally, we have trained six UCSF medical students in environmental health, who have subsequently worked on our team in developing educational materials. We worked with two graduate MPH students and five undergraduate research interns from UC Berkeley; all student interns engaged in projects tailored to their interests in pursuing professional careers in environmental health.
Journal Articles: 48 Displayed | Download in RIS Format
Other center views: | All 77 publications | 54 publications in selected types | All 48 journal articles |
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Abrahamsson D, Park J, Singh R, Sirota M, Woodruff T. Applications of Machine Learning to In Silico Quantification o Chemicals without Analytical Standards. Journal of Chemical Information and Modeling 2020;60(6):2718-2727. |
R835433 (Final) R835643 (Final) |
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Abrahamsson D, Siddharth A, Young T, Sirota M, Park J, Martin J, Woodruff T. In Silico Structure Predictions for Non-targeted Analysis: From Physicochemical Properties to Molecular Structures. JOURNAL OF THE AMERICAN SOCIETY FOR MASS SPECTROMOTY 2022;33(7):1134-1147 |
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Abrahamsson D, Brueck C, Prasse C, Lambropoulou D, Koronaiou L, Wang M, Park J, Woodruff T. Extracting Structural Information from Physicochemical Property Measurements Using Machine Learning-A New Approach for Structure Elucidation in Non-targeted Analysis. ENVIRONMENTAL SCIENCE & TECHNOLOGY 2023;27(40):14827-14838 |
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Bland G, Abrahamsson D, Wang M, Zlatnik M, Morello-Frosch R, Park J, Sirota M, Woodruff T. Exploring applications of non-targeted analysis in the characterization of the prenatal exposome. SCIENCE OF THE TOTAL ENVRIONMENT 2023;912(169458) |
R835433 (Final) |
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Casey JA, Karasek D, Ogburn, EL, Goin DE, Dang K, Braveman PA, Morello-Frosch R. Coal and oil power plant retirements in California:association with reduced preterm birth among populations nearby. American Journal of Epidemiology 2018;187(8):1586-1594. |
R835433 (2017) R835433 (Final) |
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Casey JA, Gemmill A, Karasek D, Ogburn, EL, Goin DE, Morello-Frosch R. Increase in fertility following coal and oil power plant retirements in California. Environmental Health 2018;17(1):44 (10 pp.). |
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Di Renzo GC, Conry JA, Blake J, DeFrancesco MS, DeNicola N, Martin Jr. JN, McCue KA, Richmond D, Shah A, Sutton P, Woodruff TJ, van der Poel SZ, Giudice LC. International Federation of Gynecology and Obstetrics opinion on reproductive health impacts of exposure to toxic environmental chemicals. International Journal of Gynaecology and Obstetrics 2015;131(3):219-225. |
R835433 (2015) R835433 (Final) |
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Gerona RR, Pan J, Zota AR, Schwartz JM, Friesen M, Taylor JA, Hunt PA, Woodruff TJ. Direct measurement of bisphenol A (BPA), BPA glucuronide and BPA sulfate in a diverse and low-income population of pregnant women reveals high exposure, with potential implications for previous exposure estimates: a cross-sectional study. Environmental Health 2016;15:50 (14 pp.). |
R835433 (2015) R835433 (2017) R835433 (Final) |
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Gerona RR, Schwartz JM, Pan J, Friesen MM, Lin T, Woodruff TJ. Suspect screening of maternal serum to identify new environmental chemical biomonitoring targets using liquid chromatography-quadrupole time-of-flight mass spectrometry. Journal of Exposure Science & Environmental Epidemiology 2018;28(2):101-108. |
R835433 (2017) R835433 (Final) R835643 (2017) |
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Goin D, Abrahamsson D, Wang M, Jiang T, Park J, Sirota M, Morello-Frosch R, DeMicco E, Zlatnik M, Woodruff T. Disparities in chemical exposures among pregnant women and neonates by socioeconomic and demographic characteristics:A nontargeted approach. ENVIRONMENTAL RESEARCH 2022;215(1):114158. |
R835433 (Final) |
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Goin D, Abrhamsson D, Wang M, Park J, Sirota M, Morello-Frosch R, DeMicco E, Trowbridge J, Augt L, O'Connell S, Ladella S, Zlatnik M, Woodruff T. Investigating geographic differences in environmental chemical exposures in maternal and cord sera using non-targeted screening and silicone wristbands in California. JOURNAL OF EXPOSURE SCIENCE AND ENVIRONMENTAL EPIDEMIOLOGY 2022;. |
R835433 (Final) |
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Huang H, Wang A, Morello-Frosch R, Lam J, Sirota M, Padula A, Woodruff TJ. Cumulative risk and impact modeling on environmental chemical and social stressors. Current Environmental Health Reports 2018;5(1):88-99. |
R835433 (2017) R835433 (Final) |
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Johnson PI, Sutton P, Atchley DS, Koustas E, Lam J, Sen S, Robinson KA, Axelrad DA, Woodruff TJ. The Navigation Guide—evidence-based medicine meets environmental health: systematic review of human evidence for PFOA effects on fetal growth. Environmental Health Perspectives 2014;122(10):1028-1039. |
R835433 (2014) R835433 (Final) |
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Johnson PI, Koustas E, Vesterinen HM, Sutton P, Atchley DS, Kim AN, Campbell M, Donald JM, Sen S, Bero L, Zeise L, Woodruff TJ. Application of the Navigation Guide systematic review methodology to the evidence for developmental and reproductive toxicity of triclosan. Environment International 2016;92-93:716-728. |
R835433 (2015) R835433 (2016) R835433 (Final) |
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Koustas E, Lam J, Sutton P, Johnson PI, Atchley DS, Sen S, Robinson KA, Axelrad DA, Woodruff TJ. The Navigation Guide—evidence-based medicine meets environmental health:systematic review of nonhuman evidence for PFOA effects on fetal growth. Environmental Health Perspectives 2014;122(10):1015-1027. |
R835433 (2014) R835433 (Final) |
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Lam J, Koustas E, Sutton P, Johnson PI, Atchley DS, Sen S, Robinson KA, Axelrad DA, Woodruff TJ. The Navigation Guide—evidence-based medicine meets environmental health:integration of animal and human evidence for PFOA effects on fetal growth. Environmental Health Perspectives 2014;122(10):1040-1051. |
R835433 (2014) R835433 (Final) |
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Lam J, Lanphear BP, Bellinger D, Axelrad DA, McPartland J, Sutton P, Davidson L, Daniels N, Sen S, Woodruff TJ. Developmental PBDE exposure and IQ/ADHD in childhood: a systematic review and meta-analysis. Environmental Health Perspectives 2017;125(8):086001 (20 pp.). |
R835433 (2016) R835433 (2017) R835433 (Final) |
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Lam J, Kotas E, Sutton P, Padula A, Cabana M, Vesterinen H, Griffiths C, Dickie M, Daniels N, Whitaker E, Woodruff T. Exposure to formaldehyde and asthma outcomes:A systematic review, meta-analysis, and economic assessment. PLOS ONE 2021;16(3):e0248258. |
R835433 (Final) |
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Lam J, Sutton P, Kalkbrenner A, Windham G, Halladay A, Koustas E, Lawler C, Davidson L, Daniels N, Newschaffer C, Woodruff T. A Systematic Review and Meta-Analysis of Multiple Airborne Pollutants and Autism Spectrum Disorder. PLoS One. 2016 Sep 21;11(9):e0161851. doi:10.1371/journal.pone.0161851. PubMed PMID:27653281; PubMed Central PMCID:PMC5031428. |
R835433 (2016) R835433 (Final) |
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McHale CM, Osborne G, Morello-Frosch R, Salmon AG, Sandy MS, Solomon G, Zhang L, Smith MT, Zeise L. Assessing health risks from multiple environmental stressors: moving from G×E to I×E. Mutation Research 2018;775:11-20. |
R835433 (2017) R835433 (Final) |
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Morello-Frosch R, Cushing LJ, Jesdale BM, Schwartz JM, Guo W, Guo T, Wang M, Harwani S, Petropoulou SE, Duong W, Park J-S, Petreas M, Gajek R, Alvaran J, She J, Dobraca D, Das R, Woodruff TJ. Environmental chemicals in an urban population of pregnant women and their newborns from San Francisco. Environmental Science & Technology 2016;50(22):12464-12472. |
R835433 (2015) R835433 (2017) R835433 (Final) |
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Morgan RL, Thayer KA, Bero L, Bruce N, Falck-Ytter Y, Ghersi D, Guyatt G, Hooijmans C, Langendam M, Mandrioli D, Mustafa RA, Rehfuess EA, Rooney AA, Shea B, Silbergeld EK, Sutton P, Wolfe MS, Woodruff TJ, Verbeek JH, Holloway AC, Santesso N, Schunemann HJ. GRADE: assessing the quality of evidence in environmental and occupational health. Environment International 2016;92-93:611-616. |
R835433 (2015) R835433 (2016) R835433 (Final) |
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Parry E, Zota AR, Park J-S, Woodruff TJ. Polybrominated diphenyl ethers (PBDEs) and hydroxylated PBDE metabolites (OH-PBDEs): a six-year temporal trend in Northern California pregnant women. Chemosphere 2018;195-777-783. |
R835433 (2017) R835433 (Final) |
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Pelch K, Reade A, Kwiatkowski C, Merced-Nieves F, Cavalier H, Schultz K, Wolffe T, Varshavsky J. The PFAS-Tox Database:A systematic evidence map of health studies on 29 per-and polyfluoroalkyl substances. ENVIRONMENTAL INTERNATIONAL 2022;167(107408). |
R835433 (Final) |
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Roadmap Epigenomics Consortium, Kundaje A, Meuleman W, Ernst J, Bilenky M, Yen A, Heravi-Moussavi A, Kheradpour P, Zhang Z, Wang J, Ziller MJ, Amin V, Whitaker JW, Schultz MD, Ward LD, Sarkar A, Quon G, Sandstrom RS, Eaton ML, Wu YC, Pfenning AR, Wang X, Claussnitzer M, Liu Y, Coarfa C, Harris RA, Shoresh N, Epstein CB, Gjoneska E, Leung D, Xie W, Hawkins RD, Lister R, Hong C, Gascard P, Mungall AJ, Moore R, Chuah E, Tam A, Canfield TK, Hansen RS, Kaul R, Sabo PJ, Bansal MS, Carles A, Dixon JR, Farh KH, Feizi X, Karlic R, Kim AR, Kulkarni A, Li D, Lowdon R, Elliott G, Mercer TR, Naph SJ, Onuchic V, Polak P, Rajagopal N, Ray P, Sallari RC, Siebenthall KT, Sinnott-Armstrong NA, Stevens M, Thurman RE, Wu J, Zhang B, Zhou X, Beaudet AE, Boyer LA, De Jager PL, Farnham PJ, Fisher SJ, Haussler D, Jones SJ, Li W, Marra MA, McManus MT, Sunyaev S, Thomson JA, Tlsty TD, Tsai LH, Wang W, Waterland RA, Zhang MQ, Chadwick LH, Bernstein BE, Costello JF, Ecker JR, Hirst M, Meissner A, Milosavljevic A, Ren B, Stamatoyannopoulos JA, Wang T, Kellis M. Integrative analysis of 111 reference human epigenomes. Nature 2015;518(7539):317-330. |
R835433 (2014) R835433 (Final) |
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Robinson JF, Kapidzic M, Gormley M, Ona K, Dent T, Seifikar H, Hamilton EG, Fisher SJ. Transcriptional dynamics of cultured human villous cytotrophoblasts. Endocrinology 2017;158(6):1581-1594. |
R835433 (2016) R835433 (2017) R835433 (Final) |
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Robinson J, Hamilton E, Lam J, Chen H, Woodruff T. Differences in cytochrome p450 enzyme expression and activity in fetal and adult tissues. PLACENTA 2020;100:35-44. |
R835433 (Final) R834678 (Final) |
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Solomon GM, Morello-Frosch R, Zeise L, Faust JB. Cumulative environmental impacts: science and policy to protect communities. Annual Review of Public Health 2016;37:83-96. |
R835433 (2015) R835433 (2017) R835433 (Final) |
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Stotland NE, Sutton P, Trowbridge J, Atchley DS, Conry J, Trasande L, Gerbert B, Charlesworth A, Woodruff TJ. Counseling patients on preventing prenatal environmental exposures--a mixed-methods study of obstetricians. PLoS ONE 2014;9(6):e98771 (7 pp.). |
R835433 (2014) R835433 (Final) |
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Sutton PM, Giudice LC, Woodruff TJ. Moving from awareness to action on preventing patient exposure to toxic environmental chemicals. American Journal of Obstetrics and Gynecology 2016;214(5):555-558. |
R835433 (2015) R835433 (Final) |
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Sutton, P, Woodruff, TJ, Conry, J, Giudice, LC. Exposure to toxic chemicals:reproductive health professionals speak about the first 1,000 days. San Francisco Medicine 2014;87(9):12-13. |
R835433 (2014) R835433 (Final) |
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Uyghurturk D, Goin D, Martinez-MierEA, Woodruff T, DenBesten P. Maternal and fetal exposures to fluoride during mid-gestation among pregnant women in northern California. ENVIRONMENTAL HEALTH 2020;19(1):38. |
R835433 (Final) |
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Vandenberg LN, Ågerstrand M, Beronius A, Beausoleil C, Bergman A, Bero LA, Bornehag CG, Boyer CS, Cooper GS, Cotgreave I, Gee D, Grandjean P, Guyton KZ, Hass U, Heindel JJ, Jobling S, Kidd KA, Kortenkamp A, Macleod MR, Martin OV, Norinder U, Scheringer M, Thayer KA, Toppari J, Whaley P, Woodruff TJ, Ruden C. A proposed framework for the systematic review and integrated assessment (SYRINA) of endocrine disrupting chemicals. Environmental Health 2016;15(1):74. |
R835433 (2015) R835433 (Final) |
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Vandenberg LN, Gerona RR, Kannan K, Taylor JA, van Breemen RB, Dickenson CA, Liao C, Yuan Y, Newbold RR, Padmanabhan V, Vom Saal FS, Woodruff TJ. Erratum to: A round robin approach to the analysis of bisphenol A (BPA) in human blood samples. Environmental Health 2016;15:43. |
R835433 (2017) R835433 (Final) |
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Varshavsky J, Zota A, Woodruff T. A Novel Method for Calculating Potency-Weighted Cumulative Phthalates Exposure with Implications for Identifying Racial/Ethnic Disparities among Reproductive-Aged Women in NHANES 2001-2012. ENVIRONMENTAL SCIENCE & TECHNOLOGY 2016;5(19):10616-10624. |
R835433 (Final) |
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Varshavsky J, Morello-Frosch R, Woodruff T, Zota A. Dietary sources of cumulative phthalates exposure among the general population in NHANES 2005-2014. ENVIRONMENT INTERNATIONAL 2018;115:417-429. |
R835433 (Final) |
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Varshavsky J, Morello-Frosch R, Harwani S, Snider M, Petropoulou S, Park J, Petras M, Reynolda P, Nguyen T, Quach T. A Pilot Biomonitoring Study of Cumulative Phthalates Exposure among Vietnamese American Nail Salon Workers. INTERNATIONAL JOURNAL OF ENVIRONMENTAL RESEARCH AND PUBLIC HEALTH 2020;17(1). |
R835433 (Final) |
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Varshavsky J, Smith A, Wang A, Hom E, Izano M, Huang H, Padula A, Woodruff T. Heightened susceptibility:A review of how pregnancy and chemical exposures influence maternal health. Reproductive Toxicology 2020;92(SI):14-56. |
R835433 (Final) R835643 (Final) |
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Vesterinen HM, Johnson PI, Koustas E, Lam J, Sutton P, Woodruff TJ. In support of EHP's proposal to adopt the ARRIVE guidelines. Environmental Health Perspectives 2013;121(11‐12):A325. |
R835433 (2013) R835433 (2014) R835433 (Final) |
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Vesterinen HM, Morello-Frosch R, Sen S, Zeise L, Woodruff TJ. Cumulative effects of prenatal-exposure to exogenous chemicals and psychosocial stress on fetal growth: systematic-review of the human and animal evidence. PLoS One 2017;12(7):e0176331 (29 pp.). |
R835433 (2017) R835433 (Final) |
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Wang A, Padula A, Sirota M, Woodruff TJ. Environmental influences on reproductive health: the importance of chemical exposures. Fertility and Sterility 2016;106(4):905-929. |
R835433 (2016) R835433 (2017) R835433 (Final) R835643 (2016) R835643 (2017) |
Exit Exit |
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Wang A, Gerona RR, Schwartz JM, Lin T, Sirota M, Morello-Frosch R, Woodruff TJ. A suspect screening method for characterizing multiple chemical exposures among a demographically diverse population of pregnant women in San Francisco. Environmental Health Perspectives 2018;126(7):077009 (13 pp.). |
R835433 (2017) R835433 (Final) |
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Woodruff TJ, Sutton P. The Navigation Guide systematic review methodology: a rigorous and transparent method for translating environmental health science into better health outcomes. Environmental Health Perspectives 2014;122(10):1007-1014. |
R835433 (2014) R835433 (Final) |
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Zota AR, Linderholm L, Park JS, Petreas M, Guo T, Privalsky ML, Zoeller RT, Woodruff TJ. Temporal comparison of PBDEs, OH-PBDEs, PCBs, and OH-PCBs in the serum of second trimester pregnant women recruited from San Francisco General Hospital, California. Environmental Science & Technology 2013;47(20):11776-11784. |
R835433 (2017) R835433 (Final) |
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Zota AR, Mitro SD, Robinson JF, Hamilton EG, Park JS, Parry E, Zoeller RT, Woodruff TJ. Polybrominated diphenyl ether (PBDEs) and hydroxylated PBDE metabolites (OH-PBDEs) in maternal and fetal tissues, and associations with fetal cytochrome P450 gene expression. Environment International 2018;112:269-278. |
R835433 (2017) R835433 (Final) |
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Zota A, Mitro S, Robinson J, Hamilton E, Park J, Parry E, Zoeller R, Woodruff J. Polybrominated diphenyl ethers PBDEs and hydroxylated PBDE metabolites OH-PBDEs in maternal and fetal tissues, and associations with fetal cytochrome P450 gene expression. ENVIRONMENT INTERNATIONAL 2018;112:269-278. |
R835433 (Final) |
Exit Exit |
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Morello-Frosch R, Cushing LJ, Jesdale BM, Schwartz JM, Guo W, Guo T, Wang M, Harwani S, Syrago-Petropoulou SSE, Duong W, Park J-S, Petreas M, Gajek R, Alvaran J, She J, Dobraca D, Das R, Woodruff TJ (2016) Environmental Chemicals in an Urban Population of Pregnant Women and their Newborns from San Francisco. Environ Sci and Technol DOI:10.1021/acs.est.6b03492. |
R835433 (2016) |
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Johnson PI, Sutton P, Koustas E, Vesterinen HM, Woodruff TJ. Response to correspondence by Heather Lynch, Julie Goodman and Nancy Beck Re:"Application of the Navigation Guide systematic review methodology to the evidence for developmental and reproductive toxicity of triclosan". Environ Int. 2017 Feb 21. pii:S0160-4120(17)30231-3. doi:10.1016/j.envint.2017.02.007. [Epub ahead of print] PubMed PMID:28236502. |
R835433 (2016) R835433 (Final) |
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Supplemental Keywords:
Endocrine disrupting chemicals, reproductive environmental health, prenatal chemical exposure, exposure research, UCSF, chemical exposure, placenta, perinatal outcomes, maternal and child healthRelevant Websites:
UCSF Program on Reproductive Health and the Environment Exit
Progress and Final Reports:
Original AbstractThe perspectives, information and conclusions conveyed in research project abstracts, progress reports, final reports, journal abstracts and journal publications convey the viewpoints of the principal investigator and may not represent the views and policies of ORD and EPA. Conclusions drawn by the principal investigators have not been reviewed by the Agency.
Project Research Results
- 2017 Progress Report
- 2016 Progress Report
- 2015 Progress Report
- 2014 Progress Report
- 2013 Progress Report
- Original Abstract
48 journal articles for this center