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Article: The Crowded Uterine Horn Mouse Model for Examining Postnatal Metabolic Consequences of Intrauterine Growth Restriction vs. Macrosomia in Siblings.

Taylor, Julia A / Coe, Benjamin L / Shioda, Toshi / Vom Saal, Frederick S

2022 Volume 12, Issue 2

Abstract: Differential placental blood flow and nutrient transport can lead to both intrauterine growth restriction (IUGR) and macrosomia. Both conditions can lead to adult obesity and other conditions clustered as metabolic syndrome. We previously showed that ... ...

Abstract	Differential placental blood flow and nutrient transport can lead to both intrauterine growth restriction (IUGR) and macrosomia. Both conditions can lead to adult obesity and other conditions clustered as metabolic syndrome. We previously showed that pregnant hemi-ovariectomized mice have a crowded uterine horn, resulting in siblings whose birth weights differ by over 100% due to differential blood flow based on uterine position. We used this crowded uterus model to compare IUGR and macrosomic male mice and also identified IUGR males with rapid (IUGR-R) and low (IUGR-L) postweaning weight gain. At week 12 IUGR-R males were heavier than IUGR-L males and did not differ from macrosomic males. Rapid growth in IUGR-R males led to glucose intolerance compared to IUGR-L males and down-regulation of adipocyte signaling pathways for fat digestion and absorption and type II diabetes. Macrosomia led to increased fat mass and altered adipocyte size distribution compared to IUGR males, and down-regulation of signaling pathways for carbohydrate and fat digestion and absorption relative to IUGR-R. Clustering analysis of gonadal fat transcriptomes indicated more similarities than differences between IUGR-R and macrosomic males compared to IUGR-L males. Our findings suggest two pathways to adult metabolic disease: macrosomia and IUGR with rapid postweaning growth rate.
Language	English
Publishing date	2022-01-22
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2662251-8
ISSN	2218-1989
ISSN	2218-1989
DOI	10.3390/metabo12020102
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Article ; Online: Interactive Effects of Perinatal BPA or DES and Adult Testosterone and Estradiol Exposure on Adult Urethral Obstruction and Bladder, Kidney, and Prostate Pathology in Male Mice.

Taylor, Julia A / Jones, Maren Bell / Besch-Williford, Cynthia L / Berendzen, Ashley F / Ricke, William A / S Vom Saal, Frederick

International journal of molecular sciences

2020 Volume 21, Issue 11

Abstract: Obstructive voiding disorder (OVD) occurs during aging in men and is often, but not always, associated with increased prostate size, due to benign prostatic hyperplasia (BPH), prostatitis, or prostate cancer. Estrogens are known to impact the development ...

Abstract	Obstructive voiding disorder (OVD) occurs during aging in men and is often, but not always, associated with increased prostate size, due to benign prostatic hyperplasia (BPH), prostatitis, or prostate cancer. Estrogens are known to impact the development of both OVD and prostate diseases, either during early urogenital tract development in fetal-neonatal life or later in adulthood. To examine the potential interaction between developmental and adult estrogen exposure on the adult urogenital tract, male CD-1 mice were perinatally exposed to bisphenol A (BPA), diethylstilbestrol (DES) as a positive control, or vehicle negative control, and in adulthood were treated for 4 months with Silastic capsules containing testosterone and estradiol (T+E2) or empty capsules. Animals exposed to BPA or DES during perinatal development were more likely than negative controls to have urine flow/kidney problems and enlarged bladders, as well as enlarged prostates. OVD in adult T+E2-treated perinatal BPA and DES animals was associated with dorsal prostate hyperplasia and prostatitis. The results demonstrate a relationship between elevated exogenous estrogen levels during urogenital system development and elevated estradiol in adulthood and OVD in male mice. These findings support the two-hit hypothesis for the development of OVD and prostate diseases.
MeSH term(s)	Animals ; Benzhydryl Compounds/toxicity ; Biological Assay ; Diethylstilbestrol/toxicity ; Estradiol/pharmacology ; Female ; Hydronephrosis ; Kidney/pathology ; Male ; Mice ; Organ Size ; Phenols/toxicity ; Pregnancy ; Pregnancy, Animal ; Prenatal Exposure Delayed Effects ; Prostate/pathology ; Prostatic Hyperplasia/pathology ; Prostatitis/pathology ; Testosterone/pharmacology ; Urethral Obstruction/physiopathology ; Urinary Bladder/pathology
Chemical Substances	Benzhydryl Compounds ; Phenols ; Testosterone (3XMK78S47O) ; Estradiol (4TI98Z838E) ; Diethylstilbestrol (731DCA35BT) ; bisphenol A (MLT3645I99)
Language	English
Publishing date	2020-05-30
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2019364-6
ISSN	1422-0067 ; 1422-0067 ; 1661-6596
ISSN (online)	1422-0067
ISSN	1422-0067 ; 1661-6596
DOI	10.3390/ijms21113902
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Article ; Online: Estrogen receptor 1 expression and methylation of

Bhandari, Ramji K / Taylor, Julia A / Sommerfeld-Sager, Jennifer / Tillitt, Donald E / Ricke, William A / Vom Saal, Frederick S

Environmental epigenetics

2019 Volume 5, Issue 3, Page(s) dvz012

Abstract: Fetal/neonatal environmental estrogen exposures alter developmental programing of the prostate gland causing onset of diseases later in life. We have previously ... ...

Abstract	Fetal/neonatal environmental estrogen exposures alter developmental programing of the prostate gland causing onset of diseases later in life. We have previously shown
Language	English
Publishing date	2019-08-22
Publishing country	England
Document type	Journal Article
ZDB-ID	2831217-X
ISSN	2058-5888 ; 2058-5888
ISSN (online)	2058-5888
ISSN	2058-5888
DOI	10.1093/eep/dvz012
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Article ; Online: Experimental BPA Exposure and Glucose-Stimulated Insulin Response in Adult Men and Women.

Stahlhut, Richard W / Myers, John Peterson / Taylor, Julia A / Nadal, Angel / Dyer, Jonathan A / Vom Saal, Frederick S

Journal of the Endocrine Society

2018 Volume 2, Issue 10, Page(s) 1173–1187

Abstract: Context: Human cross-sectional and animal studies have shown an association of the chemical bisphenol A (BPA) with insulin resistance, type 2 diabetes, and other metabolic diseases, but no human experimental study has investigated whether BPA alters ... ...

Abstract	Context: Human cross-sectional and animal studies have shown an association of the chemical bisphenol A (BPA) with insulin resistance, type 2 diabetes, and other metabolic diseases, but no human experimental study has investigated whether BPA alters insulin/C-peptide secretion. Design: Men and postmenopausal women (without diabetes) were orally administered either the vehicle or a BPA dose of 50 µg/kg body weight, which has been predicted by US regulators (Food and Drug Administration, Environmental Protection Agency) to be the maximum, safe daily oral BPA dose over the lifetime. Insulin response was assessed in two cross-over experiments using an oral glucose tolerance test (OGTT; experiment 1) and a hyperglycemic (HG) clamp (experiment 2). Main outcomes were the percentage change of BPA session measures relative to those of the control session. Results: Serum bioactive BPA after experimental exposure was at levels detected in human biomonitoring studies. In the OGTT, a strong positive correlation was found between hemoglobin A1c(HbA1c) and the percentage change in the insulinogenic index (Spearman = 0.92), an indicator of early-phase insulin response, and the equivalent C-peptide index (Pearson = 0.97). In the HG clamp study, focusing on the later-phase insulin response to a stable level of glucose, several measures of insulin and C-peptide appeared suppressed during the BPA session relative to the control session; the change in insulin maximum concentration (Cmax) was negatively correlated with HbA1c and the Cmax of bioactive serum BPA. Conclusions: This exploratory study suggests that BPA exposure to a dose considered safe by US regulators may alter glucose-stimulated insulin response in humans.
Language	English
Publishing date	2018-09-12
Publishing country	United States
Document type	Journal Article
ISSN	2472-1972
ISSN (online)	2472-1972
DOI	10.1210/js.2018-00151
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Article ; Online: Reduced body weight at weaning followed by increased post-weaning growth rate interacts with part-per-trillion fetal serum concentrations of bisphenol A (BPA) to impair glucose tolerance in male mice.

Taylor, Julia A / Sommerfeld-Sager, Jennifer M / Meng, Chun-Xia / Nagel, Susan C / Shioda, Toshi / Vom Saal, Frederick S

PloS one

2018 Volume 13, Issue 12, Page(s) e0208846

Abstract: There is evidence from longitudinal studies that being light at birth and weaning is associated with subsequent rapid weight gain in infants. This is referred to as "centile crossing", which can lead to increased risk of lifetime obesity, glucose ... ...

Abstract	There is evidence from longitudinal studies that being light at birth and weaning is associated with subsequent rapid weight gain in infants. This is referred to as "centile crossing", which can lead to increased risk of lifetime obesity, glucose dysregulation and type 2 diabetes. Here, pregnant CD-1 mice were hemi-ovariectomized so that the entire litter was contained in one uterine horn to increase variability in fetal growth rate. Pregnant females were implanted on gestation day (GD) 9 with a Silastic capsule containing 6, 60 or 600 μg bisphenol A (BPA). On GD 18 the mean fetal serum unconjugated BPA concentrations were 17, 177 and 1858 pg/ml, respectively. Capsules were not removed, to avoid maternal stress, and were predicted to release BPA for at least 3 weeks. Body weight at weaning was strongly negatively correlated with post-weaning weight gain in both control and BPA-treated male mice, consistent with human data; female offspring were excluded, avoiding complications associated with postpubertal estrogens. Within each treatment group, male offspring were sorted into tertiles based on relative weight gain during the two weeks after weaning, designated as having Rapid (R), Medium (M) or Slow (S) growth rate. BPA exposure was associated with altered growth rate between weaning and postnatal week 12 (young adulthood), when a low-dose (20 mg/kg, i.p.) glucose tolerance test (GTT) was performed. We found altered glucose regulation in response to all doses of BPA. However, glucose tolerance was only significantly impaired (blood glucose levels were elevated) compared to controls in males in the rapid post-weaning growth group exposed perinatally to BPA. We conclude that male mice that are light at weaning, but then experience rapid catch-up growth immediately after weaning, represent a sensitive sub-population that is vulnerable to the metabolic disrupting effects of very low pg/ml fetal serum concentrations of BPA.
MeSH term(s)	Animals ; Benzhydryl Compounds/blood ; Benzhydryl Compounds/pharmacology ; Body Weight/drug effects ; Female ; Glucose Intolerance/blood ; Glucose Tolerance Test ; Male ; Mice ; Phenols/blood ; Phenols/pharmacology ; Pregnancy ; Prenatal Exposure Delayed Effects/blood ; Weaning ; Weight Gain/drug effects
Chemical Substances	Benzhydryl Compounds ; Phenols ; bisphenol A (MLT3645I99)
Language	English
Publishing date	2018-12-17
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ISSN	1932-6203
ISSN (online)	1932-6203
DOI	10.1371/journal.pone.0208846
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Article ; Online: Endocrine disruptor bisphenol A is implicated in urinary voiding dysfunction in male mice.

Nicholson, Tristan M / Nguyen, Jalissa L / Leverson, Glen E / Taylor, Julia A / Vom Saal, Frederick S / Wood, Ronald W / Ricke, William A

American journal of physiology. Renal physiology

2018 Volume 315, Issue 5, Page(s) F1208–F1216

Abstract: Estrogens, acting synergistically with androgens, are known from animal experiments to be important in lower urinary tract symptoms (LUTS) and benign prostate enlargement. Human exposure to environmental estrogens occurs throughout the life span, but the ...

Abstract	Estrogens, acting synergistically with androgens, are known from animal experiments to be important in lower urinary tract symptoms (LUTS) and benign prostate enlargement. Human exposure to environmental estrogens occurs throughout the life span, but the urologic health risks in men are largely unknown. Bisphenol A (BPA) is an endocrine disruptor implicated in male urogenital malformations. Given the role of estrogens in male LUTS, we studied the effects of BPA administered in combination with testosterone (T) on the urinary voiding behavior of adult male mice. Adult male mice underwent subcutaneous implantation with slow-release pellets of 25 mg BPA or 2.5 mg estradiol-17β (E
MeSH term(s)	Animals ; Benzhydryl Compounds/administration & dosage ; Benzhydryl Compounds/toxicity ; Drug Implants ; Endocrine Disruptors/administration & dosage ; Endocrine Disruptors/toxicity ; Estradiol/administration & dosage ; Estradiol/toxicity ; Lower Urinary Tract Symptoms/chemically induced ; Lower Urinary Tract Symptoms/pathology ; Lower Urinary Tract Symptoms/physiopathology ; Male ; Mice, Inbred C57BL ; Organ Size ; Phenols/administration & dosage ; Phenols/toxicity ; Risk Assessment ; Testosterone/administration & dosage ; Testosterone/toxicity ; Time Factors ; Urinary Bladder/drug effects ; Urinary Bladder/pathology ; Urinary Bladder/physiopathology ; Urination Disorders/chemically induced ; Urination Disorders/pathology ; Urination Disorders/physiopathology ; Urodynamics/drug effects
Chemical Substances	Benzhydryl Compounds ; Drug Implants ; Endocrine Disruptors ; Phenols ; Testosterone (3XMK78S47O) ; Estradiol (4TI98Z838E) ; bisphenol A (MLT3645I99)
Language	English
Publishing date	2018-07-18
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	603837-2
ISSN	1522-1466 ; 0363-6127
ISSN (online)	1522-1466
ISSN	0363-6127
DOI	10.1152/ajprenal.00582.2017
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Article ; Online: Prenatal Exposure to Bisphenol A Disrupts Naturally Occurring Bimodal DNA Methylation at Proximal Promoter of fggy, an Obesity-Relevant Gene Encoding a Carbohydrate Kinase, in Gonadal White Adipose Tissues of CD-1 Mice.

Taylor, Julia A / Shioda, Keiko / Mitsunaga, Shino / Yawata, Shiomi / Angle, Brittany M / Nagel, Susan C / Vom Saal, Frederick S / Shioda, Toshi

Endocrinology

2017 Volume 159, Issue 2, Page(s) 779–794

Abstract: Exposure of mammalian fetuses to endocrine disruptors can increase the risk of adult-onset diseases. We previously showed that exposure of mouse fetuses to bisphenol A (BPA) caused adult-onset obesity. To examine roles of epigenetic changes in this ... ...

Abstract	Exposure of mammalian fetuses to endocrine disruptors can increase the risk of adult-onset diseases. We previously showed that exposure of mouse fetuses to bisphenol A (BPA) caused adult-onset obesity. To examine roles of epigenetic changes in this delayed toxicity, we determined the effects of fetal mouse exposure to BPA on genome-wide DNA methylation and messenger RNA (mRNA) expression in gonadal white adipose tissues (WATs) by deep sequencing, bisulfite pyrosequencing, and real-time quantitative polymerase chain reaction. Pregnant CD-1 mice (F0) were dosed daily with 0, 5, or 500 μg/kg/d BPA during gestational days 9 to 18, and the weaned F1 animals were fed ad libitum with standard chow until they were euthanized at 19 weeks old. In the vehicle-exposed F1 animals, fggy promoter showed a clear bimodal pattern of very strong (55% to 95%) or very weak (5% to 30%) DNA methylation occurring at nearly equal incidence with no intermediate strength. Promoter hypermethylation completely suppressed mRNA expression. BPA exposure eliminated this naturally occurring dichotomy, shifting fggy promoter toward the hypomethylation state to release transcriptional suppression. The strength of Fggy mRNA expression significantly correlated with increased whole body weight and gonadal fat weight of males but not females. Bioinformatics studies showed that expression of Fggy mRNA is stronger in mouse WATs than in brown adipose tissues and enhanced in gonadal fat by diet-induced obesity. These observations suggest that prenatal exposure to BPA may disrupt the physiological bimodal nature of epigenetic regulation of fggy in mouse WATs, possibly contributing to the adult-onset obesity phenotype.
MeSH term(s)	Adipose Tissue, White/drug effects ; Adipose Tissue, White/metabolism ; Animals ; Benzhydryl Compounds/adverse effects ; Body Weight/drug effects ; Carbohydrate Metabolism ; DNA Methylation/drug effects ; Endocrine Disruptors/adverse effects ; Epigenesis, Genetic/drug effects ; Female ; Humans ; Male ; Mice ; Obesity/enzymology ; Obesity/etiology ; Obesity/genetics ; Obesity/metabolism ; Phenols/adverse effects ; Phosphotransferases/genetics ; Phosphotransferases/metabolism ; Pregnancy ; Prenatal Exposure Delayed Effects/enzymology ; Prenatal Exposure Delayed Effects/etiology ; Prenatal Exposure Delayed Effects/genetics ; Prenatal Exposure Delayed Effects/metabolism ; Promoter Regions, Genetic/drug effects
Chemical Substances	Benzhydryl Compounds ; Endocrine Disruptors ; Phenols ; Phosphotransferases (EC 2.7.-) ; Fggy protein, mouse (EC 2.7.1.-) ; bisphenol A (MLT3645I99)
Language	English
Publishing date	2017-12-19
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	427856-2
ISSN	1945-7170 ; 0013-7227
ISSN (online)	1945-7170
ISSN	0013-7227
DOI	10.1210/en.2017-00711
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Article ; Online: Fetal bisphenol A and ethinylestradiol exposure alters male rat urogenital tract morphology at birth: Confirmation of prior low-dose findings in CLARITY-BPA.

Uchtmann, Kristen S / Taylor, Julia A / Timms, Barry G / Stahlhut, Richard W / Ricke, Emily A / Ellersieck, Mark R / Vom Saal, Frederick S / Ricke, William A

Reproductive toxicology (Elmsford, N.Y.)

2019 Volume 91, Page(s) 131–141

Abstract: Bisphenol A (BPA) is a contaminant in virtually all Americans. To examine BPA's adverse effects, the FDA-NCTR, NIEHS, and 14 groups of academic scientists formed a consortium: CLARITY-BPA. The purpose of our study was to investigate the effects of a wide ...

Abstract	Bisphenol A (BPA) is a contaminant in virtually all Americans. To examine BPA's adverse effects, the FDA-NCTR, NIEHS, and 14 groups of academic scientists formed a consortium: CLARITY-BPA. The purpose of our study was to investigate the effects of a wide range of doses of BPA on fetal development of the NCTR CD-SD male rat urogenital sinus (UGS). Pregnant rats were administered BPA or positive control ethinylestradiol (EE2) daily, via oral gavage, from gestational day 6 through parturition. Tissues were collected on postnatal day 1 and the UGS was analyzed using computer-assisted 3-D reconstruction. Importantly, only low doses of BPA, as well as EE2, significantly changed birth weight and UGS morphology, including an increased size of the colliculus and decreased size of the urethra, consistent with prior reported BPA and EE2 effects. Our findings provide further evidence that BPA mediates nonmonotonic developmental effects on the fetal urogenital sinus.
MeSH term(s)	Animals ; Benzhydryl Compounds/toxicity ; Endocrine Disruptors/toxicity ; Estrogens/toxicity ; Ethinyl Estradiol/toxicity ; Female ; Fetal Development/drug effects ; Fetus ; Humans ; Male ; Maternal-Fetal Exchange ; Phenols/toxicity ; Pregnancy ; Rats, Sprague-Dawley ; Urogenital Abnormalities/chemically induced
Chemical Substances	Benzhydryl Compounds ; Endocrine Disruptors ; Estrogens ; Phenols ; Ethinyl Estradiol (423D2T571U) ; bisphenol A (MLT3645I99)
Language	English
Publishing date	2019-11-19
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	639342-1
ISSN	1873-1708 ; 0890-6238
ISSN (online)	1873-1708
ISSN	0890-6238
DOI	10.1016/j.reprotox.2019.11.007
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Article ; Online: The Conflict between Regulatory Agencies over the 20,000-Fold Lowering of the Tolerable Daily Intake (TDI) for Bisphenol A (BPA) by the European Food Safety Authority (EFSA).

Vom Saal, Frederick S / Antoniou, Michael / Belcher, Scott M / Bergman, Ake / Bhandari, Ramji K / Birnbaum, Linda S / Cohen, Aly / Collins, Terrence J / Demeneix, Barbara / Fine, Anne Marie / Flaws, Jodi A / Gayrard, Veronique / Goodson, William H / Gore, Andrea C / Heindel, Jerrold J / Hunt, Patricia A / Iguchi, Taisen / Kassotis, Christopher D / Kortenkamp, Andreas /

Environmental health perspectives

2024 Volume 132, Issue 4, Page(s) 45001

Abstract: Background: The European Food Safety Authority (EFSA) recommended lowering their estimated tolerable daily intake (TDI) for bisphenol A (BPA) 20,000-fold to : Objectives: We identify the flaws in the assumptions that the German BfR, as well as the ... ...

Abstract	Background: The European Food Safety Authority (EFSA) recommended lowering their estimated tolerable daily intake (TDI) for bisphenol A (BPA) 20,000-fold to Objectives: We identify the flaws in the assumptions that the German BfR, as well as the FDA, have used to justify maintaining the TDI for BPA at levels above what a vast amount of academic research shows to cause harm. We argue that regulatory agencies need to incorporate 21st century science into chemical hazard identifications using the CLARITY-BPA (Consortium Linking Academic and Regulatory Insights on BPA Toxicity) nonguideline academic studies in a collaborative government-academic program model. Discussion: We strongly endorse EFSA's revised TDI for BPA and support the European Commission's (EC) apparent acceptance of this updated BPA risk assessment. We discuss challenges to current chemical risk assessment assumptions about EDCs that need to be addressed by regulatory agencies to, in our opinion, become truly protective of public health. Addressing these challenges will hopefully result in BPA, and eventually other structurally similar bisphenols (called regrettable substitutions) for which there are known adverse effects, being eliminated from all food-related and many other uses in the EU and elsewhere. https://doi.org/10.1289/EHP13812.
MeSH term(s)	Humans ; Benzhydryl Compounds ; Food Safety ; No-Observed-Adverse-Effect Level ; Phenols ; Systematic Reviews as Topic
Chemical Substances	Benzhydryl Compounds ; bisphenol A (MLT3645I99) ; Phenols
Language	English
Publishing date	2024-04-09
Publishing country	United States
Document type	Journal Article
ZDB-ID	195189-0
ISSN	1552-9924 ; 0091-6765 ; 1078-0475
ISSN (online)	1552-9924
ISSN	0091-6765 ; 1078-0475
DOI	10.1289/EHP13812
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Article ; Online: Comment on "Optimal Exposure Biomarkers for Nonpersistent Chemicals in Environmental Epidemiology".

Stahlhut, Richard W / van Breemen, Richard B / Gerona, Roy R / Taylor, Julia A / Welshons, Wade V / vom Saal, Frederick S

Environmental health perspectives

2016 Volume 124, Issue 4, Page(s) A66

MeSH term(s)	Biomarkers/blood ; Biomarkers/urine ; Environmental Exposure/analysis ; Environmental Monitoring/methods ; Environmental Pollutants/blood ; Environmental Pollutants/urine ; Humans
Chemical Substances	Biomarkers ; Environmental Pollutants
Language	English
Publishing date	2016-04
Publishing country	United States
Document type	Comment ; Letter
ZDB-ID	195189-0
ISSN	1552-9924 ; 0091-6765 ; 1078-0475
ISSN (online)	1552-9924
ISSN	0091-6765 ; 1078-0475
DOI	10.1289/ehp.1511057
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