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Article ; Online: Per‐ and polyfluoroalkyl substances activate UPR pathway, induce steatosis and fibrosis in liver cells

Qi, Qi / Niture, Suryakant / Gadi, Sashi / Arthur, Elena / Moore, John / Levine, Keith E. / Kumar, Deepak

Environmental Toxicology. 2023 Jan., v. 38, no. 1 p.225-242

2023

Abstract: Per‐ and polyfluoroalkyl substances (PFAS), which include perfluorooctanoic acid (PFOA), heptafluorobutyric acid (HFBA), and perfluorotetradecanoic acid (PFTA), are commonly occurring organic pollutants. Exposure to PFAS affects the immune system, ... ...

Abstract	Per‐ and polyfluoroalkyl substances (PFAS), which include perfluorooctanoic acid (PFOA), heptafluorobutyric acid (HFBA), and perfluorotetradecanoic acid (PFTA), are commonly occurring organic pollutants. Exposure to PFAS affects the immune system, thyroid and kidney function, lipid metabolism, and insulin signaling and is also involved in the development of fatty liver disease and cancer. The molecular mechanisms by which PFAS cause fatty liver disease are not understood in detail. In the current study, we investigated the effect of low physiologically relevant concentrations of PFOA, HFBA, and PFTA on cell survival, steatosis, and fibrogenic signaling in liver cell models. Exposure of PFOA and HFBA (10 to 1000 nM) specifically promoted cell survival in HepaRG and HepG2 cells. PFAS increased the expression of TNFα and IL6 inflammatory markers, increased endogenous reactive oxygen species (ROS) production, and activated unfolded protein response (UPR). Furthermore, PFAS enhanced cell steatosis and fibrosis in HepaRG and HepG2 cells which were accompanied by upregulation of steatosis (SCD1, ACC, SRBP1, and FASN), and fibrosis (TIMP2, p21, TGFβ) biomarkers expression, respectively. RNA‐seq data suggested that chronic exposures to PFOA modulated the expression of fatty acid/lipid metabolic genes that are involved in the development of NFALD and fatty liver disease. Collectively our data suggest that acute/chronic physiologically relevant concentrations of PFAS enhance liver cell steatosis and fibrosis by the activation of the UPR pathway and by modulation of NFALD‐related gene expression.
Keywords	biomarkers ; cell viability ; ecotoxicology ; fatty acids ; fatty liver ; fibrosis ; gene expression ; hepatocytes ; immune system ; insulin ; interleukin-6 ; lipid metabolism ; liver ; perfluorooctanoic acid ; reactive oxygen species ; renal function ; sequence analysis ; unfolded protein response
Language	English
Dates of publication	2023-01
Size	p. 225-242.
Publishing place	John Wiley & Sons, Inc.
Document type	Article ; Online
Note	JOURNAL ARTICLE
ZDB-ID	1463449-1
ISSN	1522-7278 ; 1520-4081
ISSN (online)	1522-7278
ISSN	1520-4081
DOI	10.1002/tox.23680
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Article ; Online: Cyanotoxins Increase Cytotoxicity and Promote Nonalcoholic Fatty Liver Disease Progression by Enhancing Cell Steatosis.

Niture, Suryakant / Gadi, Sashi / Qi, Qi / Rios-Colon, Leslimar / Khatiwada, Sabin / Vandana / Fernando, Reshan A / Levine, Keith E / Kumar, Deepak

Toxins

2023 Volume 15, Issue 7

Abstract: Freshwater prokaryotic cyanobacteria within harmful algal blooms produce cyanotoxins which are considered major pollutants in the aquatic system. Direct exposure to cyanotoxins through inhalation, skin contact, or ingestion of contaminated drinking water ...

Abstract	Freshwater prokaryotic cyanobacteria within harmful algal blooms produce cyanotoxins which are considered major pollutants in the aquatic system. Direct exposure to cyanotoxins through inhalation, skin contact, or ingestion of contaminated drinking water can target the liver and may cause hepatotoxicity. In the current study, we investigated the effect of low concentrations of cyanotoxins on cytotoxicity, inflammation, modulation of unfolded protein response (UPR), steatosis, and fibrosis signaling in human hepatocytes and liver cell models. Exposure to low concentrations of microcystin-LR (MC-LR), microcystin-RR (MC-RR), nodularin (NOD), and cylindrospermopsin (CYN) in human bipotent progenitor cell line HepaRG and hepatocellular carcinoma (HCC) cell lines HepG2 and SK-Hep1 resulted in increased cell toxicity. MC-LR, NOD, and CYN differentially regulated inflammatory signaling, activated UPR signaling and lipogenic gene expression, and induced cellular steatosis and fibrotic signaling in HCC cells. MC-LR, NOD, and CYN also regulated AKT/mTOR signaling and inhibited autophagy. Chronic exposure to MC-LR, NOD, and CYN upregulated the expression of lipogenic and fibrosis biomarkers. Moreover, RNA sequencing (RNA seq) data suggested that exposure of human hepatocytes, HepaRG, and HCC HepG2 cells to MC-LR and CYN modulated expression levels of several genes that regulate non-alcoholic fatty liver disease (NAFLD). Our data suggest that low concentrations of cyanotoxins can cause hepatotoxicity and cell steatosis and promote NAFLD progression.
MeSH term(s)	Humans ; Non-alcoholic Fatty Liver Disease/chemically induced ; Bacterial Toxins/toxicity ; Carcinoma, Hepatocellular ; Liver Neoplasms ; Cyanobacteria Toxins ; Microcystins/toxicity ; Fibrosis ; Chemical and Drug Induced Liver Injury
Chemical Substances	Bacterial Toxins ; Cyanobacteria Toxins ; Microcystins
Language	English
Publishing date	2023-06-25
Publishing country	Switzerland
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	2518395-3
ISSN	2072-6651 ; 2072-6651
ISSN (online)	2072-6651
ISSN	2072-6651
DOI	10.3390/toxins15070411
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Article ; Online: Residential Proximity to Metal-Containing Superfund Sites and Their Potential as a Source of Disparities in Metal Exposure among U.S. Women.

Trottier, Brittany A / Niehoff, Nicole M / Keil, Alexander P / Jones, Rena R / Levine, Keith E / MacNell, Nathaniel S / White, Alexandra J

Environmental health perspectives

2023 Volume 131, Issue 3, Page(s) 37701

MeSH term(s)	Humans ; Female ; Hazardous Substances ; Environmental Exposure ; Refuse Disposal
Chemical Substances	Hazardous Substances
Language	English
Publishing date	2023-03-14
Publishing country	United States
Document type	Research Support, N.I.H., Intramural ; Letter
ZDB-ID	195189-0
ISSN	1552-9924 ; 0091-6765 ; 1078-0475
ISSN (online)	1552-9924
ISSN	0091-6765 ; 1078-0475
DOI	10.1289/EHP11045
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Article: A comparative review: Chronic Kidney Disease of unknown etiology (CKDu) research conducted in Latin America versus Asia

Redmon, Jennifer Hoponick / Levine, Keith E / Lebov, Jill / Harrington, James / Kondash, A.J

Environmental research. 2021 Jan., v. 192

2021

Abstract: The incidence of chronic kidney disease of unknown or uncertain etiology (CKDu) is recognized as a global non-communicable health crisis. The goal of this work is to compare the types of research studies in Latin America and Asia, two regions with ... ...

Abstract	The incidence of chronic kidney disease of unknown or uncertain etiology (CKDu) is recognized as a global non-communicable health crisis. The goal of this work is to compare the types of research studies in Latin America and Asia, two regions with increasing CKDu incidence.A comparative literature review was conducted to evaluate the CKDu research design for peer-reviewed articles published from 2015 to 2019. Full texts were reviewed to identify study location, study type, study design, risk factors evaluated, and if applicable, sample type and number.In Asia and Latin America, 82 and 65 articles were identified in total, respectively, with 55 field studies in Asia versus 34 in Latin America. In Asia, research was focused on drinking water (34), heavy metals (20), and agrochemical product usage (19) as potential risk factors. In Latin America, research focused mostly on heat stress/dehydration (36) and agrochemical product usage (18) as potential CKDu risk factors. Biological samples were collected more frequently than environmental samples, especially in Latin America.Research to pinpoint the risk factors associated with CKDu to date is not standardized and typically limited in geographical scope. The emphasis of CKDu research varies by geographic region, with a greater priority placed on water quality and chemical exposure in Asia, versus dehydration and heat stress in Latin America. Using a harmonized approach to CKDu research would yield improved understanding of the risk factors associated with CKDu and how they compare across affected regions.
Keywords	agrochemicals ; etiology ; experimental design ; heat stress ; kidney diseases ; research ; water quality ; Asia ; Latin America
Language	English
Dates of publication	2021-01
Publishing place	Elsevier Inc.
Document type	Article
Note	NAL-AP-2-clean
ZDB-ID	205699-9
ISSN	1096-0953 ; 0013-9351
ISSN (online)	1096-0953
ISSN	0013-9351
DOI	10.1016/j.envres.2020.110270
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Article ; Online: Cadmium modulates steatosis, fibrosis, and oncogenic signaling in liver cancer cells by activating notch and AKT/mTOR pathways

Niture, Suryakant / Gadi, Sashi / Lin, Minghui / Qi, Qi / Niture, Samiksha S. / Moore, John T. / Bodnar, Wanda / Fernando, Reshan A. / Levine, Keith E. / Kumar, Deepak

Environmental Toxicology. 2023 Mar., v. 38, no. 4 p.783-797

2023

Abstract: Cadmium (Cd) is an environmental pollutant that increases hepatotoxicity and the risk of liver diseases. In the current study, we investigated the effect of a physiologically relevant, low concentration of Cd on the regulation of liver cancer cell ... ...

Abstract	Cadmium (Cd) is an environmental pollutant that increases hepatotoxicity and the risk of liver diseases. In the current study, we investigated the effect of a physiologically relevant, low concentration of Cd on the regulation of liver cancer cell proliferation, steatosis, and fibrogenic/oncogenic signaling. Exposure to low concentrations of Cd increased endogenous reactive oxygen species (ROS) production and enhanced cell proliferation in a human bipotent progenitor cell line HepaRG and hepatocellular carcinoma (HCC) cell lines. Acute exposure of Cd increased Jagged‐1 expression and activated Notch signaling in HepaRG and HCC cells HepG2 and SK‐Hep1. Cd activated AKT/mTOR signaling by increasing phosphorylation of AKT‐S473 and mTOR‐S‐4448 residues. Moreover, a low concentration of Cd also promoted cell steatosis and induced fibrogenic signaling in HCC cells. Chronic exposure to low concentrations of Cd‐activated Notch and AKT/mTOR signaling induced the expression of pro‐inflammatory cytokines tumor necrosis factor‐alpha (TNFα) and its downstream target TNF‐α‐Induced Protein 8 (TNFAIP8). RNA‐Seq data revealed that chronic exposure to low concentrations of Cd modulated the expression of several fatty liver disease‐related genes involved in cell steatosis/fibrosis in HepaRG and HepG2 cells. Collectively, our data suggest that low concentrations of Cd modulate steatosis along with fibrogenic and oncogenic signaling in HCC cells by activating Notch and AKT/mTOR pathways.
Keywords	acute exposure ; cadmium ; cell lines ; cell proliferation ; chronic exposure ; ecotoxicology ; fatty liver ; fibrosis ; hepatoma ; hepatotoxicity ; humans ; liver ; neoplasm cells ; phosphorylation ; pollutants ; reactive oxygen species ; risk ; sequence analysis ; stem cells ; tumor necrosis factor-alpha
Language	English
Dates of publication	2023-03
Size	p. 783-797.
Publishing place	John Wiley & Sons, Inc.
Document type	Article ; Online
Note	JOURNAL ARTICLE
ZDB-ID	1463449-1
ISSN	1522-7278 ; 1520-4081
ISSN (online)	1522-7278
ISSN	1520-4081
DOI	10.1002/tox.23731
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Article ; Online: Toenail and serum levels as biomarkers of iron status in pre- and postmenopausal women: correlations and stability over eight-year follow-up.

Von Holle, Ann / O'Brien, Katie M / Sandler, Dale P / Janicek, Robert / Karagas, Margaret R / White, Alexandra J / Niehoff, Nicole M / Levine, Keith E / Jackson, Brian P / Weinberg, Clarice R

Scientific reports

2024 Volume 14, Issue 1, Page(s) 1682

Abstract: Iron status is often assessed in epidemiologic studies, and toenails offer a convenient alternative to serum because of ease of collection, transport, and storage, and the potential to reflect a longer exposure window. Very few studies have examined the ... ...

Abstract	Iron status is often assessed in epidemiologic studies, and toenails offer a convenient alternative to serum because of ease of collection, transport, and storage, and the potential to reflect a longer exposure window. Very few studies have examined the correlation between serum and toenail levels for trace metals. Our aim was to compare iron measures using serum and toenails on both a cross-sectional and longitudinal basis. Using a subset of the US-wide prospective Sister Study cohort, we compared toenail iron measures to serum concentrations for iron, ferritin and percent transferrin saturation. Among 146 women who donated both blood and toenails at baseline, a subsample (59%, n = 86) provided specimens about 8 years later. Cross-sectional analyses included nonparametric Spearman's rank correlations between toenail and serum biomarker levels. We assessed within-woman maintenance of rank across time for the toenail and serum measures and fit mixed effects models to measure change across time in relation to change in menopause status. Spearman correlations at baseline (follow-up) were 0.08 (0.09) for serum iron, 0.08 (0.07) for transferrin saturation, and - 0.09 (- 0.17) for ferritin. The within-woman Spearman correlation for toenail iron between the two time points was higher (0.47, 95% CI 0.30, 0.64) than for serum iron (0.30, 95% CI 0.09, 0.51) and transferrin saturation (0.34, 95% CI 0.15, 0.54), but lower than that for ferritin (0.58, 95% CI 0.43, 0.73). Serum ferritin increased over time while nail iron decreased over time for women who experienced menopause during the 8-years interval. Based on cross-sectional and repeated assessments, our evidence does not support an association between serum biomarkers and toenail iron levels. Toenail iron concentrations did appear to be moderately stable over time but cannot be taken as a proxy for serum iron biomarkers and they may reflect physiologically distinct fates for iron.
MeSH term(s)	Humans ; Female ; Iron/metabolism ; Nails/metabolism ; Follow-Up Studies ; Prospective Studies ; Postmenopause ; Cross-Sectional Studies ; Ferritins ; Biomarkers ; Transferrins ; Transferrin
Chemical Substances	Iron (E1UOL152H7) ; Ferritins (9007-73-2) ; Biomarkers ; Transferrins ; Transferrin
Language	English
Publishing date	2024-01-19
Publishing country	England
Document type	Journal Article
ZDB-ID	2615211-3
ISSN	2045-2322 ; 2045-2322
ISSN (online)	2045-2322
ISSN	2045-2322
DOI	10.1038/s41598-023-50506-5
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Article ; Online: Seasonal patterns in trace elements assessed in toenails.

Wojcik, Kaitlyn M / Holle, Ann Von / O'Brien, Katie M / White, Alexandra J / Karagas, Margaret R / Levine, Keith E / Jackson, Brian P / Weinberg, Clarice R

Environmental advances

2024 Volume 15

Abstract: Background: Seasonal patterns in measured exposure biomarkers can cause measurement error in epidemiological studies. There is little research about the seasonality of metals and trace elements when assessed in toenail samples. Adjusting for such ... ...

Abstract	Background: Seasonal patterns in measured exposure biomarkers can cause measurement error in epidemiological studies. There is little research about the seasonality of metals and trace elements when assessed in toenail samples. Adjusting for such patterns in models for estimating associations between long-term exposures and health outcomes can potentially improve precision and reduce bias. Objectives: Assess and describe seasonal patterns in toenail measurements of trace elements. Methods: The Sister Study enrolled women residing in the US, including Puerto Rico, whose sister had been diagnosed with breast cancer. At the time of enrollment, participants removed nail polish and collected their toenail clippings, which were cleaned before analysis. We considered the following elements: iron, vanadium, aluminum, chromium, manganese, cobalt, nickel, copper, zinc, arsenic, selenium, molybdenum, cadmium, tin, antimony, mercury, and lead. For two subsamples of the cohort, we fit trigonometric regression models with toenail element measures as the outcome, using sine and cosine functions of the collection day (transformed to an angle) to capture seasonal patterns. These models can estimate the amplitude and timing of the peaks in measures. We evaluated the evidence for a seasonal effect by comparing for each measured element the trigonometric model to a model that was constant across time. Results: There was a seasonal trend in toenail element concentration for iron, aluminum, vanadium, chromium, manganese, cobalt, arsenic, molybdenum, cadmium, tin, and lead, all of which peaked near mid-August. Seasonal patterns were concordant across two non-overlapping samples of women, analyzed in different labs. Discussion: Given the evidence supporting seasonal patterns for 11 of the 17 elements measured in toenails, correcting for seasonality of toenail levels of those trace elements in models estimating the association between those exposures and health outcomes is important. The basis for higher concentrations in toenails collected during the summer remains unknown.
Language	English
Publishing date	2024-02-02
Publishing country	England
Document type	Journal Article
ISSN	2666-7657
ISSN (online)	2666-7657
DOI	10.1016/j.envadv.2024.100496
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Article: Total sulfur analysis of fine particulate mass on nylon filters by ICP–OES

Dombek, Tracy / Poitras, Eric / Hand, Jenny / Schichtel, Bret / Harrington, James M. / Levine, Keith E.

Journal of environmental quality. 2020 May, v. 49, no. 3

2020

Abstract: Sulfur (S) and sulfate (SO₄²⁻) in fine particulate matter (PM₂.₅) are monitored by the Interagency Monitoring of Protected Visual Environments (IMPROVE) network at remote and rural sites across the United States. Within the IMPROVE network, S is ... ...

Abstract	Sulfur (S) and sulfate (SO₄²⁻) in fine particulate matter (PM₂.₅) are monitored by the Interagency Monitoring of Protected Visual Environments (IMPROVE) network at remote and rural sites across the United States. Within the IMPROVE network, S is determined from X‐ray fluorescence (XRF) spectroscopy from a Teflon filter, and SO₄²⁻ is determined via ion chromatography (IC) from a nylon filter. Differences in S and SO₄²⁻ estimates may indicate the presence of organosulfur (OS) species or biases between sampling and analytical methods. To reduce potential biases, an inductively coupled plasma–optical emission spectroscopy (ICP–OES) method was developed to allow for analysis of SO₄²⁻ and S from a single filter extract. Sulfur (ICP–OES) and SO₄²⁻ (IC) estimates from 2016 IMPROVE filters correlated strongly, suggesting that, on average, ICP–OES accurately estimated S. However, observed differences between slopes suggested the presence of water‐soluble OS species, especially during summer. Organosulfur species are important indicators of secondary organic aerosols formed through reactions of biogenic and anthropogenic pollutants and can be quantified through laboratory techniques such as reverse‐phase liquid chromatography (RPLC) or hydrophilic liquid interaction chromatography (HILIC) coupled to electrospray ionization–high‐resolution tandem mass spectrometry (RPLC/ESI‐HR–MS/MS and HILIC/ESI–HR–MS/MS, respectively), and field techniques using Aerodyne aerosol mass spectrometry (AMS). However, these methods are costly and introduce relatively large uncertainties when scaled for large networks such as IMPROVE. The method described in this report provides an inexpensive complement to XRF, which measures total S (insoluble and water‐soluble S) to estimate water‐soluble S and OS concentrations in PM.
Keywords	X-radiation ; aerosols ; complement ; environmental quality ; fluorescence ; hydrophilicity ; ion exchange chromatography ; liquids ; nylon ; particulates ; polytetrafluoroethylene ; reversed-phase liquid chromatography ; sulfates ; sulfur ; summer ; tandem mass spectrometry ; water solubility
Language	English
Dates of publication	2020-05
Size	p. 762-768.
Publishing place	John Wiley & Sons, Ltd
Document type	Article
Note	JOURNAL ARTICLE
ZDB-ID	120525-0
ISSN	1537-2537 ; 0047-2425
ISSN (online)	1537-2537
ISSN	0047-2425
DOI	10.1002/jeq2.20066
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Article ; Online: Per- and polyfluoroalkyl substances activate UPR pathway, induce steatosis and fibrosis in liver cells.

Qi, Qi / Niture, Suryakant / Gadi, Sashi / Arthur, Elena / Moore, John / Levine, Keith E / Kumar, Deepak

Environmental toxicology

2022 Volume 38, Issue 1, Page(s) 225–242

Abstract: Per- and polyfluoroalkyl substances (PFAS), which include perfluorooctanoic acid (PFOA), heptafluorobutyric acid (HFBA), and perfluorotetradecanoic acid (PFTA), are commonly occurring organic pollutants. Exposure to PFAS affects the immune system, ... ...

Abstract	Per- and polyfluoroalkyl substances (PFAS), which include perfluorooctanoic acid (PFOA), heptafluorobutyric acid (HFBA), and perfluorotetradecanoic acid (PFTA), are commonly occurring organic pollutants. Exposure to PFAS affects the immune system, thyroid and kidney function, lipid metabolism, and insulin signaling and is also involved in the development of fatty liver disease and cancer. The molecular mechanisms by which PFAS cause fatty liver disease are not understood in detail. In the current study, we investigated the effect of low physiologically relevant concentrations of PFOA, HFBA, and PFTA on cell survival, steatosis, and fibrogenic signaling in liver cell models. Exposure of PFOA and HFBA (10 to 1000 nM) specifically promoted cell survival in HepaRG and HepG2 cells. PFAS increased the expression of TNFα and IL6 inflammatory markers, increased endogenous reactive oxygen species (ROS) production, and activated unfolded protein response (UPR). Furthermore, PFAS enhanced cell steatosis and fibrosis in HepaRG and HepG2 cells which were accompanied by upregulation of steatosis (SCD1, ACC, SRBP1, and FASN), and fibrosis (TIMP2, p21, TGFβ) biomarkers expression, respectively. RNA-seq data suggested that chronic exposures to PFOA modulated the expression of fatty acid/lipid metabolic genes that are involved in the development of NFALD and fatty liver disease. Collectively our data suggest that acute/chronic physiologically relevant concentrations of PFAS enhance liver cell steatosis and fibrosis by the activation of the UPR pathway and by modulation of NFALD-related gene expression.
MeSH term(s)	Humans ; Fluorocarbons/toxicity ; Unfolded Protein Response ; Non-alcoholic Fatty Liver Disease ; Environmental Pollutants/toxicity ; Fibrosis ; Alkanesulfonic Acids
Chemical Substances	perfluorotetradecanoic acid ; Fluorocarbons ; perfluorooctanoic acid (947VD76D3L) ; perfluorobutyric acid (375-22-4) ; Environmental Pollutants ; Alkanesulfonic Acids
Language	English
Publishing date	2022-10-17
Publishing country	United States
Document type	Journal Article
ZDB-ID	1463449-1
ISSN	1522-7278 ; 1520-4081
ISSN (online)	1522-7278
ISSN	1520-4081
DOI	10.1002/tox.23680
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Article ; Online: A comparative review: Chronic Kidney Disease of unknown etiology (CKDu) research conducted in Latin America versus Asia.

Redmon, Jennifer Hoponick / Levine, Keith E / Lebov, Jill / Harrington, James / Kondash, A J

Environmental research

2020 Volume 192, Page(s) 110270

Abstract: Introduction: The incidence of chronic kidney disease of unknown or uncertain etiology (CKDu) is recognized as a global non-communicable health crisis. The goal of this work is to compare the types of research studies in Latin America and Asia, two ... ...

Abstract	Introduction: The incidence of chronic kidney disease of unknown or uncertain etiology (CKDu) is recognized as a global non-communicable health crisis. The goal of this work is to compare the types of research studies in Latin America and Asia, two regions with increasing CKDu incidence. Methods: A comparative literature review was conducted to evaluate the CKDu research design for peer-reviewed articles published from 2015 to 2019. Full texts were reviewed to identify study location, study type, study design, risk factors evaluated, and if applicable, sample type and number. Results: In Asia and Latin America, 82 and 65 articles were identified in total, respectively, with 55 field studies in Asia versus 34 in Latin America. In Asia, research was focused on drinking water (34), heavy metals (20), and agrochemical product usage (19) as potential risk factors. In Latin America, research focused mostly on heat stress/dehydration (36) and agrochemical product usage (18) as potential CKDu risk factors. Biological samples were collected more frequently than environmental samples, especially in Latin America. Discussion: Research to pinpoint the risk factors associated with CKDu to date is not standardized and typically limited in geographical scope. The emphasis of CKDu research varies by geographic region, with a greater priority placed on water quality and chemical exposure in Asia, versus dehydration and heat stress in Latin America. Using a harmonized approach to CKDu research would yield improved understanding of the risk factors associated with CKDu and how they compare across affected regions.
MeSH term(s)	Asia/epidemiology ; Drinking Water/analysis ; Humans ; Latin America/epidemiology ; Metals, Heavy ; Renal Insufficiency, Chronic/epidemiology ; Renal Insufficiency, Chronic/etiology ; Sri Lanka
Chemical Substances	Drinking Water ; Metals, Heavy
Language	English
Publishing date	2020-10-07
Publishing country	Netherlands
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	205699-9
ISSN	1096-0953 ; 0013-9351
ISSN (online)	1096-0953
ISSN	0013-9351
DOI	10.1016/j.envres.2020.110270
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