Evidence map›Paper›PMID 30622099›Full record

ArticleCancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology2019

Urinary Biomarkers of Carcinogenic Exposure among Cigarette, Waterpipe, and Smokeless Tobacco Users and Never Users of Tobacco in the Golestan Cohort Study.

Arash Etemadi, Hossein Poustchi, Cindy M Chang, Benjamin C Blount, Antonia M Calafat, Lanqing Wang, Victor R De Jesus, Akram Pourshams, Ramin Shakeri, Meredith S Shiels and 17 more

Abstract readComparative Study
In one paragraph

Article in Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology, 2019. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 36 papers.

0numbers the graph read from it
0cells of the map it votes in
36citing papers in PubMed
–field-weighted citation impact
1 · What the graph read from it

What it found

Each row is one number read from the abstract, on the scale the paper reported it, with its interval. Left of the dashed line favours the treatment, right favours the comparator. Under each row is the sentence it came from. New to these charts? A ten-minute tutorial.

The abstract states no effect estimate the extractor could read, or names no intervention and outcome on the map, so this paper lights no cell and moves no belief. It is still indexed, cited and linked below.

2 · The registry

The trial behind it

Trials whose registry record cites this paper, or whose number appears in the abstract. A trial that started after this paper was published is citing it as background, not reporting it.

Neither the registry nor the abstract names a trial number. If this is a trial report, that itself is worth knowing.

3 · Its place in the literature

Who cites it

36 citing papers in PubMed.

  1. Manipulation of Menthol and Nicotine Content in Cigarettes: Effects on Smoking Behavior and Toxicant Exposure in Women Menthol Smokers.Nicotine & tobacco research : official journal of the Society for Research on Nicotine and Tobacco · 2023
    Trial
  2. Article
  3. Article
  4. Consistency of Biomarkers of Exposure in the Population Assessment of Tobacco and Health Study from Samples Taken 3 to 5 Years Apart.Nicotine & tobacco research : official journal of the Society for Research on Nicotine and Tobacco · 2026
    Article
  5. Article
  6. Associations between Opium Route of Use and Exposure to Polycyclic Aromatic Hydrocarbons as Potential Carcinogenicity Mechanism.Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology · 2025
    Article
  7. Article
  8. Article
  9. High-throughput UPLC-ESI/MSMS method for simultaneous measurement of the urinary metabolites of volatile organic compounds and tobacco alkaloids.Journal of chromatography. B, Analytical technologies in the biomedical and life sciences · 2025
    Article
  10. Toxicity of waterpipe tobacco smoking: the role of flavors, sweeteners, humectants, and charcoal.Toxicological sciences : an official journal of the Society of Toxicology · 2024
    Review
  11. Article
  12. Unveiling an Association between Waterpipe Smoking and Bladder Cancer Risk: A Multicenter Case-Control Study in Iran.Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology · 2024
    Article
  13. Article
  14. Article
  15. Influence of Half-life and Smoking/Nonsmoking Ratio on Biomarker Consistency between Waves 1 and 2 of the Population Assessment of Tobacco and Health Study.Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology · 2024
    Article
  16. Article
  17. Article
  18. Smoke exposure associated with higher urinary benzene biomarker muconic acid (MUCA) in Golestan Cohort Study participants.Biomarkers : biochemical indicators of exposure, response, and susceptibility to chemicals · 2023
    Article
  19. Article
  20. Article
4 · The record

Corrections and comments

PubMed lists nothing against this paper. Absence here is not a guarantee, only a check that was made.

5 · Who and what money

Authors and funding

27 authors.

Arash EtemadiDivision of Cancer Epidemiology and Genetics, National Cancer Institute, NIH, Bethesda, Maryland. arash.etemadi@nih.gov malek@ams.ac.ir.
Hossein PoustchiDigestive Oncology Research Center, Digestive Disease Research Institute, Tehran University of Medical Sciences, Tehran, Iran.
Cindy M ChangCenter for Tobacco Products, Food and Drug Administration, Silver Spring, Maryland.ORCID 0000-0002-2103-8222
Benjamin C BlountNational Center for Environmental Health, Centers for Disease Control and Prevention, Atlanta, Georgia.ORCID 0000-0003-4788-8169
Antonia M CalafatNational Center for Environmental Health, Centers for Disease Control and Prevention, Atlanta, Georgia.
Lanqing WangNational Center for Environmental Health, Centers for Disease Control and Prevention, Atlanta, Georgia.
Victor R De JesusNational Center for Environmental Health, Centers for Disease Control and Prevention, Atlanta, Georgia.
Akram PourshamsDigestive Oncology Research Center, Digestive Disease Research Institute, Tehran University of Medical Sciences, Tehran, Iran.
Ramin ShakeriDigestive Oncology Research Center, Digestive Disease Research Institute, Tehran University of Medical Sciences, Tehran, Iran.
Meredith S ShielsDivision of Cancer Epidemiology and Genetics, National Cancer Institute, NIH, Bethesda, Maryland.
Maki Inoue-ChoiDivision of Cancer Epidemiology and Genetics, National Cancer Institute, NIH, Bethesda, Maryland.
Bridget K AmbroseCenter for Tobacco Products, Food and Drug Administration, Silver Spring, Maryland.ORCID 0000-0001-9263-3056
Carol H ChristensenCenter for Tobacco Products, Food and Drug Administration, Silver Spring, Maryland.
Baoguang WangCenter for Tobacco Products, Food and Drug Administration, Silver Spring, Maryland.
Gwen MurphyDivision of Cancer Epidemiology and Genetics, National Cancer Institute, NIH, Bethesda, Maryland.
Xiaoyun YeNational Center for Environmental Health, Centers for Disease Control and Prevention, Atlanta, Georgia.
Deepak BhandariNational Center for Environmental Health, Centers for Disease Control and Prevention, Atlanta, Georgia.
Jun FengNational Center for Environmental Health, Centers for Disease Control and Prevention, Atlanta, Georgia.
Baoyun XiaNational Center for Environmental Health, Centers for Disease Control and Prevention, Atlanta, Georgia.ORCID 0000-0001-5081-7447
Connie S SosnoffNational Center for Environmental Health, Centers for Disease Control and Prevention, Atlanta, Georgia.ORCID 0000-0001-9162-633X
Farin KamangarDepartment of Biology, School of Computer, Mathematical, and Natural Sciences, Morgan State University, Baltimore, Maryland.
Paul BrennanInternational Agency for Research on Cancer, Lyon, France.
Paolo BoffettaThe Tisch Cancer Institute, Mount Sinai School of Medicine and Institute for Translational Epidemiology, New York, New York.
Sanford M DawseyDivision of Cancer Epidemiology and Genetics, National Cancer Institute, NIH, Bethesda, Maryland.
Christian C AbnetDivision of Cancer Epidemiology and Genetics, National Cancer Institute, NIH, Bethesda, Maryland.
Reza MalekzadehDigestive Oncology Research Center, Digestive Disease Research Institute, Tehran University of Medical Sciences, Tehran, Iran. arash.etemadi@nih.gov malek@ams.ac.ir.ORCID 0000-0002-9820-6335
Neal D FreedmanDivision of Cancer Epidemiology and Genetics, National Cancer Institute, NIH, Bethesda, Maryland.

Funding

Upper Gastrointestinal Cancer StudiesZIACP000185 · NCI · DIVISION OF CANCER EPIDEMIOLOGY AND GENETICS · PI ABNET, CHRISTIAN · 2009 to 2025
$25.6M
Cancer Research UK C20/A5860Intramural NIH HHS Z99 CA999999World Health Organization 001
6 · The paper itself

Abstract

backgroundHow carcinogen exposure varies across users of different, particularly noncigarette, tobacco products remains poorly understood.

methodsWe randomly selected 165 participants of the Golestan Cohort Study from northeastern Iran: 60 never users of any tobacco, 35 exclusive cigarette, 40 exclusive (78% daily) waterpipe, and 30 exclusive smokeless tobacco (nass) users. We measured concentrations of 39 biomarkers of exposure in 4 chemical classes in baseline urine samples: tobacco alkaloids, tobacco-specific nitrosamines (TSNA), polycyclic aromatic hydrocarbons (PAH), and volatile organic compounds (VOC). We also quantified the same biomarkers in a second urine sample, obtained 5 years later, among continuing cigarette smokers and never tobacco users.

resultsNass users had the highest concentrations of tobacco alkaloids. All tobacco users had elevated TSNA concentrations, which correlated with nicotine dose. In both cigarette and waterpipe smokers, PAH and VOC biomarkers were higher than never tobacco users and nass users, and highly correlated with nicotine dose. PAH biomarkers of phenanthrene and pyrene and two VOC metabolites (phenylmercapturic acid and phenylglyoxylic acid) were higher in waterpipe smokers than in all other groups. PAH biomarkers among Golestan never tobacco users were comparable to those in U.S. cigarette smokers. All biomarkers had moderate to good correlations over 5 years, particularly in continuing cigarette smokers.

conclusionsWe observed two patterns of exposure biomarkers that differentiated the use of the combustible products (cigarettes and waterpipe) from the smokeless product. Environmental exposure from nontobacco sources appeared to contribute to the presence of high levels of PAH metabolites in the Golestan Cohort. IMPACT: Most of these biomarkers would be useful for exposure assessment in a longitudinal study.

Indexed as

AdultAlkaloidsBiomarkers, TumorCarcinogensCohort StudiesHumansIranMiddle AgedNitrosaminesPolycyclic Aromatic HydrocarbonsSmokingTobacco ProductsTobacco, SmokelessTobacco UseVolatile Organic CompoundsWater Pipe SmokingAlkaloidsBiomarkers, TumorCarcinogensNitrosaminesPolycyclic Aromatic HydrocarbonsVolatile Organic Compounds

Identifiers

PMID30622099
PMCPMC6935158

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Registered trials

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Read under generation 80e0d062 · epoch 390. Bibliography from PubMed, PubMed Central and OpenAlex; grants from NIH RePORTER; trial links from ClinicalTrials.gov; estimates, votes and beliefs from the OpenQuestion graph.