Metabolites of the Polycyclic Aromatic Hydrocarbon Phenanthrene in the Urine of Cigarette Smokers from Five Ethnic Groups with Differing Risks for Lung Cancer
Results from the Multiethnic Cohort Study demonstrated significant differences in lung cancer risk among cigarette smokers from five different ethnic/racial groups. For the same number of cigarettes smoked, and particularly among light smokers, African Americans and Native Hawaiians had the highest...
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| Veröffentlicht in: | PloS one 2016-06, Vol.11 (6), p.e0156203 |
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| creator | Patel, Yesha M Park, Sungshim L Carmella, Steven G Paiano, Viviana Olvera, Natalie Stram, Daniel O Haiman, Christopher A Le Marchand, Loic Hecht, Stephen S |
| description | Results from the Multiethnic Cohort Study demonstrated significant differences in lung cancer risk among cigarette smokers from five different ethnic/racial groups. For the same number of cigarettes smoked, and particularly among light smokers, African Americans and Native Hawaiians had the highest risk for lung cancer, Whites had intermediate risk, while Latinos and Japanese Americans had the lowest risk. We analyzed urine samples from 331-709 participants from each ethnic group in this study for metabolites of phenanthrene, a surrogate for carcinogenic polycyclic aromatic hydrocarbon exposure. Consistent with their lung cancer risk and our previous studies of several other carcinogens and toxicants of cigarette smoke, African Americans had significantly (p |
| doi_str_mv | 10.1371/journal.pone.0156203 |
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For the same number of cigarettes smoked, and particularly among light smokers, African Americans and Native Hawaiians had the highest risk for lung cancer, Whites had intermediate risk, while Latinos and Japanese Americans had the lowest risk. We analyzed urine samples from 331-709 participants from each ethnic group in this study for metabolites of phenanthrene, a surrogate for carcinogenic polycyclic aromatic hydrocarbon exposure. Consistent with their lung cancer risk and our previous studies of several other carcinogens and toxicants of cigarette smoke, African Americans had significantly (p<0.0001) higher median levels of the two phenanthrene metabolites 3-hydroxyphenanthrene (3-PheOH, 0.931 pmol/ml) and phenanthrene tetraol (PheT, 1.13 pmol/ml) than Whites (3-PheOH, 0.697 pmol/ml; PheT, 0.853 pmol/ml) while Japanese-Americans had significantly (p = 0.002) lower levels of 3-PheOH (0.621 pmol/ml) than Whites. PheT levels (0.838 pmol/ml) in Japanese-Americans were not different from those of Whites. These results are mainly consistent with the lung cancer risk of these three groups, but the results for Native Hawaiians and Latinos were more complex. We also carried out a genome wide association study in search of factors that could influence PheT and 3-PheOH levels. Deletion of GSTT1 explained 2.2% of the variability in PheT, while the strongest association, rs5751777 (p = 1.8x10-62) in the GSTT2 gene, explained 7.7% of the variability in PheT. These GWAS results suggested a possible protective effect of lower GSTT1 copy number variants on the diol epoxide pathway, which was an unexpected result. Collectively, the results of this study provide further evidence that different patterns of cigarette smoking are responsible for the higher lung cancer risk of African Americans than of Whites and the lower lung cancer risk of Japanese Americans, while other factors appear to be involved in the differing risks of Native Hawaiians and Latinos.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0156203</identifier><identifier>PMID: 27275760</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Aged ; Aromatic hydrocarbons ; Biology and Life Sciences ; Cancer ; Carcinogens ; Cigarette smoke ; Cigarette smoking ; Cigarettes ; Complications and side effects ; Copy number ; Demographic aspects ; Deoxyribonucleic acid ; Diagnosis ; DNA ; Epidemiology ; Female ; Gene Dosage ; Genome-wide association studies ; Genomes ; Glutathione Transferase - genetics ; GSTT1 protein ; Health risks ; Humans ; Hydrocarbons ; Laboratory animals ; Lung cancer ; Lung diseases ; Lung Neoplasms - enzymology ; Lung Neoplasms - ethnology ; Lung Neoplasms - genetics ; Lung Neoplasms - urine ; Male ; Medicine and Health Sciences ; Metabolites ; Middle Aged ; Minority & ethnic groups ; Mutation ; Neoplasm Proteins - genetics ; People and places ; Phenanthrene ; Phenanthrenes - urine ; Physical Sciences ; Physiological aspects ; Polycyclic aromatic hydrocarbons ; Preventive medicine ; Questionnaires ; Risk analysis ; Risk Factors ; Smoke ; Smoking ; Smoking - ethnology ; Smoking - genetics ; Smoking - metabolism ; Smoking - urine ; Studies ; Tobacco smoke ; Toxicants ; Urine ; Variability</subject><ispartof>PloS one, 2016-06, Vol.11 (6), p.e0156203</ispartof><rights>COPYRIGHT 2016 Public Library of Science</rights><rights>2016 Patel et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2016 Patel et al 2016 Patel et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c725t-4f9eb6d9372650187d37e25ca4c2404e395836248e033e34bcc8eaaadb9635163</citedby><cites>FETCH-LOGICAL-c725t-4f9eb6d9372650187d37e25ca4c2404e395836248e033e34bcc8eaaadb9635163</cites><orcidid>0000-0001-7228-1356</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4898721/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4898721/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2102,2928,23866,27924,27925,53791,53793,79600,79601</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27275760$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Costa, Max</contributor><creatorcontrib>Patel, Yesha M</creatorcontrib><creatorcontrib>Park, Sungshim L</creatorcontrib><creatorcontrib>Carmella, Steven G</creatorcontrib><creatorcontrib>Paiano, Viviana</creatorcontrib><creatorcontrib>Olvera, Natalie</creatorcontrib><creatorcontrib>Stram, Daniel O</creatorcontrib><creatorcontrib>Haiman, Christopher A</creatorcontrib><creatorcontrib>Le Marchand, Loic</creatorcontrib><creatorcontrib>Hecht, Stephen S</creatorcontrib><title>Metabolites of the Polycyclic Aromatic Hydrocarbon Phenanthrene in the Urine of Cigarette Smokers from Five Ethnic Groups with Differing Risks for Lung Cancer</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Results from the Multiethnic Cohort Study demonstrated significant differences in lung cancer risk among cigarette smokers from five different ethnic/racial groups. For the same number of cigarettes smoked, and particularly among light smokers, African Americans and Native Hawaiians had the highest risk for lung cancer, Whites had intermediate risk, while Latinos and Japanese Americans had the lowest risk. We analyzed urine samples from 331-709 participants from each ethnic group in this study for metabolites of phenanthrene, a surrogate for carcinogenic polycyclic aromatic hydrocarbon exposure. Consistent with their lung cancer risk and our previous studies of several other carcinogens and toxicants of cigarette smoke, African Americans had significantly (p<0.0001) higher median levels of the two phenanthrene metabolites 3-hydroxyphenanthrene (3-PheOH, 0.931 pmol/ml) and phenanthrene tetraol (PheT, 1.13 pmol/ml) than Whites (3-PheOH, 0.697 pmol/ml; PheT, 0.853 pmol/ml) while Japanese-Americans had significantly (p = 0.002) lower levels of 3-PheOH (0.621 pmol/ml) than Whites. PheT levels (0.838 pmol/ml) in Japanese-Americans were not different from those of Whites. These results are mainly consistent with the lung cancer risk of these three groups, but the results for Native Hawaiians and Latinos were more complex. We also carried out a genome wide association study in search of factors that could influence PheT and 3-PheOH levels. Deletion of GSTT1 explained 2.2% of the variability in PheT, while the strongest association, rs5751777 (p = 1.8x10-62) in the GSTT2 gene, explained 7.7% of the variability in PheT. These GWAS results suggested a possible protective effect of lower GSTT1 copy number variants on the diol epoxide pathway, which was an unexpected result. Collectively, the results of this study provide further evidence that different patterns of cigarette smoking are responsible for the higher lung cancer risk of African Americans than of Whites and the lower lung cancer risk of Japanese Americans, while other factors appear to be involved in the differing risks of Native Hawaiians and Latinos.</description><subject>Aged</subject><subject>Aromatic hydrocarbons</subject><subject>Biology and Life Sciences</subject><subject>Cancer</subject><subject>Carcinogens</subject><subject>Cigarette smoke</subject><subject>Cigarette smoking</subject><subject>Cigarettes</subject><subject>Complications and side effects</subject><subject>Copy number</subject><subject>Demographic aspects</subject><subject>Deoxyribonucleic acid</subject><subject>Diagnosis</subject><subject>DNA</subject><subject>Epidemiology</subject><subject>Female</subject><subject>Gene Dosage</subject><subject>Genome-wide association studies</subject><subject>Genomes</subject><subject>Glutathione Transferase - 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ethnology</subject><subject>Smoking - genetics</subject><subject>Smoking - metabolism</subject><subject>Smoking - urine</subject><subject>Studies</subject><subject>Tobacco smoke</subject><subject>Toxicants</subject><subject>Urine</subject><subject>Variability</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNqNk89u1DAQxiMEoqXwBggsISE47JLYTuJcKlVL_6xU1KqlXC3HmWzcZu3Fdgr7Mjwrs91t1UU9oBwynvy-b-yJJ0neZuk4Y2X25doN3qp-vHAWxmmWFzRlz5LdrGJ0tIqfP4p3klchXKdpzkRRvEx2aEnLvCzS3eTPN4iqdr2JEIhrSeyAnLt-qZe6N5oceDdXEYOTZeOdVr52lpx3YJWNnQcLxNg7zZU3uECDiZkpDzECuZy7G_CBtOhBjswtkMPYWfQ69m5YBPLLxI58NW0LqJ2RCxNuEHaenA64nCirwb9OXrSqD_Bm895Lro4Ov09ORqdnx9PJwelIlzSPI95WUBdNxUpa5GkmyoaVQHOtuKY85cCqXLCCcgEpY8B4rbUApVRTVwXLs4LtJe_XvoveBblpbZBZWXFBKXYQiemaaJy6lgtv5sovpVNG3iWcn0nlsVM9yLopalpCVWmO1XUmaiZy0QKmUwp5hV77m2pDPYdGg41e9Vum21-s6eTM3UouKlHSDA0-bQy8-zlAiHJugoa-VxbcgPsWKXK85KtaH_5Bnz7dhpopPICxrcO6emUqD3jO8XIJLpAaP0Hh08DcaLyHrcH8luDzlgCZCL_jTA0hyOnlxf-zZz-22Y-P2A5UH7vg-iEaZ8M2yNeg9i4ED-1Dk7NUrsbovhtyNUZyM0Yoe_f4Bz2I7ueG_QVIZxjk</recordid><startdate>20160608</startdate><enddate>20160608</enddate><creator>Patel, Yesha M</creator><creator>Park, Sungshim L</creator><creator>Carmella, Steven G</creator><creator>Paiano, Viviana</creator><creator>Olvera, Natalie</creator><creator>Stram, Daniel O</creator><creator>Haiman, Christopher A</creator><creator>Le Marchand, Loic</creator><creator>Hecht, Stephen S</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0001-7228-1356</orcidid></search><sort><creationdate>20160608</creationdate><title>Metabolites of the Polycyclic Aromatic Hydrocarbon Phenanthrene in the Urine of Cigarette Smokers from Five Ethnic Groups with Differing Risks for Lung Cancer</title><author>Patel, Yesha M ; Park, Sungshim L ; Carmella, Steven G ; Paiano, Viviana ; Olvera, Natalie ; Stram, Daniel O ; Haiman, Christopher A ; Le Marchand, Loic ; Hecht, Stephen S</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c725t-4f9eb6d9372650187d37e25ca4c2404e395836248e033e34bcc8eaaadb9635163</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Aged</topic><topic>Aromatic hydrocarbons</topic><topic>Biology and Life Sciences</topic><topic>Cancer</topic><topic>Carcinogens</topic><topic>Cigarette smoke</topic><topic>Cigarette smoking</topic><topic>Cigarettes</topic><topic>Complications and side effects</topic><topic>Copy number</topic><topic>Demographic aspects</topic><topic>Deoxyribonucleic acid</topic><topic>Diagnosis</topic><topic>DNA</topic><topic>Epidemiology</topic><topic>Female</topic><topic>Gene Dosage</topic><topic>Genome-wide association studies</topic><topic>Genomes</topic><topic>Glutathione Transferase - 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Academic</collection><collection>ProQuest Engineering Collection</collection><collection>ProQuest Biological Science Collection</collection><collection>Agricultural Science Database</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>Engineering Database</collection><collection>Nursing & Allied Health Premium</collection><collection>Advanced Technologies & Aerospace Database</collection><collection>ProQuest Advanced Technologies & Aerospace Collection</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environmental Science Database</collection><collection>Materials Science Collection</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>Engineering Collection</collection><collection>Environmental Science Collection</collection><collection>Genetics Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Patel, Yesha M</au><au>Park, Sungshim L</au><au>Carmella, Steven G</au><au>Paiano, Viviana</au><au>Olvera, Natalie</au><au>Stram, Daniel O</au><au>Haiman, Christopher A</au><au>Le Marchand, Loic</au><au>Hecht, Stephen S</au><au>Costa, Max</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Metabolites of the Polycyclic Aromatic Hydrocarbon Phenanthrene in the Urine of Cigarette Smokers from Five Ethnic Groups with Differing Risks for Lung Cancer</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2016-06-08</date><risdate>2016</risdate><volume>11</volume><issue>6</issue><spage>e0156203</spage><pages>e0156203-</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Results from the Multiethnic Cohort Study demonstrated significant differences in lung cancer risk among cigarette smokers from five different ethnic/racial groups. For the same number of cigarettes smoked, and particularly among light smokers, African Americans and Native Hawaiians had the highest risk for lung cancer, Whites had intermediate risk, while Latinos and Japanese Americans had the lowest risk. We analyzed urine samples from 331-709 participants from each ethnic group in this study for metabolites of phenanthrene, a surrogate for carcinogenic polycyclic aromatic hydrocarbon exposure. Consistent with their lung cancer risk and our previous studies of several other carcinogens and toxicants of cigarette smoke, African Americans had significantly (p<0.0001) higher median levels of the two phenanthrene metabolites 3-hydroxyphenanthrene (3-PheOH, 0.931 pmol/ml) and phenanthrene tetraol (PheT, 1.13 pmol/ml) than Whites (3-PheOH, 0.697 pmol/ml; PheT, 0.853 pmol/ml) while Japanese-Americans had significantly (p = 0.002) lower levels of 3-PheOH (0.621 pmol/ml) than Whites. PheT levels (0.838 pmol/ml) in Japanese-Americans were not different from those of Whites. These results are mainly consistent with the lung cancer risk of these three groups, but the results for Native Hawaiians and Latinos were more complex. We also carried out a genome wide association study in search of factors that could influence PheT and 3-PheOH levels. Deletion of GSTT1 explained 2.2% of the variability in PheT, while the strongest association, rs5751777 (p = 1.8x10-62) in the GSTT2 gene, explained 7.7% of the variability in PheT. These GWAS results suggested a possible protective effect of lower GSTT1 copy number variants on the diol epoxide pathway, which was an unexpected result. Collectively, the results of this study provide further evidence that different patterns of cigarette smoking are responsible for the higher lung cancer risk of African Americans than of Whites and the lower lung cancer risk of Japanese Americans, while other factors appear to be involved in the differing risks of Native Hawaiians and Latinos.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>27275760</pmid><doi>10.1371/journal.pone.0156203</doi><orcidid>https://orcid.org/0000-0001-7228-1356</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2016-06, Vol.11 (6), p.e0156203 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_1794822203 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Public Library of Science (PLoS) Journals Open Access; EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Aged Aromatic hydrocarbons Biology and Life Sciences Cancer Carcinogens Cigarette smoke Cigarette smoking Cigarettes Complications and side effects Copy number Demographic aspects Deoxyribonucleic acid Diagnosis DNA Epidemiology Female Gene Dosage Genome-wide association studies Genomes Glutathione Transferase - genetics GSTT1 protein Health risks Humans Hydrocarbons Laboratory animals Lung cancer Lung diseases Lung Neoplasms - enzymology Lung Neoplasms - ethnology Lung Neoplasms - genetics Lung Neoplasms - urine Male Medicine and Health Sciences Metabolites Middle Aged Minority & ethnic groups Mutation Neoplasm Proteins - genetics People and places Phenanthrene Phenanthrenes - urine Physical Sciences Physiological aspects Polycyclic aromatic hydrocarbons Preventive medicine Questionnaires Risk analysis Risk Factors Smoke Smoking Smoking - ethnology Smoking - genetics Smoking - metabolism Smoking - urine Studies Tobacco smoke Toxicants Urine Variability |
| title | Metabolites of the Polycyclic Aromatic Hydrocarbon Phenanthrene in the Urine of Cigarette Smokers from Five Ethnic Groups with Differing Risks for Lung Cancer |
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