Longitudinal stability in cigarette smokers of urinary eicosanoid biomarkers of oxidative damage and inflammation

Steven G. Carmella; Alisa K. Heskin; Mei Kuen Tang; Joni Jensen; Xianghua Luo; Chap T. Le; Sharon E. Murphy; Neal L. Benowitz; F. Joseph McClernon; Ryan Vandrey; Sharon S. Allen; Rachel Denlinger-Apte; Paul M. Cinciripini; Andrew A. Strasser; Mustafa Al’Absi; Jason D. Robinson; Eric C. Donny; Dorothy K. Hatsukami; Stephen S. Hecht

doi:10.1371/journal.pone.0215853

Longitudinal stability in cigarette smokers of urinary eicosanoid biomarkers of oxidative damage and inflammation

Steven G. Carmella, Alisa K. Heskin, Mei Kuen Tang, Joni Jensen, Xianghua Luo, Chap T. Le, Sharon E. Murphy, Neal L. Benowitz, F. Joseph McClernon, Ryan Vandrey, Sharon S. Allen, Rachel Denlinger-Apte, Paul M. Cinciripini, Andrew A. Strasser, Mustafa Al’Absi, Jason D. Robinson, Eric C. Donny, Dorothy K. Hatsukami, Stephen S. Hecht

Research output: Contribution to journal › Article › peer-review

7 Scopus citations

Abstract

The urinary metabolites (Z)-7-[1R,2R,3R,5S)-3,5-dihydroxy-2-[(E,3S)-3-hydroxyoct-1-enyl] cyclopentyl]hept-5-enoic acid (8-iso-PGF _2α ), an F2-isoprostane and biomarker of oxidative damage, and “prostaglandin E ₂ metabolite” (PGE-M), a biomarker of inflammation, are elevated in cigarette smokers. However, there is little information in the literature on the longitudinal stability of these widely used biomarkers. In a large clinical trial involving 10 institutional sites, smokers were given, free of charge over a period of 20 weeks, Spectrum NRC600/601 research cigarettes containing 15.5 mg nicotine/g tobacco. All participants were instructed to smoke these cigarettes for the duration of the study. At weeks 4, 8, 12, 16, and 20, first morning urine voids were collected and analyzed for 8-iso-PGF _2α and PGE-M using validated liquid chromatography-electrospray ionization-tandem mass spectrometry methods. The mean level of 8-iso-PGF _2α at Week 4 was 1.34 ± 1.08 (S.D.) pmol/mg creatinine (N = 226) while that of PGE-M was 73.7 ± 113 (S.D.) pmol/mg creatinine (N = 232). The corresponding levels at Week 20 were 1.35 ± 0.93 (S.D.) pmol/mg creatinine (N = 209) for 8-iso-PGF _2α and 74.2 ± 142 (S.D.) pmol/mg creatinine (N = 210) for PGE-M. There was variation in these values in the intervening weeks. The intra-class correlation coefficients (ICC) were 0.51 (95% CI, 0.45, 0.57) and 0.36 (0.30, 0.43), for 8-iso-PGF _2α and PGE-M, respectively, indicating fair longitudinal stability for 8-iso-PGF _2α and poorer longitudinal stability for PGE-M in cigarette smokers. Males had higher ICC values than females for both 8-iso-PGF _2α and PGE-M. These results indicate that, in addition to cigarette smoking, endogenous processes of oxidative damage and inflammation influence the levels of these biomarkers over time among current smokers.

Original language	English (US)
Article number	e0215853
Journal	PloS one
Volume	14
Issue number	4
DOIs	https://doi.org/10.1371/journal.pone.0215853
State	Published - Apr 2019

Bibliographical note

Funding Information:
This work was supported by National Institute on Drug Abuse and Food and Drug Administration grant U54 DA-031659 (ECD, DKH, CTL, and SSH). The funders had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and decision to submit the manuscript for publication. The authors are indebted to the contributions of the Masonic Cancer Center Analytical Biochemistry Shared Resource, which provided mass spectrometry support essential for this study. The Shared Resource is supported in part by National Cancer Institute Cancer Center Support Grant CA-077598.

PubMed: MeSH publication types

Journal Article
Research Support, N.I.H., Extramural
Research Support, U.S. Gov't, P.H.S.

Access

10.1371/journal.pone.0215853

Fingerprint Dive into the research topics of 'Longitudinal stability in cigarette smokers of urinary eicosanoid biomarkers of oxidative damage and inflammation'. Together they form a unique fingerprint.

Cite this

Carmella, S. G., Heskin, A. K., Tang, M. K., Jensen, J., Luo, X., Le, C. T., Murphy, S. E., Benowitz, N. L., Joseph McClernon, F., Vandrey, R., Allen, S. S., Denlinger-Apte, R., Cinciripini, P. M., Strasser, A. A., Al’Absi, M., Robinson, J. D., Donny, E. C., Hatsukami, D. K., & Hecht, S. S. (2019). Longitudinal stability in cigarette smokers of urinary eicosanoid biomarkers of oxidative damage and inflammation. PloS one, 14(4), [e0215853]. https://doi.org/10.1371/journal.pone.0215853

Longitudinal stability in cigarette smokers of urinary eicosanoid biomarkers of oxidative damage and inflammation. / Carmella, Steven G.; Heskin, Alisa K.; Tang, Mei Kuen; Jensen, Joni; Luo, Xianghua ; Le, Chap T.; Murphy, Sharon E.; Benowitz, Neal L.; Joseph McClernon, F.; Vandrey, Ryan; Allen, Sharon S.; Denlinger-Apte, Rachel; Cinciripini, Paul M.; Strasser, Andrew A.; Al’Absi, Mustafa; Robinson, Jason D.; Donny, Eric C.; Hatsukami, Dorothy K.; Hecht, Stephen S.

In: PloS one, Vol. 14, No. 4, e0215853, 04.2019.

Research output: Contribution to journal › Article › peer-review

Carmella, SG, Heskin, AK, Tang, MK, Jensen, J, Luo, X , Le, CT , Murphy, SE, Benowitz, NL, Joseph McClernon, F, Vandrey, R, Allen, SS, Denlinger-Apte, R, Cinciripini, PM, Strasser, AA, Al’Absi, M, Robinson, JD, Donny, EC, Hatsukami, DK & Hecht, SS 2019, 'Longitudinal stability in cigarette smokers of urinary eicosanoid biomarkers of oxidative damage and inflammation', PloS one, vol. 14, no. 4, e0215853. https://doi.org/10.1371/journal.pone.0215853

Carmella, Steven G. ; Heskin, Alisa K. ; Tang, Mei Kuen ; Jensen, Joni ; Luo, Xianghua ; Le, Chap T. ; Murphy, Sharon E. ; Benowitz, Neal L. ; Joseph McClernon, F. ; Vandrey, Ryan ; Allen, Sharon S. ; Denlinger-Apte, Rachel ; Cinciripini, Paul M. ; Strasser, Andrew A. ; Al’Absi, Mustafa ; Robinson, Jason D. ; Donny, Eric C. ; Hatsukami, Dorothy K. ; Hecht, Stephen S. / Longitudinal stability in cigarette smokers of urinary eicosanoid biomarkers of oxidative damage and inflammation. In: PloS one. 2019 ; Vol. 14, No. 4.

@article{193200af5da14c18a939e5770ed52b9b,

title = "Longitudinal stability in cigarette smokers of urinary eicosanoid biomarkers of oxidative damage and inflammation",

abstract = " The urinary metabolites (Z)-7-[1R,2R,3R,5S)-3,5-dihydroxy-2-[(E,3S)-3-hydroxyoct-1-enyl] cyclopentyl]hept-5-enoic acid (8-iso-PGF 2α ), an F2-isoprostane and biomarker of oxidative damage, and “prostaglandin E 2 metabolite” (PGE-M), a biomarker of inflammation, are elevated in cigarette smokers. However, there is little information in the literature on the longitudinal stability of these widely used biomarkers. In a large clinical trial involving 10 institutional sites, smokers were given, free of charge over a period of 20 weeks, Spectrum NRC600/601 research cigarettes containing 15.5 mg nicotine/g tobacco. All participants were instructed to smoke these cigarettes for the duration of the study. At weeks 4, 8, 12, 16, and 20, first morning urine voids were collected and analyzed for 8-iso-PGF 2α and PGE-M using validated liquid chromatography-electrospray ionization-tandem mass spectrometry methods. The mean level of 8-iso-PGF 2α at Week 4 was 1.34 ± 1.08 (S.D.) pmol/mg creatinine (N = 226) while that of PGE-M was 73.7 ± 113 (S.D.) pmol/mg creatinine (N = 232). The corresponding levels at Week 20 were 1.35 ± 0.93 (S.D.) pmol/mg creatinine (N = 209) for 8-iso-PGF 2α and 74.2 ± 142 (S.D.) pmol/mg creatinine (N = 210) for PGE-M. There was variation in these values in the intervening weeks. The intra-class correlation coefficients (ICC) were 0.51 (95% CI, 0.45, 0.57) and 0.36 (0.30, 0.43), for 8-iso-PGF 2α and PGE-M, respectively, indicating fair longitudinal stability for 8-iso-PGF 2α and poorer longitudinal stability for PGE-M in cigarette smokers. Males had higher ICC values than females for both 8-iso-PGF 2α and PGE-M. These results indicate that, in addition to cigarette smoking, endogenous processes of oxidative damage and inflammation influence the levels of these biomarkers over time among current smokers. ",

author = "Carmella, {Steven G.} and Heskin, {Alisa K.} and Tang, {Mei Kuen} and Joni Jensen and Xianghua Luo and Le, {Chap T.} and Murphy, {Sharon E.} and Benowitz, {Neal L.} and {Joseph McClernon}, F. and Ryan Vandrey and Allen, {Sharon S.} and Rachel Denlinger-Apte and Cinciripini, {Paul M.} and Strasser, {Andrew A.} and Mustafa Al{\textquoteright}Absi and Robinson, {Jason D.} and Donny, {Eric C.} and Hatsukami, {Dorothy K.} and Hecht, {Stephen S.}",

note = "Funding Information: This work was supported by National Institute on Drug Abuse and Food and Drug Administration grant U54 DA-031659 (ECD, DKH, CTL, and SSH). The funders had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and decision to submit the manuscript for publication. The authors are indebted to the contributions of the Masonic Cancer Center Analytical Biochemistry Shared Resource, which provided mass spectrometry support essential for this study. The Shared Resource is supported in part by National Cancer Institute Cancer Center Support Grant CA-077598.",

year = "2019",

month = apr,

doi = "10.1371/journal.pone.0215853",

language = "English (US)",

volume = "14",

journal = "PLoS One",

issn = "1932-6203",

publisher = "Public Library of Science",

number = "4",

}

TY - JOUR

T1 - Longitudinal stability in cigarette smokers of urinary eicosanoid biomarkers of oxidative damage and inflammation

AU - Carmella, Steven G.

AU - Heskin, Alisa K.

AU - Tang, Mei Kuen

AU - Jensen, Joni

AU - Luo, Xianghua

AU - Le, Chap T.

AU - Murphy, Sharon E.

AU - Benowitz, Neal L.

AU - Joseph McClernon, F.

AU - Vandrey, Ryan

AU - Allen, Sharon S.

AU - Denlinger-Apte, Rachel

AU - Cinciripini, Paul M.

AU - Strasser, Andrew A.

AU - Al’Absi, Mustafa

AU - Robinson, Jason D.

AU - Donny, Eric C.

AU - Hatsukami, Dorothy K.

AU - Hecht, Stephen S.

N1 - Funding Information: This work was supported by National Institute on Drug Abuse and Food and Drug Administration grant U54 DA-031659 (ECD, DKH, CTL, and SSH). The funders had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and decision to submit the manuscript for publication. The authors are indebted to the contributions of the Masonic Cancer Center Analytical Biochemistry Shared Resource, which provided mass spectrometry support essential for this study. The Shared Resource is supported in part by National Cancer Institute Cancer Center Support Grant CA-077598.

PY - 2019/4

Y1 - 2019/4

N2 - The urinary metabolites (Z)-7-[1R,2R,3R,5S)-3,5-dihydroxy-2-[(E,3S)-3-hydroxyoct-1-enyl] cyclopentyl]hept-5-enoic acid (8-iso-PGF 2α ), an F2-isoprostane and biomarker of oxidative damage, and “prostaglandin E 2 metabolite” (PGE-M), a biomarker of inflammation, are elevated in cigarette smokers. However, there is little information in the literature on the longitudinal stability of these widely used biomarkers. In a large clinical trial involving 10 institutional sites, smokers were given, free of charge over a period of 20 weeks, Spectrum NRC600/601 research cigarettes containing 15.5 mg nicotine/g tobacco. All participants were instructed to smoke these cigarettes for the duration of the study. At weeks 4, 8, 12, 16, and 20, first morning urine voids were collected and analyzed for 8-iso-PGF 2α and PGE-M using validated liquid chromatography-electrospray ionization-tandem mass spectrometry methods. The mean level of 8-iso-PGF 2α at Week 4 was 1.34 ± 1.08 (S.D.) pmol/mg creatinine (N = 226) while that of PGE-M was 73.7 ± 113 (S.D.) pmol/mg creatinine (N = 232). The corresponding levels at Week 20 were 1.35 ± 0.93 (S.D.) pmol/mg creatinine (N = 209) for 8-iso-PGF 2α and 74.2 ± 142 (S.D.) pmol/mg creatinine (N = 210) for PGE-M. There was variation in these values in the intervening weeks. The intra-class correlation coefficients (ICC) were 0.51 (95% CI, 0.45, 0.57) and 0.36 (0.30, 0.43), for 8-iso-PGF 2α and PGE-M, respectively, indicating fair longitudinal stability for 8-iso-PGF 2α and poorer longitudinal stability for PGE-M in cigarette smokers. Males had higher ICC values than females for both 8-iso-PGF 2α and PGE-M. These results indicate that, in addition to cigarette smoking, endogenous processes of oxidative damage and inflammation influence the levels of these biomarkers over time among current smokers.

AB - The urinary metabolites (Z)-7-[1R,2R,3R,5S)-3,5-dihydroxy-2-[(E,3S)-3-hydroxyoct-1-enyl] cyclopentyl]hept-5-enoic acid (8-iso-PGF 2α ), an F2-isoprostane and biomarker of oxidative damage, and “prostaglandin E 2 metabolite” (PGE-M), a biomarker of inflammation, are elevated in cigarette smokers. However, there is little information in the literature on the longitudinal stability of these widely used biomarkers. In a large clinical trial involving 10 institutional sites, smokers were given, free of charge over a period of 20 weeks, Spectrum NRC600/601 research cigarettes containing 15.5 mg nicotine/g tobacco. All participants were instructed to smoke these cigarettes for the duration of the study. At weeks 4, 8, 12, 16, and 20, first morning urine voids were collected and analyzed for 8-iso-PGF 2α and PGE-M using validated liquid chromatography-electrospray ionization-tandem mass spectrometry methods. The mean level of 8-iso-PGF 2α at Week 4 was 1.34 ± 1.08 (S.D.) pmol/mg creatinine (N = 226) while that of PGE-M was 73.7 ± 113 (S.D.) pmol/mg creatinine (N = 232). The corresponding levels at Week 20 were 1.35 ± 0.93 (S.D.) pmol/mg creatinine (N = 209) for 8-iso-PGF 2α and 74.2 ± 142 (S.D.) pmol/mg creatinine (N = 210) for PGE-M. There was variation in these values in the intervening weeks. The intra-class correlation coefficients (ICC) were 0.51 (95% CI, 0.45, 0.57) and 0.36 (0.30, 0.43), for 8-iso-PGF 2α and PGE-M, respectively, indicating fair longitudinal stability for 8-iso-PGF 2α and poorer longitudinal stability for PGE-M in cigarette smokers. Males had higher ICC values than females for both 8-iso-PGF 2α and PGE-M. These results indicate that, in addition to cigarette smoking, endogenous processes of oxidative damage and inflammation influence the levels of these biomarkers over time among current smokers.

UR - http://www.scopus.com/inward/record.url?scp=85064867621&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85064867621&partnerID=8YFLogxK

U2 - 10.1371/journal.pone.0215853

DO - 10.1371/journal.pone.0215853

M3 - Article

C2 - 31022220

AN - SCOPUS:85064867621

VL - 14

JO - PLoS One

JF - PLoS One

SN - 1932-6203

IS - 4

M1 - e0215853

ER -