Associated Links Among Smoking, Chronic Obstructive Pulmonary Disease, and Small Cell Lung Cancer: A Pooled Analysis in the International Lung Cancer Consortium

Ruyi Huang; Yongyue Wei; Rayjean J Hung; Geoffrey Liu; Li Su; Ruyang Zhang; Xuchen Zong; Zuo-Feng Zhang; Hal Morgenstern; Irene Brüske; Joachim Heinrich; Yun-Chul Hong; Jin Hee Kim; Michele Cote; Angela Wenzlaff; Ann G Schwartz; Isabelle Stucker; John Mclaughlin; Michael W Marcus; Michael P A Davies; Triantafillos Liloglou; John K Field; Keitaro Matsuo; Matt Barnett; Mark Thornquist; Gary Goodman; Yi Wang; Size Chen; Ping Yang; Eric J Duell; Angeline S Andrew; Philip Lazarus; Joshua Muscat; Penella Woll; Janet Horsman; M Dawn Teare; Anath Flugelman; Gad Rennert; Yan Zhang; Hermann Brenner; Christa Stegmaier; Erik H F M van der Heijden; Katja Aben; Lambertus Kiemeney; Juan Barros-Dios; Monica Pérez-Ríos; Alberto Ruano-Ravina; Neil E Caporaso; Pier Alberto Bertazzi; Maria Teresa Landi; Juncheng Dai; Hongbing Hongbing Shen; Guillermo Fernandez-Tardon; Marta Rodriguez-Suarez; Adonina Tardon; David C Christiani

doi:10.1016/j.ebiom.2015.09.031

Associated Links Among Smoking, Chronic Obstructive Pulmonary Disease, and Small Cell Lung Cancer: A Pooled Analysis in the International Lung Cancer Consortium

Ruyi Huang, Yongyue Wei, Rayjean J Hung, Geoffrey Liu, Li Su, Ruyang Zhang, Xuchen Zong, Zuo-Feng Zhang, Hal Morgenstern, Irene Brüske, Joachim Heinrich, Yun-Chul Hong, Jin Hee Kim, Michele Cote, Angela Wenzlaff, Ann G Schwartz, Isabelle Stucker, John Mclaughlin, Michael W Marcus, Michael P A DaviesTriantafillos Liloglou, John K Field, Keitaro Matsuo, Matt Barnett, Mark Thornquist, Gary Goodman, Yi Wang, Size Chen, Ping Yang, Eric J Duell, Angeline S Andrew, Philip Lazarus, Joshua Muscat, Penella Woll, Janet Horsman, M Dawn Teare, Anath Flugelman, Gad Rennert, Yan Zhang, Hermann Brenner, Christa Stegmaier, Erik H F M van der Heijden, Katja Aben, Lambertus Kiemeney, Juan Barros-Dios, Monica Pérez-Ríos, Alberto Ruano-Ravina, Neil E Caporaso, Pier Alberto Bertazzi, Maria Teresa Landi, Juncheng Dai, Hongbing Hongbing Shen, Guillermo Fernandez-Tardon, Marta Rodriguez-Suarez, Adonina Tardon, David C Christiani

Medical School

University of Liverpool

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

56 Citations (Scopus)

Abstract

BACKGROUND: The high relapse and mortality rate of small-cell lung cancer (SCLC) fuels the need for epidemiologic study to aid in its prevention.

METHODS: We included 24 studies from the ILCCO collaboration. Random-effects panel logistic regression and cubic spline regression were used to estimate the effects of smoking behaviors on SCLC risk and explore their non-linearity. Further, we explored whether the risk of smoking on SCLC was mediated through COPD.

FINDINGS: Significant dose-response relationships of SCLC risk were observed for all quantitative smoking variables. Smoking pack-years were associated with a sharper increase of SCLC risk for pack-years ranged 0 to approximately 50. The former smokers with longer cessation showed a 43%quit_for_5-9 years to 89%quit_for_≥ 20 years declined SCLC risk vs. subjects who had quit smoking < 5 years. Compared with non-COPD subjects, smoking behaviors showed a significantly higher effect on SCLC risk among COPD subjects, and further, COPD patients showed a 1.86-fold higher risk of SCLC. Furthermore, smoking behaviors on SCLC risk were significantly mediated through COPD which accounted for 0.70% to 7.55% of total effects.

INTERPRETATION: This is the largest pooling study that provides improved understanding of smoking on SCLC, and further demonstrates a causal pathway through COPD that warrants further experimental study.

Original language	English
Pages (from-to)	1677-85
Number of pages	9
Journal	eBioMedicine
Volume	2
Issue number	11
DOIs	https://doi.org/10.1016/j.ebiom.2015.09.031
Publication status	Published - Nov 2015

Keywords

Aged
Case-Control Studies
Female
Humans
Lung Neoplasms/epidemiology
Male
Middle Aged
Models, Biological
Odds Ratio
Population Surveillance
Pulmonary Disease, Chronic Obstructive/complications
Risk
Small Cell Lung Carcinoma/epidemiology
Smoking/adverse effects
Time Factors

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1016/j.ebiom.2015.09.031

Cite this

Huang, R., Wei, Y., Hung, R. J., Liu, G., Su, L., Zhang, R., Zong, X., Zhang, Z.-F., Morgenstern, H., Brüske, I., Heinrich, J., Hong, Y.-C., Kim, J. H., Cote, M., Wenzlaff, A., Schwartz, A. G., Stucker, I., Mclaughlin, J., Marcus, M. W., ... Christiani, D. C. (2015). Associated Links Among Smoking, Chronic Obstructive Pulmonary Disease, and Small Cell Lung Cancer: A Pooled Analysis in the International Lung Cancer Consortium. eBioMedicine, 2(11), 1677-85. https://doi.org/10.1016/j.ebiom.2015.09.031

@article{b551f6b764714cb7b2a33615f5a7b6b3,

title = "Associated Links Among Smoking, Chronic Obstructive Pulmonary Disease, and Small Cell Lung Cancer: A Pooled Analysis in the International Lung Cancer Consortium",

abstract = "BACKGROUND: The high relapse and mortality rate of small-cell lung cancer (SCLC) fuels the need for epidemiologic study to aid in its prevention.METHODS: We included 24 studies from the ILCCO collaboration. Random-effects panel logistic regression and cubic spline regression were used to estimate the effects of smoking behaviors on SCLC risk and explore their non-linearity. Further, we explored whether the risk of smoking on SCLC was mediated through COPD.FINDINGS: Significant dose-response relationships of SCLC risk were observed for all quantitative smoking variables. Smoking pack-years were associated with a sharper increase of SCLC risk for pack-years ranged 0 to approximately 50. The former smokers with longer cessation showed a 43%quit_for_5-9 years to 89%quit_for_≥ 20 years declined SCLC risk vs. subjects who had quit smoking < 5 years. Compared with non-COPD subjects, smoking behaviors showed a significantly higher effect on SCLC risk among COPD subjects, and further, COPD patients showed a 1.86-fold higher risk of SCLC. Furthermore, smoking behaviors on SCLC risk were significantly mediated through COPD which accounted for 0.70% to 7.55% of total effects.INTERPRETATION: This is the largest pooling study that provides improved understanding of smoking on SCLC, and further demonstrates a causal pathway through COPD that warrants further experimental study.",

keywords = "Aged, Case-Control Studies, Female, Humans, Lung Neoplasms/epidemiology, Male, Middle Aged, Models, Biological, Odds Ratio, Population Surveillance, Pulmonary Disease, Chronic Obstructive/complications, Risk, Small Cell Lung Carcinoma/epidemiology, Smoking/adverse effects, Time Factors",

author = "Ruyi Huang and Yongyue Wei and Hung, {Rayjean J} and Geoffrey Liu and Li Su and Ruyang Zhang and Xuchen Zong and Zuo-Feng Zhang and Hal Morgenstern and Irene Br{\"u}ske and Joachim Heinrich and Yun-Chul Hong and Kim, {Jin Hee} and Michele Cote and Angela Wenzlaff and Schwartz, {Ann G} and Isabelle Stucker and John Mclaughlin and Marcus, {Michael W} and Davies, {Michael P A} and Triantafillos Liloglou and Field, {John K} and Keitaro Matsuo and Matt Barnett and Mark Thornquist and Gary Goodman and Yi Wang and Size Chen and Ping Yang and Duell, {Eric J} and Andrew, {Angeline S} and Philip Lazarus and Joshua Muscat and Penella Woll and Janet Horsman and Teare, {M Dawn} and Anath Flugelman and Gad Rennert and Yan Zhang and Hermann Brenner and Christa Stegmaier and {van der Heijden}, {Erik H F M} and Katja Aben and Lambertus Kiemeney and Juan Barros-Dios and Monica P{\'e}rez-R{\'i}os and Alberto Ruano-Ravina and Caporaso, {Neil E} and Bertazzi, {Pier Alberto} and Landi, {Maria Teresa} and Juncheng Dai and {Hongbing Shen}, Hongbing and Guillermo Fernandez-Tardon and Marta Rodriguez-Suarez and Adonina Tardon and Christiani, {David C}",

year = "2015",

month = nov,

doi = "10.1016/j.ebiom.2015.09.031",

language = "English",

volume = "2",

pages = "1677--85",

journal = "eBioMedicine",

issn = "2352-3964",

publisher = "Elsevier BV",

number = "11",

}

Huang, R, Wei, Y, Hung, RJ, Liu, G, Su, L, Zhang, R, Zong, X, Zhang, Z-F, Morgenstern, H, Brüske, I, Heinrich, J, Hong, Y-C, Kim, JH, Cote, M, Wenzlaff, A, Schwartz, AG, Stucker, I, Mclaughlin, J, Marcus, MW, Davies, MPA, Liloglou, T, Field, JK, Matsuo, K, Barnett, M, Thornquist, M, Goodman, G, Wang, Y, Chen, S, Yang, P, Duell, EJ, Andrew, AS, Lazarus, P, Muscat, J, Woll, P, Horsman, J, Teare, MD, Flugelman, A, Rennert, G, Zhang, Y, Brenner, H, Stegmaier, C, van der Heijden, EHFM, Aben, K, Kiemeney, L, Barros-Dios, J, Pérez-Ríos, M, Ruano-Ravina, A, Caporaso, NE, Bertazzi, PA, Landi, MT, Dai, J, Hongbing Shen, H, Fernandez-Tardon, G, Rodriguez-Suarez, M, Tardon, A & Christiani, DC 2015, 'Associated Links Among Smoking, Chronic Obstructive Pulmonary Disease, and Small Cell Lung Cancer: A Pooled Analysis in the International Lung Cancer Consortium', eBioMedicine, vol. 2, no. 11, pp. 1677-85. https://doi.org/10.1016/j.ebiom.2015.09.031

TY - JOUR

T1 - Associated Links Among Smoking, Chronic Obstructive Pulmonary Disease, and Small Cell Lung Cancer

T2 - A Pooled Analysis in the International Lung Cancer Consortium

AU - Huang, Ruyi

AU - Wei, Yongyue

AU - Hung, Rayjean J

AU - Liu, Geoffrey

AU - Su, Li

AU - Zhang, Ruyang

AU - Zong, Xuchen

AU - Zhang, Zuo-Feng

AU - Morgenstern, Hal

AU - Brüske, Irene

AU - Heinrich, Joachim

AU - Hong, Yun-Chul

AU - Kim, Jin Hee

AU - Cote, Michele

AU - Wenzlaff, Angela

AU - Schwartz, Ann G

AU - Stucker, Isabelle

AU - Mclaughlin, John

AU - Marcus, Michael W

AU - Davies, Michael P A

AU - Liloglou, Triantafillos

AU - Field, John K

AU - Matsuo, Keitaro

AU - Barnett, Matt

AU - Thornquist, Mark

AU - Goodman, Gary

AU - Wang, Yi

AU - Chen, Size

AU - Yang, Ping

AU - Duell, Eric J

AU - Andrew, Angeline S

AU - Lazarus, Philip

AU - Muscat, Joshua

AU - Woll, Penella

AU - Horsman, Janet

AU - Teare, M Dawn

AU - Flugelman, Anath

AU - Rennert, Gad

AU - Zhang, Yan

AU - Brenner, Hermann

AU - Stegmaier, Christa

AU - van der Heijden, Erik H F M

AU - Aben, Katja

AU - Kiemeney, Lambertus

AU - Barros-Dios, Juan

AU - Pérez-Ríos, Monica

AU - Ruano-Ravina, Alberto

AU - Caporaso, Neil E

AU - Bertazzi, Pier Alberto

AU - Landi, Maria Teresa

AU - Dai, Juncheng

AU - Hongbing Shen, Hongbing

AU - Fernandez-Tardon, Guillermo

AU - Rodriguez-Suarez, Marta

AU - Tardon, Adonina

AU - Christiani, David C

PY - 2015/11

Y1 - 2015/11

N2 - BACKGROUND: The high relapse and mortality rate of small-cell lung cancer (SCLC) fuels the need for epidemiologic study to aid in its prevention.METHODS: We included 24 studies from the ILCCO collaboration. Random-effects panel logistic regression and cubic spline regression were used to estimate the effects of smoking behaviors on SCLC risk and explore their non-linearity. Further, we explored whether the risk of smoking on SCLC was mediated through COPD.FINDINGS: Significant dose-response relationships of SCLC risk were observed for all quantitative smoking variables. Smoking pack-years were associated with a sharper increase of SCLC risk for pack-years ranged 0 to approximately 50. The former smokers with longer cessation showed a 43%quit_for_5-9 years to 89%quit_for_≥ 20 years declined SCLC risk vs. subjects who had quit smoking < 5 years. Compared with non-COPD subjects, smoking behaviors showed a significantly higher effect on SCLC risk among COPD subjects, and further, COPD patients showed a 1.86-fold higher risk of SCLC. Furthermore, smoking behaviors on SCLC risk were significantly mediated through COPD which accounted for 0.70% to 7.55% of total effects.INTERPRETATION: This is the largest pooling study that provides improved understanding of smoking on SCLC, and further demonstrates a causal pathway through COPD that warrants further experimental study.

AB - BACKGROUND: The high relapse and mortality rate of small-cell lung cancer (SCLC) fuels the need for epidemiologic study to aid in its prevention.METHODS: We included 24 studies from the ILCCO collaboration. Random-effects panel logistic regression and cubic spline regression were used to estimate the effects of smoking behaviors on SCLC risk and explore their non-linearity. Further, we explored whether the risk of smoking on SCLC was mediated through COPD.FINDINGS: Significant dose-response relationships of SCLC risk were observed for all quantitative smoking variables. Smoking pack-years were associated with a sharper increase of SCLC risk for pack-years ranged 0 to approximately 50. The former smokers with longer cessation showed a 43%quit_for_5-9 years to 89%quit_for_≥ 20 years declined SCLC risk vs. subjects who had quit smoking < 5 years. Compared with non-COPD subjects, smoking behaviors showed a significantly higher effect on SCLC risk among COPD subjects, and further, COPD patients showed a 1.86-fold higher risk of SCLC. Furthermore, smoking behaviors on SCLC risk were significantly mediated through COPD which accounted for 0.70% to 7.55% of total effects.INTERPRETATION: This is the largest pooling study that provides improved understanding of smoking on SCLC, and further demonstrates a causal pathway through COPD that warrants further experimental study.

KW - Aged

KW - Case-Control Studies

KW - Female

KW - Humans

KW - Lung Neoplasms/epidemiology

KW - Male

KW - Middle Aged

KW - Models, Biological

KW - Odds Ratio

KW - Population Surveillance

KW - Pulmonary Disease, Chronic Obstructive/complications

KW - Risk

KW - Small Cell Lung Carcinoma/epidemiology

KW - Smoking/adverse effects

KW - Time Factors

U2 - 10.1016/j.ebiom.2015.09.031

DO - 10.1016/j.ebiom.2015.09.031

M3 - Article (journal)

C2 - 26870794

SN - 2352-3964

VL - 2

SP - 1677

EP - 1685

JO - eBioMedicine

JF - eBioMedicine

IS - 11

ER -

Associated Links Among Smoking, Chronic Obstructive Pulmonary Disease, and Small Cell Lung Cancer: A Pooled Analysis in the International Lung Cancer Consortium

Abstract

Keywords

UN SDGs

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