Risk factors for lung cancer - Cancer Australia · Risk factors for lung cancer: a systematic review is a comprehensive systematic review of the international literature commissioned

Risk factors for lung cancer A systematic review

2014

Risk factors for lung cancer: a

systematic review

Final Report

2014

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Risk factors for lung cancer: A systematic review i

Foreword

Lung cancer is the fourth most common cancer diagnosed in both men and women in

Australia and the leading cause of cancer death.

Risk factors for lung cancer: a systematic review is a comprehensive systematic review of the

international literature commissioned by Cancer Australia.

This systematic review provides a detailed analysis of the key lifestyle, environmental and

occupational factors that affect lung cancer risk, in addition to the role of family history. The

systematic review also highlights factors where the evidence is either limited or inconsistent in

relation to risk of lung cancer.

We anticipate the systematic review and the Risk factors for lung cancer: an overview, a

summary of the systematic review, will be a valuable resource to support health

professionals, policy makers and the community with evidence about exposure to risk factors

for lung cancer, to increase understanding of those who may be at greatest risk of lung

cancer and to inform interventions to ultimately reduce the burden of lung cancer.

Helen Zorbas AO

CEO

Cancer Australia

Risk factors for lung cancer: A systematic review ii

Contents

Foreword……… .....................................................................................................................................i

Acknowledgments ....................................................................................................................... xxviii

1 Introduction............................................................................................................................. 1

2 Methods .................................................................................................................................. 3

2.1 Inclusion criteria .............................................................................................................. 3

2.1.1 Types of participants ...................................................................................... 3

2.1.2 Types of intervention/Exposures of interest ............................................... 3

2.1.3 Types of outcome .......................................................................................... 4

2.1.4 Types of studies ............................................................................................... 4

2.2 Search strategy and study selection .......................................................................... 6

2.3 Critical appraisal ............................................................................................................ 7

2.4 Data extraction and synthesis ..................................................................................... 7

2.5 Use of the IARC monographs ....................................................................................... 8

3 Results ………………………………………………………………………………………………….9

3.1 Introduction ..................................................................................................................... 9

3.2 Results of database search, study selection and inclusion ................................. 15

4 Risk factor: Active smoking and passive smoking .......................................................... 17

4.1 Introduction ................................................................................................................... 17

4.2 Results ............................................................................................................................. 26

4.2.1 Active smoking and risk of lung cancer .................................................. 26

4.2.2 Active smoking, gender and risk of lung cancer ................................... 26

4.2.3 Passive smoking and risk of lung cancer ................................................. 27

4.2.4 Other forms of tobacco smoking .............................................................. 28

4.3 Summary ........................................................................................................................ 28

4.4 Conclusions.................................................................................................................... 29

4.4.1 Hazard identification ................................................................................... 29

4.4.2 Risk assessment ............................................................................................. 30

4.5 Methodological quality of studies ............................................................................ 31

5 Risk factor: Asbestos exposure ........................................................................................... 34

5.1 Introduction ................................................................................................................... 34

5.2 Results ............................................................................................................................. 41

5.2.1 Occupational exposure to asbestos and risk of lung cancer ............. 41

5.2.2 Non-occupational exposure to asbestos and risk of lung

cancer ............................................................................................................ 48

5.2.3 Asbestos exposure, gender and risk of lung cancer ............................. 49

5.2.4 Asbestos exposure, smoking status and risk of lung cancer ................ 50

5.2.5 Asbestosis, asbestos exposure and risk of lung cancer ........................ 52

5.2.6 Type of asbestos and risk of lung cancer ................................................ 53

5.3 Summary ........................................................................................................................ 54

5.4 Conclusion ..................................................................................................................... 55


5.4.2 Risk assessment ............................................................................................. 55

5.5 Methodological quality of studies ............................................................................ 56

6 Risk factor: Radon exposure ............................................................................................... 59

6.1 Introduction ................................................................................................................... 59

6.1.1 Occupational exposure to radon in Australia ........................................ 59

6.1.2 Residential exposure to radon in Australia .............................................. 60

6.2 Results ............................................................................................................................. 73

6.2.1 Occupational radon exposure and risk of lung cancer....................... 73

6.2.2 Occupational radon exposure and risk of lung cancer: Joint

effects with smoking .................................................................................... 74

6.2.3 Residential radon exposure and risk of lung cancer ............................. 76

6.2.4 Residential radon exposure and risk of lung cancer in Europe .......... 76

6.2.5 Residential radon exposure and risk of lung cancer in the US ............ 77

6.2.6 Residential radon exposure and risk of lung cancer in China ............ 77

6.2.7 Level of residential radon exposure and risk of lung cancer .............. 78

Risk factors for lung cancer: A systematic review iv

6.2.8 Residential radon exposure, smoking status and risk of lung

cancer ............................................................................................................ 78

6.2.9 Residential radon exposure, gender and risk of lung cancer ............. 79

6.3 Summary ........................................................................................................................ 80

6.4 Conclusion ..................................................................................................................... 80


6.4.2 Risk assessment ............................................................................................. 80

6.5 Methodology quality of studies ................................................................................. 82

7 Risk factor: Arsenic exposure ............................................................................................. 87

7.1 Introduction ................................................................................................................... 87

7.2 Results ............................................................................................................................. 94

7.2.1 Inhalational arsenic exposure and risk of lung cancer ......................... 94

7.2.2 Smelter workers and living near smelters ................................................. 95

7.2.3 Miners .............................................................................................................. 99

7.2.4 Smelter workers and miners ...................................................................... 102

7.2.5 Fertiliser manufacturing plant, stoking, pesticide and refinery

workers .......................................................................................................... 102

7.2.6 Inhalational arsenic exposure and risk of lung cancer by

smoking status ............................................................................................. 104

7.2.7 Inhalational arsenic exposure and risk of lung cancer by

gender .......................................................................................................... 105

7.2.8 Ingested arsenic exposure (drinking water) and risk of lung

cancer .......................................................................................................... 106


cancer by smoking status ......................................................................... 108


cancer by gender ...................................................................................... 109

7.3 Summary ...................................................................................................................... 109

7.4 Conclusion ................................................................................................................... 110

7.4.1 Hazard identification ................................................................................. 110

7.4.2 Risk assessment ........................................................................................... 111

Methodological quality of studies ........................................................................................ 112

8 Risk factor: Polycyclic aromatic hydrocarbons (PAHs) ................................................ 115

8.1 Introduction ................................................................................................................. 115

8.2 Results ........................................................................................................................... 123

8.2.1 Occupational exposure to PAH and risk of lung cancer ................... 123

8.2.2 Occupational PAH exposure and risk of lung cancer in coal

gasification workers ................................................................................... 125

8.2.3 Occupational exposure to PAHs and risk of lung cancer in

coke production workers .......................................................................... 127

8.2.4 Occupational PAH exposure and risk of lung cancer in

creosote workers ........................................................................................ 128


aluminium production workers ................................................................ 128


chimney sweeps and in workers exposed to soot ............................... 130

8.2.7 Occupational PAH exposure, smoking status and risk of lung

cancer .......................................................................................................... 130

8.2.8 Occupational PAH exposure, gender and risk of lung cancer ........ 131

8.3 Summary ...................................................................................................................... 132

8.4 Conclusion ................................................................................................................... 132


8.4.2 Risk assessment ........................................................................................... 132

8.5 Methodological quality of studies .......................................................................... 133

9 Risk factor: Family history .................................................................................................. 136

9.1 Introduction ................................................................................................................. 136

9.2 Results ........................................................................................................................... 139

9.2.1 Family history and risk of lung cancer .................................................... 139

9.2.2 Family history, smoking status and risk of lung cancer ........................ 139

9.2.3 Family history, gender and risk of lung cancer ..................................... 140

9.2.4 Risk of lung cancer by family member affected ................................. 140

9.3 Summary ...................................................................................................................... 140

9.4 Conclusion ................................................................................................................... 141


Risk factors for lung cancer: A systematic review vi

9.4.2 Risk assessment ........................................................................................... 141


10 Risk factor: Iron and steel founding ................................................................................. 144

10.1 Introduction ................................................................................................................. 144

10.2 Results ........................................................................................................................... 148

10.2.1 Overall risk of lung cancer in iron and steel foundry workers ............ 148

10.2.2 Risk of lung cancer for workers in iron and steel foundries, by

exposure to specific agents ..................................................................... 149

10.2.3 Risk of lung cancer in iron and steel foundry workers, by job

category ...................................................................................................... 150

10.2.4 Risk of lung cancer in iron and steel foundry workers, by

duration of employment ........................................................................... 151

10.2.5 Risk of lung cancer in iron and steel foundry workers by

smoking status ............................................................................................. 153

10.2.6 Risk of lung cancer in iron and steel foundry workers by gender ..... 154

10.3 Summary ...................................................................................................................... 154

10.4 Conclusion ................................................................................................................... 155


10.4.2 Risk assessment ........................................................................................... 155

10.5 Methodological quality of included studies ......................................................... 156

11 Risk factor: Silica exposure ............................................................................................... 158

11.1 Introduction ................................................................................................................. 158

11.2 Results ........................................................................................................................... 167

11.2.1 Occupational silica exposure and risk of lung cancer ....................... 167

11.2.2 Duration of silica exposure and risk of lung cancer ............................ 170

11.2.3 Intensity of silica exposure and risk of lung cancer ............................. 171

11.2.4 Silica exposure and risk of lung cancer in people with silicosis ......... 172

11.2.5 Silica exposure, smoking status and risk of lung cancer ..................... 174

11.3 Summary ...................................................................................................................... 174

11.4 Conclusion ................................................................................................................... 175


11.4.2 Risk assessment ........................................................................................... 175


12 Risk factor: Nickel exposure ............................................................................................. 179

12.1 Introduction ................................................................................................................. 179

12.2 Results ........................................................................................................................... 187

12.2.1 Occupational nickel exposure and risk of lung cancer ..................... 187

12.2.2 Duration of nickel exposure and risk of lung cancer .......................... 188

12.2.3 Cumulative exposure to nickel ................................................................ 188

12.2.4 Occupational nickel exposure, smoking status and risk of lung

cancer .......................................................................................................... 189

12.2.5 Occupational nickel exposure, type of nickel compound and

risk of lung cancer ...................................................................................... 190

12.3 Summary ...................................................................................................................... 191

12.4 Conclusion ................................................................................................................... 191


12.4.2 Risk assessment ........................................................................................... 191


13 Risk factor: Painting as an occupation ............................................................................ 194

13.1 Introduction ................................................................................................................. 194

13.2 Results ........................................................................................................................... 200

13.2.1 Overall lung cancer risk associated with any duration of work

as a painter/various levels of exposure ................................................. 200

13.2.2 Wood and gypsum paints and overall risk of lung cancer ................ 201

13.2.3 Dose response for painting as an occupation and lung cancer

risk .................................................................................................................. 202

13.2.4 Risk of lung cancer from occupational exposure to paint by

gender .......................................................................................................... 203

13.3 Summary ...................................................................................................................... 203

13.4 Conclusion ................................................................................................................... 204


13.4.2 Risk assessment ........................................................................................... 205

Risk factors for lung cancer: A systematic review viii


14 Risk factor: Cadmium exposure ....................................................................................... 209

14.1 Introduction ................................................................................................................. 209

14.2 Results ........................................................................................................................... 215

14.2.1 Occupational exposure to cadmium and risk of lung cancer ......... 215

14.2.2 Duration and intensity of occupational cadmium exposure

and risk of lung cancer ............................................................................. 217

14.2.3 Residential exposure to cadmium and risk of lung cancer ............... 221

14.2.4 Cadmium exposure, smoking status and risk of lung cancer............ 222

14.3 Summary ...................................................................................................................... 222

14.4 Conclusion ................................................................................................................... 223


14.4.2 Risk assessment ........................................................................................... 224


15 Risk factor: Air pollution ..................................................................................................... 228

15.1 Introduction ................................................................................................................. 228

15.2 Results ........................................................................................................................... 235

15.2.1 Risk of lung cancer associated with exposure to fine

particulate matter (PM2.5) ......................................................................... 235

15.2.2 Risk of lung cancer associated with exposure to fine

particulate matter (PM2.5) and gender .................................................. 235

15.2.3 Risk of lung cancer associated with exposure to sulphur

dioxide (SO2) ............................................................................................... 236

15.2.4 Risk of lung cancer associated with exposure to sulphur

dioxide (SO2) and gender ........................................................................ 236

15.2.5 Risk of lung cancer associated with exposure to nitrogen

dioxide (NO2)............................................................................................... 237


oxides (NOx) ................................................................................................. 237


oxides (NOx) and smoking status. ........................................................... 237

15.2.8 Risk of lung cancer associated with exposure to vehicular

traffic ............................................................................................................. 238

15.2.9 Risk of lung cancer associated with exposure to vehicular

traffic and smoking status ......................................................................... 239

15.3 Summary ...................................................................................................................... 239

15.4 Conclusion ................................................................................................................... 240


15.4.2 Risk assessment ........................................................................................... 240


16 Risk factor: Chromium exposure ...................................................................................... 244

16.1 Introduction ................................................................................................................. 244

16.2 Results ........................................................................................................................... 251

16.2.1 Occupational exposure to chromium and risk of lung cancer ........ 251

16.2.2 Duration of chromium exposure and risk of lung cancer................... 253

16.2.3 Chromium exposure, smoking status and risk of lung cancer ........... 254

16.3 Summary ...................................................................................................................... 254

16.4 Conclusion ................................................................................................................... 255


16.4.2 Risk assessment ........................................................................................... 255


17 Risk factor: Beryllium exposure ........................................................................................ 258

17.1 Introduction ................................................................................................................. 258

17.2 Results ........................................................................................................................... 267

17.2.1 Occupational beryllium exposure and overall risk of lung

cancer .......................................................................................................... 267

17.2.2 Dose response for occupational beryllium exposure and risk of

lung cancer ................................................................................................. 270

17.2.3 Beryllium exposure, gender, smoking status and risk of lung

cancer .......................................................................................................... 271

17.3 Summary ...................................................................................................................... 271

17.4 Conclusion ................................................................................................................... 272


17.4.2 Risk assessment ........................................................................................... 272

Risk factors for lung cancer: A systematic review x


18 Risk factor: Red meat and processed meat consumption ........................................... 276

18.1 Introduction ................................................................................................................. 276

18.2 Results ........................................................................................................................... 284

18.2.1 Red meat consumption and overall risk of lung cancer .................... 284

18.2.2 Red meat consumption, smoking status and risk of lung cancer .... 285

18.2.3 Red meat consumption and risk of lung cancer by gender ............. 287

18.2.4 Processed meat consumption and risk of lung cancer ...................... 288

18.2.5 Processed meat consumption, smoking status and risk of lung

cancer .......................................................................................................... 289

18.2.6 Processed meat consumption and risk of lung cancer by

gender .......................................................................................................... 290

18.3 Summary ...................................................................................................................... 290

18.4 Conclusion ................................................................................................................... 291


18.4.2 Risk assessment ........................................................................................... 291

18.5 Methodology quality of studies ............................................................................... 292

19 Risk factor: Alcohol consumption .................................................................................... 296

19.1 Introduction ................................................................................................................. 296

19.2 Results ........................................................................................................................... 306

19.2.1 Alcohol consumption and risk of lung cancer in the general

population ................................................................................................... 306

19.2.2 Alcohol consumption, smoking status and risk of lung cancer ......... 307

19.2.3 Alcohol consumption, gender and lung cancer risk .......................... 308

19.2.4 Types of alcoholic beverage consumed and risk of lung

cancer .......................................................................................................... 309

19.2.5 Alcohol consumption and risk of lung cancer in alcoholics .............. 310

19.3 Summary ...................................................................................................................... 311

19.4 Conclusion ................................................................................................................... 311


19.4.2 Risk assessment ........................................................................................... 312


20 Risk factor: Dietary cholesterol and blood cholesterol ................................................. 318

20.1 Introduction ................................................................................................................. 318

20.2 Results ........................................................................................................................... 328

20.2.1 Dietary cholesterol intake and overall risk of lung cancer ................ 328

20.2.2 Risk of lung cancer and dietary cholesterol intake by smoking

status ............................................................................................................. 328

20.2.3 Dietary cholesterol intake, gender and risk of lung cancer .............. 329

20.3 Risk of lung cancer and blood cholesterol concentration ................................ 332

20.4 Risk of lung cancer and blood cholesterol by gender ....................................... 332

20.5 Summary ...................................................................................................................... 334

20.5.1 Dietary cholesterol and risk of lung cancer .......................................... 334

20.5.2 Blood cholesterol concentration and risk of lung cancer ................. 334

20.6 Conclusion ................................................................................................................... 334


20.6.2 Risk assessment ........................................................................................... 334


21 Risk factor: Avian exposure .............................................................................................. 342

21.1 Introduction ................................................................................................................. 342

21.2 Results ........................................................................................................................... 345

21.2.1 Avian exposure and risk of lung cancer ................................................ 345

21.2.2 Duration of avian exposure and risk of lung cancer ........................... 346

21.2.3 Avian exposure, smoking status and risk of lung cancer ................... 346

21.2.4 Avian exposure, gender and risk of lung cancer ................................ 346

21.3 Summary ...................................................................................................................... 347

21.4 Conclusion ................................................................................................................... 347


21.4.2 Risk assessment ........................................................................................... 348


22 Risk factor: Wood dust ....................................................................................................... 351

Risk factors for lung cancer: A systematic review xii

22.1 Introduction ................................................................................................................. 351

22.2 Results ........................................................................................................................... 360

22.2.1 Wood dust exposure and risk of lung cancer ....................................... 360

22.2.2 Wood dust exposure and risk of lung cancer by gender .................. 360

22.2.3 Wood dust exposure and risk of lung cancer by smoking status ..... 361

22.2.4 Dose response relationship between wood dust exposure and

lung cancer ................................................................................................. 361

22.3 Summary ...................................................................................................................... 362

22.4 Conclusion ................................................................................................................... 362

22.4.1 Hazard Identification ................................................................................. 362

22.4.2 Risk assessment ........................................................................................... 363

22.5 Methodological quality of included studies ......................................................... 364

23 Risk factor: Physical activity.............................................................................................. 367

23.1 Introduction ................................................................................................................. 367

23.2 Results ........................................................................................................................... 372

23.2.1 Physical activity and risk of lung cancer ............................................... 372

23.2.2 Physical activity, gender and risk of lung cancer ................................ 373

23.2.3 Physical activity, smoking status and risk of lung cancer ................... 375

23.3 Summary ...................................................................................................................... 376

23.4 Conclusion ................................................................................................................... 376


23.4.2 Risk assessment ........................................................................................... 376


24 References .......................................................................................................................... 381

25 Appendices ........................................................................................................................ 413

25.1 Appendix A NHMRC Levels of Evidence19 – Aetiology ...................................... 413

25.2 Appendix B Search history ....................................................................................... 414

25.2.1 PubMed Cancer Lit .................................................................................... 414

25.2.2 Embase ......................................................................................................... 417

25.2.3 Lung Cancer search histories (minor databases) ................................ 420

JBI Library (1998 – 28/03/2011) ................................................................................. 420

Bandolier (1995 - 28/03/2011) .................................................................................. 420

Index to Theses (1970 – 29/03/2011) ....................................................................... 420

Fade: The Northwest Grey literature Service ........................................................ 420

The Networked digital library of Theses and Dissertations (1900-2012) ............ 421

Scirus ETD.. .................................................................................................................... 421

VTLS visualiser ............................................................................................................... 421

Australian Digital Theses ............................................................................................ 421

DART-Europe E-theses Portal .................................................................................... 421

25.3 Appendix C Critical appraisal instruments ........................................................... 422

25.3.1 JBI Critical Appraisal Checklist for Comparable Cohort/ Case

Control .......................................................................................................... 422

25.3.2 JBI Critical Appraisal Checklist for Systematic Reviews ...................... 423

25.4 Appendix D Excluded studies ................................................................................. 424

25.4.1 Risk factor – Asbestos ................................................................................. 424

25.4.2 Risk factor – Avian exposure .................................................................... 425

25.4.3 Risk factor – Red meat and processed meat consumption .............. 425

25.4.4 Risk factor – Family history ......................................................................... 426

25.4.5 Risk factor – Wood dust ............................................................................. 426

25.5 Appendix E Tables of included studies ................................................................. 428

25.5.1 Air Pollution .................................................................................................. 428

25.5.2 Alcohol Consumption ................................................................................ 432

25.5.3 Arsenic exposure ........................................................................................ 440

25.5.4 Asbestos ....................................................................................................... 445

25.5.5 Avian Exposure ........................................................................................... 453

25.5.6 Beryllium exposure ...................................................................................... 455

25.5.7 Cadmium ..................................................................................................... 459

25.5.8 Chromium IV ................................................................................................ 466

25.5.9 Dietary Cholesterol and Blood Cholesterol ........................................... 471

25.5.10 Family history ............................................................................................... 482

Risk factors for lung cancer: A systematic review xiv

25.5.11 Iron and Steel .............................................................................................. 483

25.5.12 Red Meat and Processed Meat Consumption .................................... 486

25.5.13 Nickel ............................................................................................................ 495

25.5.14 Polycyclic Aromatic Hydrocarbons (PAH) exposure ........................... 501

25.5.15 Painting as an occupation ....................................................................... 507

25.5.16 Physical Activity .......................................................................................... 511

25.5.17 Radon ........................................................................................................... 515

25.5.18 Silica .............................................................................................................. 527

25.5.19 Smoking: Active and passive smoking ................................................... 533

25.5.20 Wood Dust ................................................................................................... 540

Tables

Table 3.1 Summary of results of database searching, papers retrieved based on

eligibility criteria and number of included studies ..................................................... 16

Table 4.1 Study characteristics relevant to the association between smoking and

lung cancer ....................................................................................................................... 19

Table 4.2 Risk of lung cancer due to smoking in current and former smokers.

Referent category of never smokers31 ......................................................................... 26

Table 4.3 Differences in RR estimate of lung cancer in current smokers dependent

on the study design used31 ............................................................................................. 26

Table 4.4 Dose response RR estimates for lung cancer in current smoking men and

women31 ............................................................................................................................ 27

Table 4.5 Risk of lung cancer with workplace exposure to environmental tobacco

smoke32 .............................................................................................................................. 27

Table 4.6 Relative risk of lung cancer in never smoking men alone and both

genders when exposed to environmental smoke from their spouse33 .................. 28

Table 4.7 Second hand smoke (ETS) exposure during childhood and risk of lung

cancer34 ............................................................................................................................. 28

Table 4.8 Active smoking and passive smoking: Methodological quality of

included studies ............................................................................................................... 31

Table 5.1 Study characteristics relevant to the association between asbestos

exposure and lung cancer ............................................................................................ 36

Table 5.2 Risk estimates of lung cancer due to occupational asbestos exposure –

Mining worker cohort studies, IARC monograph 40 ................................................... 42

Table 5.3 Occupational asbestos exposure and risk estimates of lung cancer from

manufacturing worker cohort studies, IARC monograph40 unless

otherwise stated ............................................................................................................... 42

Table 5.4 Relative risk estimates of lung cancer due to occupational asbestos

exposure – Case controls with exposure measured in number of years,

IARC monograph40 .......................................................................................................... 45

Table 5.5 Case controls with exposure measured in number of hours, IARC

monograph40 .................................................................................................................... 46

Table 5.6 Risk estimates of lung cancer due to occupational asbestos exposure –

case-controls with categorical exposure, IARC monograph40 unless

otherwise stated ............................................................................................................... 47

Risk factors for lung cancer: A systematic review xvi

Table 5.7 Non-occupational asbestos exposure and risk of lung cancer, IARC

monograph40 .................................................................................................................... 49

Table 5.8 Asbestos exposure, gender and risk of lung cancer , IARC monograph40 ........... 50

Table 5.9 Occupational exposure to asbestos, smoking status and risk of lung

cancer ................................................................................................................................ 50

Table 5.10 Asbestosis and risk of lung cancer ................................................................................ 52

Table 5.11 Asbestos exposure: Methodological quality of included studies .......................... 56

Table 6.1 Study characteristics relevant to the association between radon


Table 6.2 Occupational radon exposure and risk of lung cancer in Europe (cohort

studies) ............................................................................................................................... 73

Table 6.3 Level of occupational radon exposure and risk of lung cancer in German

uranium miners, (Schnelzer et al. 2010)69 ..................................................................... 73

Table 6.4 Occupational radon exposure and risk of lung cancer in haematite/iron

miners, IARC monograph55 ............................................................................................ 74

Table 6.5 Occupational radon exposure and risk of lung cancer in Swedish iron ore

miners, (Jonsson et al. 2010) .......................................................................................... 74

Table 6.6 Occupational radon exposure, smoking and risk of lung cancer in miners,

IARC monograph 55 ......................................................................................................... 75

Table 6.7 Occupational radon exposure and risk of lung cancer in German

uranium miners: risk to smokers compared with non-smokers, (Schnelzer

et al. 2010)69 ...................................................................................................................... 75

Table 6.8 Occupational radon exposure, smoking status and risk of lung cancer in

German, French and Czech uranium miners, Leuraud et al. 201171 ..................... 75

Table 6.9 Residential radon exposure and risk of lung cancer, IARC monograph55 ........... 76

Table 6.10 Duration of residential radon exposure in Germany, (Kreutzer et al. 2003) 72 .......................................................................................................................................... 77

Table 6.11 Residential radon exposure and risk of lung cancer in the US, ( Krewski et

al. 2005)66 ........................................................................................................................... 77

Table 6.12 Residential radon exposure and lung cancer risk in China,(Lubin et al.

2004)73................................................................................................................................. 77

Table 6.13 Residential radon exposure and risk of lung cancer - a synthesis of data

from different exposure levels, (Pavia et al. 2003)75 .................................................. 78

Table 6.14 Residential radon exposure, smoking status and risk of lung cancer in

Sweden, (Lagarde et al. 2001) ...................................................................................... 78

Table 6.15 Residential radon exposure of 100 Bq/m3 for at least five years, smoking

status and risk of lung cancer, (Lubin et al. 2004) ..................................................... 79

Table 6.16 Residential radon exposure, gender and risk of lung cancer in Italy (Pisa

et al. 2001) ......................................................................................................................... 79

Table 6.17 Radon exposure: Methodological quality of included studies .............................. 82

Table 7.1 Study characteristics relevant to the association between arsenic


Table 7.2 Risk estimates for ever exposed versus non-exposed, before and after

adjustment for metals and other occupational exposures (‘t Mannetje et

al. 2011) .............................................................................................................................. 94

Table 7.3 Risk estimates for lung cancer according to exposure-response analyses

for arsenic dust and arsenic fumes/mist in terms of duration (years) (‘t

Mannetje et al. 2011) ...................................................................................................... 94

Table 7.4 Risk estimates of lung cancer due to occupational arsenic exposure –

Smelter studies; IARC monograph80 unless otherwise stated .................................. 96


Mining studies, IARC monograph80 unless otherwise stated ................................... 99

Table 7.6 Risk of lung cancer, by occupation in smelters or mines ....................................... 102


Fertilisation plant, stoking, pesticides and refinery studies, IARC

monograph80 unless otherwise stated ....................................................................... 103

Table 7.8 Risk estimates for lung cancer due to arsenic exposure among men living

near arsenic-emitting smelters, by smoking status (Pershagen et al. 1985) ....... 104

Table 7.9 Cumulative air arsenic exposure index* (CAAEI) in all male primary

smelter workers and in primary smelter workers who were current smokers

(Lundstrom et al. 2006) .................................................................................................. 105

Table 7.10 Age-adjusted relative risks for ever and current tobacco use in male tin

miners at high risk for lung cancer (Qiao et al. 1997) ............................................. 105

Table 7.11 Lung cancer mortality in male and female workers .............................................. 106

Table 7.12 Risk estimates of lung cancer due to arsenic exposure from drinking

water, IARC monograph 80 unless otherwise stated ............................................... 107

Table 7.13 Risk estimates for lung cancer mortality according to arsenic

concentration of well water, by smoking status (Tsuda et al. 1989) .................... 108

Risk factors for lung cancer: A systematic review xviii

Table 7.14 Risk of lung cancer and exposure to arsenic in drinking water by smoking

status ................................................................................................................................. 108

Table 7.15 Risk of lung cancer and exposure to arsenic in drinking water in males

and females, IARC monograph80 ............................................................................... 109

Table 7.16 Arsenic exposure: Methodological quality of included studies .............................. 112

Table 8.1 Study characteristics relevant to the association between PAH exposure

and lung cancer ............................................................................................................ 117

Table 8.2 Overall SMR and pooled RR with 95% CI for exposure to PAH in various

industries and occupations96 ....................................................................................... 123

Table 8.3 Risk estimates for lung cancer from occupational exposure to PAHs ................. 124

Table 8.4 Occupational exposure to PAHs and risk of lung cancer in coal

gasification workers ....................................................................................................... 126

Table 8.5 Occupational PAH exposure and risk of lung cancer in coke production

workers ............................................................................................................................. 127

Table 8.6 Occupational PAH exposure and risk of lung cancer in creosote workers.

(Tornqvist et al. 1986) ..................................................................................................... 128

Table 8.7 Occupational PAH exposure and risk of lung cancer in aluminium

production workers ........................................................................................................ 129

Table 8.8 Occupational PAH exposure, smoking status and risk estimates for lung

cancer .............................................................................................................................. 131

Table 8.9 Occupational PAH exposure, gender and hazard ratio and 95% CI for

lung cancer 103 ................................................................................................................ 131

Table 8.10 PAH exposure: Methodological quality of included studies ................................ 133

Table 9.1 Study characteristics relevant to the association between family history

and lung cancer ............................................................................................................ 137

Table 9.2 Pooled analysis of the overall risk of lung cancer associated with family

history114............................................................................................................................ 139

Table 9.3 Risk of lung cancer associated with family history, by smoking status –

and affected family member (case-control) ........................................................... 139

Table 9.4 Family history and the risk of lung cancer by gender,114 ........................................ 140

Table 9.5 Risk of lung cancer associated with family history, by family member

type, from the Lissowska et al. (2010) 114 case-control study ................................. 140

Table 9.6 Family history: Methodological quality of included studies .................................. 142

Table 10.1 Study characteristics relevant to the association between iron and steel

founding and lung cancer ........................................................................................... 145

Table 10.2 Iron and steel foundry workers and overall risk of lung cancer ............................ 148

Table 10.3 Risk estimates of lung cancer in iron and steel foundry workers, by

specific exposure to silica and formaldehyde124 ..................................................... 149

Table 10.4 Risk estimates of lung cancer in iron and steel foundry workers, by job

category .......................................................................................................................... 150

Table 10.5 Risk of lung cancer in iron and steel foundry workers, by duration of

employment, IARC monograph108 ............................................................................. 152

Table 10.6 Risk of lung cancer in iron and steel foundry workers, by smoking status........... 153

Table 10.7 Risk of lung cancer in iron and steel foundry workers; by gender and job,

(Ahn et al. 2010) ............................................................................................................. 154

Table 10.8 Iron and steel founding: Methodological quality of included studies ................ 156

Table 11.1 Study characteristics relevant to the association between silica exposure

and lung cancer ............................................................................................................ 160

Table 11.2 Overall risk of lung cancer associated with exposure to silica ............................. 167

Table 11.3 Risk estimates of lung cancer due to occupational silica exposure – Ore

mining; cohort & case-control studies, IARC Monograph (1997)128 ..................... 168

Table 11.4 Risk estimates of lung cancer due to occupational silica exposure –

Ceramics, pottery, refractory brick and diatomaceous earth; cohort &

case-control studies, IARC Monograph (1997)128 .................................................... 169

Table 11.5 Risk estimates of lung cancer due to occupational silica exposure –

Quarries and granite production and foundry workers; IARC Monograph

(1997)128 ............................................................................................................................ 170

Table 11.6 Duration of silica exposure and risk of lung cancer ................................................ 171

Table 11.7 Cumulative silica exposure and risk of lung cancer ............................................... 171

Table 11.8 Intensity of silica exposure and risk of lung cancer ................................................. 171

Table 11.9 Lung cancer risk associated with silica exposure in silicotic patients .................. 173

Table 11.10 Risk estimates of lung cancer due to occupational silica exposure in

silicotics, case-control studies, IARC Monograph (1997)128 ................................... 174

Table 11.11 Silica exposure, smoking status and risk of lung cancer135 .................................... 174

Table 11.12 Silica exposure: Methodological quality of included studies ............................... 176

Risk factors for lung cancer: A systematic review xx

Table 12.1 Study characteristics relevant to the association between nickel

exposure and lung cancer .......................................................................................... 181

Table 12.2 Occupational exposure to nickel and overall lung cancer risk; all studies

included in the IARC monograph139 except for where denoted......................... 187

Table 12.3 Duration of nickel exposure and risk of lung cancer .............................................. 188

Table 12.4 Cumulative exposure to water soluble nickel and Ni oxide and risk of lung

cancer; IARC 2012.139 .................................................................................................... 188

Table 12.5 Risk resulting from exposure to nickel and smoking status ..................................... 189

Table 12.6 Type of nickel compound and lung cancer risk, (Grimsrud et al. 2002) ............. 190

Table 12.7 Nickel exposure: Methodological quality of included studies .............................. 192

Table 13.1 Study characteristics relevant to the association between painting as an

occupation and lung cancer ..................................................................................... 196

Table 13.2 Overall lung cancer risk for painting as an occupation, any duration ............... 200

Table 13.3 Lung cancer risk for exposure to wood and gypsum paints,

(Ramanakumar et al. 2011)157 ..................................................................................... 202

Table 13.4 RR of lung cancer and occupational exposure to paint by duration of

employment, (Guha et al. 2010)153 ............................................................................ 202

Table 13.5 Lung cancer risk for general painting work (not spraying) and spray

painting in Chinese non-smoking men by duration of employment (Tse et

al. 2011) ............................................................................................................................ 202

Table 13.6 Lung cancer risk for painting as an occupation and exposure to wood

and gypsum paints by duration of employment157................................................. 203

Table 13.7 Lung cancer risk for painting as an occupation by gender153 ............................. 203

Table 13.8 Painting as an occupation: Methodological quality of included studies .......... 206

Table 14.1 Study characteristics relevant to the association between cadmium


Table 14.2 Risk estimates of lung cancer due to occupational cadmium exposure;

research synthesis148 ...................................................................................................... 215

Table 14.3 Risk estimates of lung cancer due to occupational exposure to

cadmium, case-control study (t Mannetje et al. 2011)92 ....................................... 215

Table 14.4 Risk estimates of lung cancer due to occupational cadmium exposure,

cohort studies – IARC monograph160 ......................................................................... 216

Table 14.5 Duration of occupational cadmium exposure and risk of lung cancer ............. 220

Table 14.6 Risk of lung cancer resulting from occupational cadmium exposure by

weighted duration or cumulative exposure (t Mannetje et al. 2011)92 ............... 220

Table 14.7 Risk of lung cancer from occupational cadmium exposure, by exposure

intensity ............................................................................................................................ 221

Table 14.8 Residential cadmium exposure and risk of lung cancer ........................................ 222

Table 14.9 Risk of lung cancer resulting from any level of cadmium exposure in non-

smokers vs smokers ........................................................................................................ 222

Table 14.10 Cadmium exposure: Methodological quality of included studies ...................... 225

Table 15.1 Study characteristics relevant to the association between air pollution

and lung cancer ............................................................................................................ 230

Table 15.2 Risk of lung cancer associated with exposure to fine particulate matter

(PM2.5) ............................................................................................................................. 235

Table 15.3 Risk of lung cancer associated with exposure to fine particulate matter

(PM2.5) and gender, (Chen et al.)188 ......................................................................... 236

Table 15.4 Sulphur dioxide (SO2) exposure and risk of lung cancer ........................................ 236

Table 15.5 Risk of lung cancer associated with exposure to sulphur dioxide (SO2)

and gender, (Chen et al. 2008) .................................................................................. 236

Table 15.6 Risk of lung cancer associated with exposure to nitrogen dioxide (NO2) .......... 237

Table 15.7 Risk of lung cancer associated with exposure to nitrogen oxides (NOx) ........... 237

Table 15.8 Risk of lung cancer associated with a 20yr exposure to nitrogen oxides

(NOx) and smoking status, (Raaschou-Nielsen et al.)194 ........................................ 238

Table 15.9 Risk of lung cancer associated with a 20 yr exposure to nitrogen oxides

(NOx) and gender, (Raaschou-Nielsen et al.)194 ..................................................... 238

Table 15.10 Risk of lung cancer associated with exposure to vehicular traffic ....................... 238

Table 15.11 Risk of lung cancer associated with exposure to vehicular traffic and

smoking status195............................................................................................................. 239

Table 15.12 Air pollution: Methodological quality of included studies ..................................... 242

Table 16.1 Study characteristics relevant to the association between chromium (VI)


Table 16.2 Risk estimates of lung cancer due to occupational Cr VI exposure,

research syntheses ......................................................................................................... 251

Table 16.3 Risk estimates of lung cancer due to occupational Cr VI exposure,

cohort studies - IARC monograph (2012f) and Hara et al. (2010) ........................ 252

Risk factors for lung cancer: A systematic review xxii

Table 16.4 Lung cancer risk resulting from occupational Cr VI exposure - by duration ...... 253

Table 16.5 Risk of lung cancer resulting from occupational Cr VI exposure by

weighted duration or cumulative exposure, (‘t Mannetje et al 2011) ................ 253

Table 16.6 Risk of lung cancer resulting from occupational Cr VI exposure, 211 211 .............. 254

Table 16.7 Overall risk of lung cancer resulting from occupational Cr VI exposure

and smoking,148 .............................................................................................................. 254

Table 16.8 Chromium exposure: Methodological quality of included studies ..................... 256

Table 17.1 Study characteristics relevant to the association between beryllium


Table 17.2 Occupational beryllium exposure and overall risk of lung cancer ...................... 267

Table 17.3 Quantified levels of occupational beryllium exposure and overall risk of

lung cancer ..................................................................................................................... 269

Table 17.4 SMRs for lung cancer in US male beryllium workers employed 1940-1969

by latency and employment duration (Ward et al. 1992) .................................... 270

Table 17.5 Lung cancer risk estimates by cumulative occupational beryllium

exposure, (Sanderson et al. 2001)............................................................................... 270

Table 17.6 Lung cancer risk estimates by cumulative occupational beryllium

exposure (lagged 10 years), Schubauer-Berigan et al (2011a) ............................ 271

Table 17.7 Beryllium exposure: Methodological quality of included studies ........................ 273

Table 18.1 Study characteristics relevant to the association between red/processed

meat consumption and lung cancer ........................................................................ 277

Table 18.2 Red meat consumption, smoking status and risk of lung cancer ........................ 287

Table 18.3 Risk of lung cancer with processed meat consumption by smoking status

(De Stefani et al. 2009) .................................................................................................. 289

Table 18.4 Risk of lung cancer with processed meat consumption for women ................... 290

Table 18.5 Red and processed meat consumption: Methodological quality of

included studies ............................................................................................................. 292

Table 19.1 Study characteristics relevant to the association between alcohol

consumption and lung cancer ................................................................................... 298

Table 19.2 Risk of lung cancer incidence in general population by lowest and

highest alcohol intake categories .............................................................................. 307

Table 19.3 Risk ratios for alcohol consumption and lung cancer risk in non-smokers

(Korte et al. 2002) ........................................................................................................... 307

Table 19.4 Multivariate adjusted Hazard ratio for lung cancer incidence by smoking

status (Shimazu et al 2008) ........................................................................................... 307

Table 19.5 Relative risk of lung cancer in women by smoking status (Rachtan &

Sokolowski 1997) ............................................................................................................. 308

Table 19.6 Odds ratio for alcohol consumption and lung cancer risk by smoking

status (Pierce et al 1989) ............................................................................................... 308

Table 19.7 Binge drinking and risk of lung cancer according to smoking status

(Toriola et al 2009) .......................................................................................................... 308

Table 19.8 Relative risk of lung cancer among binge drinkers compared with non-

binge drinkers in men with no history of lung cancer at baseline (Toriola

et al 2009) ........................................................................................................................ 309

Table 19.9 Increased risk of lung cancer in men with increasing amount of alcohol

(Balder et al 2009) .......................................................................................................... 309

Table 19.10 Risk of lung cancer with consumption of vodka in women (Rachtan et al

1997) ................................................................................................................................. 309

Table 19.11 Relative risk for alcoholic beverage types and lung cancer risk (Chao et

al. 2007) ............................................................................................................................ 310

Table 19.12 Odds ratio for beer consumption and risk of lung cancer (Mayne et al.

1994) ................................................................................................................................. 310

Table 19.13 Alcohol consumption: Methodological quality of included studies ................... 313

Table 20.1 Study characteristics relevant to the association between cholesterol

and lung cancer ............................................................................................................ 319

Table 20.2 Risk of lung cancer and dietary cholesterol intake in quartiles of

consumption ................................................................................................................... 328

Table 20.3 Pooled multivariate-adjusted RRs and 95% CIs of lung cancer for dietary

cholesterol (for 100mg/day increases), (Smith Warner et al. 2002) ..................... 328

Table 20.4 RRs and 95% CIs of lung cancer by smoking status according to quartile

intake of dietary cholesterol among postmenopausal women (Wu et al.

1994) ................................................................................................................................. 329

Table 20.5 ORs and 95% CIs for the development of lung cancer among males, by

quartiles of cholesterol consumption, (Goodman et al. 1988) ............................. 329

Table 20.6 ORs and 95% CIs for lung cancer risk with highest quartile of cholesterol

intake compared to other quartiles in men, (Steenland et al. 1995) .................. 330

Table 20.7 Risk of lung cancer and dietary cholesterol consumption in quartiles ............... 330

Risk factors for lung cancer: A systematic review xxiv

Table 20.8 Risk of lung cancer and dietary cholesterol consumption in tertiles for

men. No CIs reported, (Shekelle et al. 1991) ............................................................ 330

Table 20.9 Risk of lung cancer and dietary cholesterol consumption in women in

quintiles ............................................................................................................................ 331

Table 20.10 Risk of lung cancer and dietary cholesterol consumption in quartiles ............... 331

Table 20.11 ORs and 95% CIs for lung cancer risk with highest quartile of cholesterol

intake compared to other quartiles in women (Steenland et al. 1995) .............. 331

Table 20.12 RRs and 95% CIs of lung cancer in relation to serum total cholesterol

(mg/dL) in quintiles (Ahn et al. 2009) ......................................................................... 332

Table 20.13 Association of plasma HDL-cholesterol quartiles with incidence of lung

cancer (RRs & 95% CIs) (Kucharska-Newton et al. 2008) ....................................... 332

Table 20.14 Lung cancer risk and serum cholesterol level (Keys et al. 1985) .......................... 333

Table 20.15 Relative Hazards and 95% CIs of lung cancer mortality by low plasma

cholesterol (

Table 22.6 Lung cancer risk among pulp and paper industry workers exposed to

wood dust by cumulative dose (Szadkowska-Stanczyk & Szymczak 2001) ....... 362

Table 22.7 Wood dust: Methodological quality of included studies ...................................... 364

Table 23.1 Study characteristics relevant to the association between physical

activity and lung cancer .............................................................................................. 368

Table 23.2 Leisure time physical activity (LPA) and lung cancer (Tardon et al. 2005) ........ 372

Table 23.3 Relative Risk of lung cancer at different levels of physical activity (Lee et

al. 1994) ............................................................................................................................ 372

Table 23.4 Relative Risk of lung cancer according to frequency of physical

activity/week (Leitzmann et al. 2009) ........................................................................ 373

Table 23.5 Lung cancer risk in women with different measures of leisure time

physical activity (LPA) (Sinner et al. 2006) ................................................................. 373

Table 23.6 Incident rate ratios (IRR) for lung cancer in relation to categories

according to time spent on each of the different types of physical

activity in leisure time (Bak et al. 2005) ...................................................................... 374

Table 23.7 Risk of lung cancer by type of physical activity (PA) and by gender

(Steindorf et al. 2006) .................................................................................................... 374

Table 23.8 Physical activity: Methodological quality of included studies ............................. 378

Risk factors for lung cancer: A systematic review xxvi

Figures

Figure 5.1 Meta-analysis of effect estimates of cohort studies presenting risk of lung

cancer with occupational exposure in crocidolite miners, IARC

monograph40 .................................................................................................................... 41


cancer with occupational exposure in manufacturing workers, IARC

monograph40 .................................................................................................................... 44


cancer with occupational exposure in shipyard, rail yard workers and

plumbers, IARC monograph40 ....................................................................................... 44

Figure 5.4 Meta-analysis of effect estimates of case control studies presenting risk of

lung cancer with occupational exposure to asbestos (a) < 7-10 years, (b)

> 8-10 years. ...................................................................................................................... 47

Figure 8.1 Occupational exposure to PAHs and risk of lung cancer, by longest

duration of exposure (≥30 years) ................................................................................ 125

Figure 8.2 Occupational exposure to PAHs and risk of lung cancer in coal

gasification workers ....................................................................................................... 126

Figure 8.3 Occupational cumulative PAH exposure (BaP) and risk of lung cancer in

aluminium production workers .................................................................................... 129

Figure 8.4 Occupational PAH exposure and risk of lung cancer in chimney sweeps

and in workers exposed to soot .................................................................................. 130

Figure 10.1 Iron and steel foundry workers and overall risk of lung cancer ............................ 149

Figure 10.2 Risk of lung cancer in iron and steel foundry workers employed for more

than 30 years ................................................................................................................... 151

Figure 10.3 Risk of lung cancer in iron and steel foundry workers employed for less

than 10 years ................................................................................................................... 152

Figure 11.1 Overall risk of lung cancer due to occupational silica exposure in workers

in ore mining industry ..................................................................................................... 168

Figure 11.2 Risk estimates of lung cancer due to occupational silica exposure in

workers in Ceramics, Pottery and Diatomaceous earth industries ...................... 169

Figure 18.1 Meta-analysis of risk of lung cancer with red meat consumption including

all cohorts ........................................................................................................................ 285

Figure 18.2 Risk of lung cancer associated with red meat consumption for men ................ 287

Figure 18.3 Red meat consumption and risk of lung cancer in women .................................. 288

Figure 18.4 Meta-analysis of risk of lung cancer with processed meat consumption in

11 included cohorts ....................................................................................................... 289

Figure 18.5 Risk of lung cancer with processed meat consumption for men ......................... 290

Figure 19.1 Meta-analysis of risk of lung cancer (RR) in individuals with high alcohol

consumption ................................................................................................................... 306

Figure 19.2 Risk of lung cancer among alcoholic male and female patients ....................... 311

Figure 20.1 Risk of lung cancer and dietary cholesterol intake by highest tertile of

consumption in men ...................................................................................................... 329

Figure 21.1 Meta-analysis of risk of lung cancer (RR) and avian exposure ............................. 345

Figure 21.2 Meta-analysis of risk of lung cancer (RR) in never smoking women from

avian exposure .............................................................................................

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