Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review
  • Published:

Biologic damage resulting from exposure to tobacco smoke and from radon: implication for preventive interventions

Oncogene volume 21, pages 7365–7375 (2002)Cite this article

Abstract

Cigarette smoking and residential radon are, respectively, the first and second leading cause of lung cancer in the United States today. Of the approximately 157 000 lung deaths occurring in 2000, approximately 90% can be attributed to cigarette smoking and 30% of the lung cancer deaths among non-smokers can be attributed to residential radon exposure. Although dwarfed by cigarette related lung cancer, lung cancer among lifetime non-smokers is a leading cause of death in the United States, and many other countries, accounting for approximately 16 000 deaths per year in the US. Laboratory studies and epidemiological investigations, particularly those conducted in the past decade, are yielding evidence that tobacco smoke and radon may share important elements of lung cancer's pathologic mechanism(s). Lung cancer prevention among smokers, ex-smokers and lifetime nonsmokers can be enhanced as we learn more about the etiologic mechanism(s) of lung cancer resulting from these and other exposures including diet, non-malignant respiratory diseases, occupational exposures, and susceptibility-gene. In this article we review both laboratory and epidemiologic data that gives insight into the biologic damage done to the lung from these exposures.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1

Similar content being viewed by others

References

  • Adams GED . 1986 Introduction to the cellular and molecular biology of cancer LM Franks and N Teich (eds) Oxford: Oxford University Press pp 154–175

    Google Scholar 

  • Alavanja MCR, Brownson RC, Benichou J, Swanson C, Boice Jr JD . 1995 Cancer Causes Control 6: 209–216

  • Alavanja MCR, Brownson RC, Boice JD, Hocke E . 1992 Am. J. Epidemiol. 136: 623–632

  • Albanes D . 1999 Am. J. Clin. Nutr. 69: 1345S–1350S

  • Ames BN . 1989 Free Radic Res. 7: 121–128

  • Aruoma OI, Halliwell B, Gajewski E, Dizarougle M . 1991 Biochem. J. 273: 601–604

  • Asami S, Hirano T, Yamaguchi R, Tomioka Y, Itoh H, Kasai H . 1996 Cancer Res. 56: 2546–2549

  • Azzam EI, de Toledo SM, Gooding T, Little JB . 1998 Radiat. Res. 150: 497–504

  • Azzam EI, de Toledo SM, Walker AJ, Little JB . 2000 Cancer Res. 60: 2623–2631

  • Bartsch H . 1996 Mutat. Res. 340: 67–69

  • Bartsch H, Hietanen E . 1996 Environ. Health Perspect. 104: 569–577

  • Bartsch H, Hollstein M, Mustonen R, Schmidt J, Spiethoff A, Wesch H, Wiehege T, Muller KM . 1995a Lancet 346: 121

  • Bartsch H, Nair J, Velic I . 1997 Eur. J. Can. Prev. 6: 529–534

  • Bartsch H, Petruzzelli S, De Flora S, Hietanen E, Camus AM, Castegnaro M, Geneste O, Camoirano R, Saracci R, Giuntini C . 1991 Mutat. Res. 250: 103–114

  • Bartsch H, Rojas M, Alexandrov K, Camus AM, Castegnaro M, Malavelli C, Anttila S, Hirvonen K, Husgafvel-Pursianinen K, Hietanen E, Vainio H . 1995b Pharmacogenetics 5: S84–S90

  • Bendich A . 1994 Pure Appl. Chem. 66: 1017–1024

  • Bessho T, Tamo K, Kasai H, Ohtsuka E, Nishimura S . 1993 J. Biol. Chem. 268: 19416–19421

  • Blot WJ, Fraumeni JF . 1996 Cancers of the lung and pleura Scottenfeld D and Fraumeni JF (eds) New York: Oxford Press pp 637–665

    Google Scholar 

  • Bohm F, Tinkler JH, Truscott TG . 1995 Nat. Med. 1: 98–99

  • Breimer LH . 1991 Free Radic. Res. Commun. 14: 159–171

  • Brenner DJ, Little JB, Sachs RK . 2001 Radiat. Res. 155: 402–408

  • Brooks AL, Newton GJ, Shyr LJ, Seller FA, Scott BR . 1990 Int. J. Radiat. Biol. 58: 799–811

  • Byers T, Perry G . 1992 Annu. Rev. Nutr. 12: 139–159

  • Candelora EC, Stockwell HG, Armstrong AW, Pinkham PA . 1992 Nutr. Cancer 17: 263–270

  • Carson DA, Ribeiro JM . 1993 Lancet 341: 1251–1254

  • Chamulitrat W, Hugh M, Eling TE, Mason RP . 1991 Arch. Biochem. Biophys. 290: 153–159

  • Cheng KC, Cahill DS, Kasai H, Nishimura S, Loeb LA . 1992 J. Biol. Chem. 267: 166–172

  • Chung FL . 1992 Cancer Chemoprevention Wattenberg L, Lipkin M, Boone CW and Kelloff GJ (eds) Boco Raton, FL: CRC Press

    Google Scholar 

  • Church DF, Pryor WA . 1985 Environ. Health Perspect. 64: 111–126

  • Cueto R, Pryor WA . 1994 Vib. Spectrosc. 7: 97–111

  • Degan P, Bonassi S, De Caterina M, Korkina LG, Pinto I, Scopacasa F, Zatterale A, Calzone R, Pagano G . 1995 Carcinogenesis 16: 735–741

  • De Kok TMCM, Vaarwerk F, Zwingman I, van Maanen JMS, Kleinjans JCS . 1994 Carcinogenesis 15: 1399–1401

  • Demple B, Harrison L . 1994 Enzymol. Biol. 63: 915–948

  • Denissenko MF, Pao A, Moon-Shong T, Pfeifer GP . 1996 Science 274: 430–432

  • Deshpande A, Goodwin EH, Bailey SM, Marrone BL, Lehnert BE . 1996 Radiat. Res. 145: 260–267

  • Di Mascio P, Kaiser S, Sies H . 1989 Arch. Biochem. Biophys. 274: 532–538

  • Dizdaroglu M . 1991 Free Radic. Biol. Med. 10: 225–242

  • Emerit I, Arutyunyan R, Oganesian N, Levy A, Cernjavsky L, Sarkisan T, Pogossian A, Asrian K . 1995 Free Radic. Biol. Med. 18: 985–991

  • Evans MD, Church DF, Pryor WA . 1991 Chem. Biol. Interact. 79: 151–164

  • Evans MD, Pryor WA . 1994 Am. J. Physiol. 266: L593–L611

  • Fahey JW, Talalay P . 1999 Food Chem. Toxicol. 37: 73–979

  • Feskanich D, Zielgler RG, Michaud DS, Giovannucci EL, Speizer FE, Willett WC, Coditz GA . 2000 J. Natl. Cancer Inst. 92: 1812–1823

  • Fraga CG, Motchink PA, Wyrobeck AJ, Rempel DM, Ames BN . 1996 Mutat. Res. 351: 199–203

  • Garcia-Closas R, Agudo A, Gonzalez CA, Riboli E . 1998 Nutr. Cancer 32: 154–158

  • Grinberg-Funes RA, Singh VN, Perera FP, Bell DA, Young TL, Dickey C, Wang LW, Santella RM . 1994 Carcinogenesis 15: 2449–2454

  • Hecht SS . 1999a J. Nutr. 129: 768S–774S

  • Hecht SS . 1999b J. Natl. Cancer Inst. 91: 1194–1210

  • Hecht SS, Chung FL, Richie Jr JP, Akerkar SA, Borukhova A, Skowronski L, Carmella SG . 1995 Cancer Epidemiol. Biomarkers Prev. 4: 877–884

  • Hei TK, Liu LX, Waldren CA . 1998 Proc. Natl. Acad. Sci. USA 95: 8103–8107

  • Hei TK, Wu LJ, Liu SX, Vannais D, Waldren CA . 1997 Proc. Natl. Acad. Sci. USA, 94: 3765–3770

  • Hickman AW, Jaramillo RJ, Lechner JF, Johnson NF . 1994 Cancer Res. 54: 5797–5800

  • Higinbotham KG, Rice JM, Diwan BA, Kaspzak KS, Reed CD, Perantoni AO . 1992 Cancer Res. 52: 4727–4751

  • Hoffmann D, Hoffmann I . 1997 J. Toxicol. Environ. Health 50: 307–364

  • Hollstein M, Bartsch H, Wesch H, Kure EH, Mustonen R, Muhlbauer HR, Spiehoff A, Wegener K, Wiethege T, Muller KM . 1997 Carcinogenesis 18: 511–516

  • Hollstein M, Sidransky D, Vogelstein B, Harris CC . 1991 Science, 253: 49–53

  • Houlston RS . 1999 Cancer Epidemiol. Biomarkers Prev. 8: 675–682

  • Hussain SP, Aguilar F, Amstad P, Cerutti P . 1994 Oncogene 9: 2277–2281

  • Hussain SP, Harris CC . 1998 Cancer Res 85: 4023–4037

  • IARC. 1986 IARC Monogr. Eval. Carcinog. Risks Hum 38: 389–394

  • Jansen MCJF, Buene-De-Mesquita HB, Leena Rasanen, Fidanza F, Nissinen AM, Menotti A, Kok FJ, Kromhout D . 2001 Int. J. Cancer 92: 913–918

  • Jeffrey AM, Jennette KW, Blobstein SH, Weinstein IB, Beland FA, Harvey RG, Kasai H, Miura I, Nakanishi K . 1976 J. Am. Chem. Soc. 98: 5714–5715

  • Jonas SK, Riley PA . 1992 Free Radic. Res. 17: 407–419

  • Kalra J, Chaudhary AK, Prasad K . 1991 Int. J. Exp. Pathol. 72: 1–7

  • Kennedy A, Symons MCR . 1997 Carcinogenesis 8: 683–688

  • Kennedy CH, Mitchell CE, Fukushima NH, Neft RE, Lechner JF . 1996 Carcinogenesis 17: 1671–1676

  • Ketterer B . 1998 Free Radic. Res 28: 647–658

  • Knekt P, Jarviven R, Tempo L, Aromaa A, Seppanen R . 1999 J Natl. Cancer Inst. 91: 182–184

  • Kolm RH, Danielson Uh, Zhang Y, Talalay P, Mannervik B . 1995 Biochem. J. 311: 453–459

  • Kriek E, Rojas M, Alexandrov K, Bartsch H . 1998 Mutat. Res. 400: 215–231

  • Krinsky NI . 1993 Annu. Rev. Nutr. 13: 561–587

  • Kuchino Y, Mori F, Kasai H, Inoue H, Iwai S, Miura K, Ohtsuka E, Nishimura S . 1987 Nature 327: 77–79

  • Landis S, Murray T, Bolden S, Wingo P . 1999 CA Cancer J. Clin. 49: 8–31

  • Leanderson P, Tagesson C . 1992 Chem. Biol. Interact. 81: 197–208

  • Lehnert B, Goodwin EH . 1997 Cancer Res. 57: 2164–2171

  • le Marchand L, Hankin JH, Kolonel LN, Beecher GR, Wilkens LR, Zhao LP . 1993 Cancer Epidemiol. Biomarkers Prev. 2: 183–187

  • Lenaz G . 1998 Biochim. Biophys. Acta 1366: 53–67

  • Little MP, Wakefield R . 2001 Radiat. Res. 156: 695–699

  • Loft S, Larsen PN . 1996 J. Mol. Med. 74: 297–312

  • Loft S, Larsen PN, Rasmussen A . 1995 Transplantation, 59: 16–20

  • Loft S, Vistisen K, Ewertz m, Tjonneland A, Overvad K, Poulsen HE . 1992 Carcinogenesis 13: 2241–2247

  • Loft S, Astrup A, Buemann B, Poulsen HE . 1994 FASEB J. 8: 534–537

  • London SJ, Yuan J-M, Chung F-L, Gao Y-T, Coetzee GA, Ross RK, Yu MC . 2000 Lancet 356: 724–729

  • Lubin JH, Boice Jr JD, Edling C . 1994 Radon and lung cancer risk: a joint analysis of 11 underground miner studies Bethesda, MD: US National Institutes of Health

  • Maynes ST, Janerich DT, Greenwald P, Chorost S, Tucci C, Zaman MB, Melamed MR, Keily M, Mckneally MF . 1994 J. Natl. Cancer Inst. 86: 33–38

  • Michaud DS, Feskanich D, Rimm EB, Colditz GA, Speizer FE, Willet WC, Giovannucci E . 2000 Am. J. Clin. Nutr. 72: 990–997

  • McDonald JW, Taylor JA, Watson MA, Saccomanno G, Devereux TR . 1995 Cancer Epidemiol. Biomarkers Prev. 4: 791–793

  • Mooney LA, Bell DA, Santella RM, van Bennekum AM, Ottman R, Paik M, Blaner WS, Lucier GW, Covey L, Young TL, Cooper TB, Glassman AH, Perera FP . 1997 Carcinogenesis 18: 503–509

  • Mooney LA, Santella RM, Covey L, Jeffrey AM, Bigbee W, Randell MC, Cooper TB, Ottman R, Tsai WY, Wazneh L, Glassman AH, Young TL, Perera FP . 1995 Cancer Epidemiol. Biomarkers Prev. 4: 627–634

  • Mortensen A, Skibsted LH . 1997 Free Radic. Res. 27: 229–234

  • National Research Council. 1999 Report of the Committee on the Biological Effects of Ionizing Radiation: Health Effects of Exposure to Radon (BEIR VI) Washington, D.C.: National Academy Press

  • Nagasawa H, Little JB . 1992 Cancer Res. 52: 6394–6396

  • Nagasawa H, Little JB . 1999 Radiat. Res. 152: 522–557

  • Nyberg F, Agrenius V, Svartengren K, Svensson C, Pershagen G . 1998 Int. J. Cancer 78: 430–436

  • Osborne MR, Beland FA, Harvey RG, Brookes P . 1976 Int. J. Cancer 18: 362–368

  • Prieme H, Loft S, Klarlund M, Gronbaek K, Tonnesen P, Poulsen H . 1998 Carcinogenesis 19: 347–351

  • Prise KM, Belyakov OV, Folkard M, Michael BD . 1998 Int. J. Radiat. Biol. 74: 793–798

  • Pryor WA . 1997 Environ. Health Perspect. 105: 875–882

  • Pryor WA, Prier DG, Church DF . 1983 Environ. Health Perspect. 47: 345–355

  • Riley PA . 1994 Int. J. Radiat. Biol. 65: 27–33

  • Roots R, Okada S . 1972 Int. J. Radiat. Biol. 21: 329–342

  • Ross TG, Goncharova ET . 1998 Mutat. Res. 402: 103–110

  • Samet JM . 1989 J. Natl. Cancer Inst. 81: 745–757

  • Sawant SG, Randers-Pherson G, Geard CR, Brenner DJ, Hall EJ . 2001 Radiat. Res. 155: 397–401

  • Slater TF . 1972 Free radical mechanisms in tissue injury London: Pion Press

    Google Scholar 

  • Speizer FE, Colditz GA, Hunter DJ, Rosner B, Hennekens C . 1999 Cancer Causes Control 10: 475–482

  • Spitz MR, Duphorne CM, Detry MA, Pillow PC, Amos CI, Lei L, de Andrade M, Gu X, Hong WK, Wu X . 2000 Cancer Epidemiol. Biomarkers Prev. 9: 1017–1020

  • Steinmetz KA, Potter JD . 1991 Cancer Causes Control 12: 427–442

  • Stone K, Bermudez E, Pyror WA . 1994 Environ. Health Perspect. 102: 173–178

  • Surgeon General. 1988 The health consequences of smoking: nicotine addiction Washington, DC: US Gov. Print

  • Taylor JA, Go VLW, Di Magno EP . 1994 Lancet 343: 86–87

  • Teebor GW, Boorstein RJ, Cadet J . 1988 Int. J. Radiat. Biol. 54: 131–150

  • United Nations Scientific Committee on the Effects of Atomic Radiation (UNSCEAR). 2000 Sources and Effects of Ionizing Radiation New York: United Nations

  • US Department of Health and Human Services. 2001 Women and Smoking. A Report of the Surgeon General US Department of Health and Human Services, Public Health Service Rockville, MD: Office of the Surgeon General

  • US Department of Health and Human Services. 1990 The Health Benefits of Smoking Cessation. A Report of the Surgeon General. US Department of Health and Human Services, Public Health Service Atlanta, GA: Office of Smoking and Health

  • Vahakangas K, Haugen A, Harris CC . 1985 Carcinogenesis 6: 1109–1116

  • Vahakangas KH, Set JM, Metcalf RA, Welsh JA, Bennett WP, Lane DP, Harris CC . 1992 Lancet 339: 576–580

  • van Lieshout EM, Ekkel MP, Bedaf MM, Nijhoff WA, Peters WH . 1998 Oncol. Res. 5: 959–963

  • van Poppel G, Verhoeven DT, Verhagen H, Goldbohm RA . 1999 Adv. Exp. Med. Biol. 472: 159–168

  • Verhagen H, de Vries A, Nijhoff WA, Shouten A, van Poppel G, Peters WH, van den Berg H . 1997 Cancer Lett. 114: 127–130

  • Verhoevan DT, Goldbohm RA, van Poppel G, Peters WH, Verhagen H, van den Brandt PA . 1996 Cancer Epidemiol. Biomarkers Prev. 5: 733–748

  • von Sonntag C . 1994 Int. J. Radiat. Biol. 65: 19–26

  • Voorrips LE, Goldblohm RA, Verhoeven DT, van Poppel GA, Sturmans F, Hermus RJ, van den Brandt PA . 2000 Cancer Causes Control 11: 101–115

  • Wei YH . 1998 Proc. Soc. Exp. Biol. Med. 217: 53–63

  • Westra WH, Slebos RJ, Offerhaus GJ, Goodman SN, Evers SG, Kensler TW . 1993 Cancer 72: 432–438

  • Williams JA . 2001 Carcinogenesis 22: 209–214

  • Wu A, Fontham E, Reynolds P . 1995 Am. J. Epidemiol. 141: 1023–1032

  • Wu LJ, Randers-Pehrson G, XU A, Waldren CA, Geard CR, Yu Z, Hei T . 1999 Proc. Natl. Acad. Sci USA 96: 4959–4964

  • Yarborough A, Zhang YJ, Hsu TM, Santella R . 1996 Cancer Res. 56: 683–688

  • Yngveson A, Williams C, Hjerpe A, Lunderberg J, Soderkvist P, Pershagen G . 1999 Cancer Epidemiol. Biomarkers Prev. 8: 433–438

  • Yu R, Mandlekar S, Harvey KJ, Ucker DS, Kong AN . 1998 Cancer Res. 58: 402–408

  • Zhao B, Seow A, Lee EJD, Poh WT, Ming The, Eng P, Wang Y-T, Tan W-C, Yu MC, Lee H-P . 2001 Cancer Epidemiol. Biomarkers Prev. 10: 1063–1067

  • Zhang LH, Cooney RV, Betram JS . 1992 Cancer Res. 52: 5702–5712

  • Zhou H, Randers-Pehrson G, Waldern CA, Vanais D, Hall EJ, Hei TK . 2000 Proc. Natl. Acad. Sci. USA 97: 2099–2104

  • Ziegler RG, Colavito EA, Hartge P . 1996a J. Natl. Cancer Inst. 88: 612–615

  • Ziegler RG, Mayne ST, Swanson CA . 1996b Cancer Causes Control 7: 157–177

Download references

Author information

Authors and Affiliations

  1. Division of Cancer Epidemiology and Genetics, National Cancer Institute, 6120 Executive Blvd., Room 8000, Rockville, 20892, Maryland, MD, USA

    Michael CR Alavanja

Authors
  1. Michael CR Alavanja
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Michael CR Alavanja.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Alavanja, M. Biologic damage resulting from exposure to tobacco smoke and from radon: implication for preventive interventions. Oncogene 21, 7365–7375 (2002). https://doi.org/10.1038/sj.onc.1205798

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/sj.onc.1205798

Keywords

This article is cited by

Search

Advanced search

Quick links