Skip to main content

Advertisement

SpringerLink
Log in

A worldwide trend of increasing primary adenocarcinoma of the lung

  • Review Article
  • Published:
Surgery Today Aims and scope Submit manuscript

Abstract

The four major histological types of lung cancer are adenocarcinoma, squamous cell carcinoma (SQ), large cell carcinoma and small cell carcinoma. Over the past few decades, the incidence of lung adenocarcinoma has increased gradually in most countries as the most frequently occurring histological type, displacing SQ. Adenocarcinoma is the predominant type of lung cancer among lifelong non-smokers and among females. Especially in East Asian countries, the cause(s) of the increase in adenocarcinomas are not clear. Several genetic mutations specific to lung adenocarcinomas have been found, representing attractive targets for molecular therapy. Recently, the pathological classification of lung adenocarcinoma was revised by integrating the newer clinical and biological knowledge concerning this prevailing type. Additional epidemiological, pathological and genetic studies are required to better understand this type of lung cancer.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Parkin DM, Bray F, Ferlay J, Pisani P. Global cancer statistics, 2002. CA Cancer J Clin. 2005;55:74–108.

    Article  PubMed  Google Scholar 

  2. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin. 2011;61:69–90.

    Article  PubMed  Google Scholar 

  3. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2012. CA Cancer J Clin. 2012;62:10–29.

    Article  PubMed  Google Scholar 

  4. Devesa SS, Bray F, Vizcaino AP, Parkin DM. International lung cancer trends by histologic type: male:female differences diminishing and adenocarcinoma rates rising. Int J Cancer. 2005;117:294–9.

    Article  CAS  PubMed  Google Scholar 

  5. Morita T. A statistical study of lung cancer in the annual of pathological autopsy cases in Japan, from 1958 to 1997, with reference to time trends of lung cancer in the world. Jpn J Cancer Res. 2002;93:15–23.

    Article  CAS  PubMed  Google Scholar 

  6. Subramanian J, Govindan R. Lung cancer in never smokers: a review. J Clin Oncol. 2007;25:561–70.

    Article  PubMed  Google Scholar 

  7. Sun Y, Ren Y, Fang Z, Li C, Fang R, Gao B, et al. Lung adenocarcinoma from East Asian never-smokers is a disease largely defined by targetable oncogenic mutant kinases. J Clin Oncol. 2010;28:4616–20.

    Article  PubMed Central  PubMed  Google Scholar 

  8. Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM. Lung cancer incidence and mortality in 2008 summary. Cancer incidence and mortality worldwide: IARC CancerBase No. 10 (Internet). International Agency for Research on Cancer. GLOBOCAN 2008 v20 2010, Lyon. http://globocan.iarc.fr/factsheets/cancers/lung.asp.

  9. Fontham ET, Correa P, Reynolds P, Wu-Williams A, Buffler PA, Greenberg RS, et al. Environmental tobacco smoke and lung cancer in nonsmoking women. A multicenter study. JAMA. 1994;271:1752–9.

    Article  CAS  PubMed  Google Scholar 

  10. Sakurai H, Asamura H, Goya T, Eguchi K, Nakanishi Y, Sawabata N, et al. Survival differences by gender for resected non-small cell lung cancer: a retrospective analysis of 12,509 cases in a Japanese Lung Cancer Registry study. J Thorac Oncol. 2010;5:1594–601.

    Article  PubMed  Google Scholar 

  11. Sawabata N, Miyaoka E, Asamura H, Nakanishi Y, Eguchi K, Mori M, et al. Japanese Joint Committee for Lung Cancer R: Japanese lung cancer registry study of 11,663 surgical cases in 2004: demographic and prognosis changes over decade. J Thorac Oncol. 2011;6:1229–35.

    Article  PubMed  Google Scholar 

  12. Sagerup CM, Smastuen M, Johannesen TB, Helland A, Brustugun OT. Sex-specific trends in lung cancer incidence and survival: a population study of 40,118 cases. Thorax. 2011;66:301–7.

    Article  PubMed  Google Scholar 

  13. Jiang X, de Groh M, Liu S, Liang H, Morrison H. Rising incidence of adenocarcinoma of the lung in Canada. Lung Cancer. 2012;78:16–22.

    Article  PubMed  Google Scholar 

  14. Chen F, Bina WF, Cole P. Declining incidence rate of lung adenocarcinoma in the United States. Chest. 2007;131:1000–5.

    Article  PubMed  Google Scholar 

  15. Au JS, Mang OW, Foo W, Law SC. Time trends of lung cancer incidence by histologic types and smoking prevalence in Hong Kong 1983–2000. Lung Cancer. 2004;45:143–52.

    Article  PubMed  Google Scholar 

  16. Gao YT, Blot WJ, Zheng W, Ershow AG, Hsu CW, Levin LI, et al. Lung cancer among Chinese women. Int J Cancer. 1987;40:604–9.

    Article  CAS  PubMed  Google Scholar 

  17. Koo LC, Ho JH. Worldwide epidemiological patterns of lung cancer in nonsmokers. Int J Epidemiol. 1990;19(Suppl 1):S14–23.

    Article  PubMed  Google Scholar 

  18. Ko YC, Lee CH, Chen MJ, Huang CC, Chang WY, Lin HJ, et al. Risk factors for primary lung cancer among non-smoking women in Taiwan. Int J Epidemiol. 1997;26:24–31.

    Article  CAS  PubMed  Google Scholar 

  19. Yu IT, Chiu YL, Au JS, Wong TW, Tang JL. Dose–response relationship between cooking fumes exposures and lung cancer among Chinese nonsmoking women. Cancer Res. 2006;66:4961–7.

    Article  CAS  PubMed  Google Scholar 

  20. Wingo PA, Ries LA, Giovino GA, Miller DS, Rosenberg HM, Shopland DR, et al. Annual report to the nation on the status of cancer, 1973–1996, with a special section on lung cancer and tobacco smoking. J Natl Cancer Inst. 1999;91:675–90.

    Article  CAS  PubMed  Google Scholar 

  21. Papadopoulos A, Guida F, Cenee S, Cyr D, Schmaus A, Radoi L, et al. Cigarette smoking and lung cancer in women: results of the French ICARE case–control study. Lung Cancer. 2011;74:369–77.

    Article  PubMed  Google Scholar 

  22. Zang EA, Wynder EL. Differences in lung cancer risk between men and women: examination of the evidence. J Natl Cancer Inst. 1996;88:183–92.

    Article  CAS  PubMed  Google Scholar 

  23. Bain C, Feskanich D, Speizer FE, Thun M, Hertzmark E, Rosner BA, et al. Lung cancer rates in men and women with comparable histories of smoking. J Natl Cancer Inst. 2004;96:826–34.

    Article  PubMed  Google Scholar 

  24. Kiyohara C, Ohno Y. Sex differences in lung cancer susceptibility: a review. Gend Med. 2010;7:381–401.

    Article  PubMed  Google Scholar 

  25. Engeland A, Haldorsen T, Andersen A, Tretli S. The impact of smoking habits on lung cancer risk: 28 years’ observation of 26,000 Norwegian men and women. Cancer Causes Control. 1996;7:366–76.

    Article  CAS  PubMed  Google Scholar 

  26. Kreuzer M, Boffetta P, Whitley E, Ahrens W, Gaborieau V, Heinrich J, et al. Gender differences in lung cancer risk by smoking: a multicentre case–control study in Germany and Italy. Br J Cancer. 2000;82:227–33.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  27. Ryberg D, Hewer A, Phillips DH, Haugen A. Different susceptibility to smoking-induced DNA damage among male and female lung cancer patients. Cancer Res. 1994;54:5801–3.

    CAS  PubMed  Google Scholar 

  28. Kure EH, Ryberg D, Hewer A, Phillips DH, Skaug V, Baera R, et al. p53 mutations in lung tumours: relationship to gender and lung DNA adduct levels. Carcinogenesis. 1996;17:2201–5.

    Article  CAS  PubMed  Google Scholar 

  29. Wei Q, Cheng L, Amos CI, Wang LE, Guo Z, Hong WK, et al. Repair of tobacco carcinogen-induced DNA adducts and lung cancer risk: a molecular epidemiologic study. J Natl Cancer Inst. 2000;92:1764–72.

    Article  CAS  PubMed  Google Scholar 

  30. Mooney LA, Perera FP, Van Bennekum AM, Blaner WS, Karkoszka J, Covey L, et al. Gender differences in autoantibodies to oxidative DNA base damage in cigarette smokers. Cancer Epidemiol Biomarkers Prev. 2001;10:641–8.

    CAS  PubMed  Google Scholar 

  31. Tang DL, Rundle A, Warburton D, Santella RM, Tsai WY, Chiamprasert S, et al. Associations between both genetic and environmental biomarkers and lung cancer: evidence of a greater risk of lung cancer in women smokers. Carcinogenesis. 1998;19:1949–53.

    Article  CAS  PubMed  Google Scholar 

  32. Guinee DG Jr, Travis WD, Trivers GE, De Benedetti VM, Cawley H, Welsh JA, et al. Gender comparisons in human lung cancer: analysis of p53 mutations, anti-p53 serum antibodies and C-erbB-2 expression. Carcinogenesis. 1995;16:993–1002.

    Article  CAS  PubMed  Google Scholar 

  33. Nelson HH, Christiani DC, Mark EJ, Wiencke JK, Wain JC, Kelsey KT. Implications and prognostic value of K-ras mutation for early-stage lung cancer in women. J Natl Cancer Inst. 1999;91:2032–8.

    Article  CAS  PubMed  Google Scholar 

  34. Shigematsu H, Lin L, Takahashi T, Nomura M, Suzuki M, Wistuba II, et al. Clinical and biological features associated with epidermal growth factor receptor gene mutations in lung cancers. J Natl Cancer Inst. 2005;97:339–46.

    Article  CAS  PubMed  Google Scholar 

  35. Cerfolio RJ, Bryant AS, Scott E, Sharma M, Robert F, Spencer SA, et al. Women with pathologic stage I, II, and III non-small cell lung cancer have better survival than men. Chest. 2006;130:1796–802.

    Article  PubMed  Google Scholar 

  36. Nakamura H, Ando K, Shinmyo T, Morita K, Mochizuki A, Kurimoto N, et al. Female gender is an independent prognostic factor in non-small-cell lung cancer: a meta-analysis. Ann Thorac Cardiovasc Surg. 2011;17:469–80.

    Article  PubMed  Google Scholar 

  37. Kawaguchi T, Matsumura A, Fukai S, Tamura A, Saito R, Zell JA, et al. Japanese ethnicity compared with Caucasian ethnicity and never-smoking status are independent favorable prognostic factors for overall survival in non-small cell lung cancer: a collaborative epidemiologic study of the National Hospital Organization Study Group for Lung Cancer (NHSGLC) in Japan and a Southern California Regional Cancer Registry databases. J Thorac Oncol. 2010;5:1001–10.

    PubMed  Google Scholar 

  38. Ou SH, Ziogas A, Zell JA. Asian ethnicity is a favorable prognostic factor for overall survival in non-small cell lung cancer (NSCLC) and is independent of smoking status. J Thorac Oncol. 2009;4:1083–93.

    Article  PubMed  Google Scholar 

  39. Nagy-Mignotte H, Guillem P, Vesin A, Toffart AC, Colonna M, Bonneterre V, et al. Primary lung adenocarcinoma: characteristics by smoking habit and sex. Eur Respir J. 2011;38:1412–9.

    Article  CAS  PubMed  Google Scholar 

  40. Grulich AE, McCredie M, Coates M. Cancer incidence in Asian migrants to New South Wales, Australia. Br J Cancer. 1995;71:400–8.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  41. Epplein M, Schwartz SM, Potter JD, Weiss NS. Smoking-adjusted lung cancer incidence among Asian-Americans (United States). Cancer Causes Control. 2005;16:1085–90.

    Article  PubMed  Google Scholar 

  42. Stellman SD, Takezaki T, Wang L, Chen Y, Citron ML, Djordjevic MV, et al. Smoking and lung cancer risk in American and Japanese men: an international case–control study. Cancer Epidemiol Biomarkers Prev. 2001;10:1193–9.

    CAS  PubMed  Google Scholar 

  43. Ando M, Wakai K, Seki N, Tamakoshi A, Suzuki K, Ito Y, et al. Attributable and absolute risk of lung cancer death by smoking status: findings from the Japan Collaborative Cohort Study. Int J Cancer. 2003;105:249–54.

    Article  CAS  PubMed  Google Scholar 

  44. Akiba S, Hirayama T. Cigarette smoking and cancer mortality risk in Japanese men and women—results from reanalysis of the six-prefecture cohort study data. Environ Health Perspect. 1990;87:19–26.

    CAS  PubMed Central  PubMed  Google Scholar 

  45. Thun MJ, Lally CA, Flannery JT, Calle EE, Flanders WD, Heath CW Jr. Cigarette smoking and changes in the histopathology of lung cancer. J Natl Cancer Inst. 1997;89:1580–6.

    Article  CAS  PubMed  Google Scholar 

  46. McLaughlin JK, Hrubec Z, Blot WJ, Fraumeni JF Jr. Smoking and cancer mortality among US veterans: a 26-year follow-up. Int J Cancer. 1995;60:190–3.

    Article  CAS  PubMed  Google Scholar 

  47. Doll R, Peto R, Wheatley K, Gray R, Sutherland I. Mortality in relation to smoking: 40 years’ observations on male British doctors. BMJ. 1994;309:901–11.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  48. Marugame T, Sobue T, Satoh H, Komatsu S, Nishino Y, Nakatsuka H, et al. Lung cancer death rates by smoking status: comparison of the Three-Prefecture Cohort study in Japan to the Cancer Prevention Study II in the USA. Cancer Sci. 2005;96:120–6.

    Article  CAS  PubMed  Google Scholar 

  49. Pesch B, Kendzia B, Gustavsson P, Jockel KH, Johnen G, Pohlabeln H, et al. Cigarette smoking and lung cancer-relative risk estimates for the major histological types from a pooled analysis of case–control studies. Int J Cancer. 2012;131:1210–9.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  50. Lynch TJ, Bell DW, Sordella R, Gurubhagavatula S, Okimoto RA, Brannigan BW, et al. Activating mutations in the epidermal growth factor receptor underlying responsiveness of non-small-cell lung cancer to gefitinib. N Engl J Med. 2004;350:2129–39.

    Article  CAS  PubMed  Google Scholar 

  51. Paez JG, Janne PA, Lee JC, Tracy S, Greulich H, Gabriel S, et al. EGFR mutations in lung cancer: correlation with clinical response to gefitinib therapy. Science. 2004;304:1497–500.

    Article  CAS  PubMed  Google Scholar 

  52. Pao W, Miller V, Zakowski M, Doherty J, Politi K, Sarkaria I, et al. EGF receptor gene mutations are common in lung cancers from “never smokers” and are associated with sensitivity of tumors to gefitinib and erlotinib. Proc Natl Acad Sci USA. 2004;101:13306–11.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  53. Yang SH, Mechanic LE, Yang P, Landi MT, Bowman ED, Wampfler J, et al. Mutations in the tyrosine kinase domain of the epidermal growth factor receptor in non-small cell lung cancer. Clin Cancer Res. 2005;11:2106–10.

    Article  CAS  PubMed  Google Scholar 

  54. Helland A, Skaug HM, Kleinberg L, Iversen ML, Rud AK, Fleischer T, et al. EGFR gene alterations in a Norwegian cohort of lung cancer patients selected for surgery. J Thorac Oncol. 2011;6:947–50.

    Article  PubMed  Google Scholar 

  55. Wu AH, Fontham ET, Reynolds P, Greenberg RS, Buffler P, Liff J, et al. Family history of cancer and risk of lung cancer among lifetime nonsmoking women in the United States. Am J Epidemiol. 1996;143:535–42.

    Article  CAS  PubMed  Google Scholar 

  56. Shiraishi K, Kunitoh H, Daigo Y, Takahashi A, Goto K, Sakamoto H, et al. A genome-wide association study identifies two new susceptibility loci for lung adenocarcinoma in the Japanese population. Nat Genet. 2012;44:900–3.

    Article  CAS  PubMed  Google Scholar 

  57. Soo RA, Loh M, Mok TS, Ou SH, Cho BC, Yeo WL, et al. Ethnic differences in survival outcome in patients with advanced stage non-small cell lung cancer: results of a meta-analysis of randomized controlled trials. J Thorac Oncol. 2011;6:1030–8.

    Article  PubMed  Google Scholar 

  58. Ginsberg R, Rubinstein L. Randomized trial of lobectomy versus limited resection for T1 N0 non-small cell lung cancer. Lung Cancer Study Group. Ann Thorac Surg. 1995;60:615–22.

    Article  CAS  PubMed  Google Scholar 

  59. Whitson BA, Groth SS, Andrade RS, Maddaus MA, Habermann EB, D’Cunha J. Survival after lobectomy versus segmentectomy for stage I non-small cell lung cancer: a population-based analysis. Ann Thorac Surg. 2011;92:1943–50.

    Article  PubMed  Google Scholar 

  60. Okada M, Yoshikawa K, Hatta T, Tsubota N. Is segmentectomy with lymph node assessment an alternative to lobectomy for non-small cell lung cancer of 2 cm or smaller? Ann Thorac Surg. 2001;71:956–60.

    Article  CAS  PubMed  Google Scholar 

  61. Koike T, Yamato Y, Yoshiya K, Shimoyama T, Suzuki R. Intentional limited pulmonary resection for peripheral T1 N0 M0 small-sized lung cancer. J Thorac Cardiovasc Surg. 2003;125:924–8.

    Article  PubMed  Google Scholar 

  62. Travis WD, Brambilla E, Noguchi M, Nicholson AG, Geisinger KR, Yatabe Y, et al. International Association for the Study of Lung Cancer/American Thoracic Society/European Respiratory Society. International multidisciplinary classification of lung adenocarcinoma. J Thorac Oncol. 2011;6:244–85.

    Article  PubMed  Google Scholar 

  63. Gealy R, Zhang L, Siegfried JM, Luketich JD, Keohavong P. Comparison of mutations in the p53 and K-ras genes in lung carcinomas from smoking and nonsmoking women. Cancer Epidemiol Biomarkers Prev. 1999;8:297–302.

    CAS  PubMed  Google Scholar 

  64. Thu KL, Vucic EA, Chari R, Zhang W, Lockwood WW, English JC, et al. Lung adenocarcinoma of never smokers and smokers harbor differential regions of genetic alteration and exhibit different levels of genomic instability. PLoS ONE. 2012;7:e33003.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  65. International Agency for Research on Cancer. Tobacco smoke and involantary smoking. IARC Monogr Eval Carcinog Risks Hum. 2004;83:1431–8.

    Google Scholar 

  66. Vineis P, Alavanja M, Buffler P, Fontham E, Franceschi S, Gao YT, et al. Tobacco and cancer: recent epidemiological evidence. J Natl Cancer Inst. 2004;96:99–106.

    Article  CAS  PubMed  Google Scholar 

  67. Lee YJ, Cho BC, Jee SH, Moon JW, Kim SK, Chang J, et al. Impact of environmental tobacco smoke on the incidence of mutations in epidermal growth factor receptor gene in never-smoker patients with non-small-cell lung cancer. J Clin Oncol. 2010;28:487–92.

    Article  CAS  PubMed  Google Scholar 

  68. Zhang Y, Sun Y, Pan Y, Li C, Shen L, Li Y, et al. Frequency of driver mutations in lung adenocarcinoma from female never-smokers varies with histologic subtypes and age at diagnosis. Clin Cancer Res. 2012;18:1947–53.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  69. Liaw YP, Ting TF, Ho KK, Yang CF. Cell type specificity of lung cancer associated with air pollution. Sci Total Environ. 2008;395:23–7.

    Article  CAS  PubMed  Google Scholar 

  70. Sisti J, Boffetta P. What proportion of lung cancer in never-smokers can be attributed to known risk factors? Int J Cancer. 2012;131:265–75.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  71. Aberle DR, Adams AM, Berg CD, Black WC, Clapp JD, Fagerstrom RM, et al. Reduced lung-cancer mortality with low-dose computed tomographic screening. N Engl J Med. 2011;365:395–409.

    Article  PubMed  Google Scholar 

  72. Bach PB, Mirkin JN, Oliver TK, Azzoli CG, Berry DA, Brawley OW, et al. Benefits and harms of CT screening for lung cancer: a systematic review. JAMA. 2012;307:2418–29.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Chest Surgery, St. Marianna University School of Medicine, 2-16-1 Sugao, Miyamae-ku, Kawasaki, Kanagawa, 216-8511, Japan

    Haruhiko Nakamura & Hisashi Saji

Authors
  1. Haruhiko Nakamura
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hisashi Saji
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Haruhiko Nakamura.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Nakamura, H., Saji, H. A worldwide trend of increasing primary adenocarcinoma of the lung. Surg Today 44, 1004–1012 (2014). https://doi.org/10.1007/s00595-013-0636-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00595-013-0636-z

Keywords

Search

Navigation