Skip to main content
Log in

Predicted lean body mass, fat mass and risk of lung cancer: prospective US cohort study

  • CANCER
  • Published:
European Journal of Epidemiology Aims and scope Submit manuscript

Abstract

An inverse association between body mass index (BMI) and risk of lung cancer has been reported. However, the association of body composition such as fat mass (FM) and lean body mass (LBM) with risk of lung cancer has not been fully investigated. Using two large prospective cohort studies (Nurses’ Health Study, 1986–2014; Health Professionals Follow-up Study, 1987–2012) in the United States, we included 100,985 participants who were followed for occurrence of lung cancer. Predicted FM and LBM derived from validated anthropometric prediction equations were categorized by sex-specific deciles. During an average 22.3-year follow-up, 2615 incident lung cancer cases were identified. BMI showed an inverse association with lung cancer risk. Participants in the 10th decile of predicted FM and LBM had a lower risk of lung cancer compared with those in the 1st decile, but when mutually adjusted for each other, predicted FM was not associated with lung cancer risk (adjusted hazard ratio [aHR] = 0.98, 95% confidence interval [CI] 0.72–1.35; P(trend) = 0.97) whereas predicted LBM had an inverse association (aHR = 0.73, 95% CI 0.53–1.00; P(trend) = 0.03), especially among participants who were current smokers or had smoked in the previous 10 years (aHR = 0.55, 95% CI 0.36–0.84; P(trend) = 0.008). In conclusion, BMI was inversely associated with lung cancer risk. Based on anthropometric prediction equations, low LBM rather than low FM accounted for the inverse association between BMI and lung cancer risk.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Renehan AG, Tyson M, Egger M, Heller RF, Zwahlen M. Body-mass index and incidence of cancer: a systematic review and meta-analysis of prospective observational studies. Lancet. 2008;371(9612):569–78. https://doi.org/10.1016/s0140-6736(08)60269-x.

    Article  PubMed  Google Scholar 

  2. Smith L, Brinton LA, Spitz MR, Lam TK, Park Y, Hollenbeck AR, et al. Body mass index and risk of lung cancer among never, former, and current smokers. J Natl Cancer Inst. 2012;104(10):778–89. https://doi.org/10.1093/jnci/djs179.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Sanikini H, Yuan J-M, Butler LM, Koh W-P, Gao Y-T, Steffen A, et al. Body mass index and lung cancer risk: a pooled analysis based on nested case-control studies from four cohort studies. BMC Cancer. 2018;18(1):220. https://doi.org/10.1186/s12885-018-4124-0.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Kabat GC, Kim M, Hunt JR, Chlebowski RT, Rohan TE. Body mass index and waist circumference in relation to lung cancer risk in the Women’s Health Initiative. Am J Epidemiol. 2008;168(2):158–69. https://doi.org/10.1093/aje/kwn109.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Bethea TN, Rosenberg L, Charlot M, O’Connor GT, Adams-Campbell LL, Palmer JR. Obesity in relation to lung cancer incidence in African American women. Cancer Causes Control. 2013;24(9):1695–703. https://doi.org/10.1007/s10552-013-0245-6.

    Article  PubMed  PubMed Central  Google Scholar 

  6. El-Zein M, Parent ME, Nicolau B, Koushik A, Siemiatycki J, Rousseau MC. Body mass index, lifetime smoking intensity and lung cancer risk. Int J Cancer. 2013;133(7):1721–31. https://doi.org/10.1002/ijc.28185.

    Article  CAS  PubMed  Google Scholar 

  7. Olson JE, Yang P, Schmitz K, Vierkant RA, Cerhan JR, Sellers TA. Differential association of body mass index and fat distribution with three major histologic types of lung cancer: evidence from a cohort of older women. Am J Epidemiol. 2002;156(7):606–15. https://doi.org/10.1093/aje/kwf084.

    Article  CAS  PubMed  Google Scholar 

  8. Chiolero A, Faeh D, Paccaud F, Cornuz J. Consequences of smoking for body weight, body fat distribution, and insulin resistance. Am J Clin Nutr. 2008;87(4):801–9. https://doi.org/10.1093/ajcn/87.4.801.

    Article  CAS  PubMed  Google Scholar 

  9. Malhotra J, Malvezzi M, Negri E, La Vecchia C, Boffetta P. Risk factors for lung cancer worldwide. Eur Respir J. 2016;48(3):889–902. https://doi.org/10.1183/13993003.00359-2016.

    Article  Google Scholar 

  10. Yu D, Zheng W, Johansson M, Lan Q, Park Y, White E, et al. Overall and central obesity and risk of lung cancer: a pooled analysis. J Natl Cancer Inst. 2018;110(8):831–42. https://doi.org/10.1093/jnci/djx286.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Dewi NU, Boshuizen HC, Johansson M, Vineis P, Kampman E, Steffen A, et al. Anthropometry and the Risk of Lung Cancer in EPIC. Am J Epidemiol. 2016;184(2):129–39. https://doi.org/10.1093/aje/kwv298.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Padwal R, Leslie WD, Lix LM, Majumdar SR. Relationship among body fat percentage, body mass index, and all-cause mortality: a cohort study. Ann Intern Med. 2016;164(8):532–41. https://doi.org/10.7326/m15-1181.

    Article  PubMed  Google Scholar 

  13. Han SS, Kim KW, Kim KI, Na KY, Chae DW, Kim S, et al. Lean mass index: a better predictor of mortality than body mass index in elderly Asians. J Am Geriatr Soc. 2010;58(2):312–7. https://doi.org/10.1111/j.1532-5415.2009.02672.x.

    Article  PubMed  Google Scholar 

  14. Lee DH, Giovannucci EL. Body composition and mortality in the general population: a review of epidemiologic studies. Exp Biol Med. 2018;243(17–18):1275–85. https://doi.org/10.1177/1535370218818161.

    Article  CAS  Google Scholar 

  15. Tsai S. Importance of lean body mass in the oncologic patient. Nutr Clin Pract. 2012;27(5):593–8. https://doi.org/10.1177/0884533612457949.

    Article  PubMed  Google Scholar 

  16. Schols AM, Broekhuizen R, Weling-Scheepers CA, Wouters EF. Body composition and mortality in chronic obstructive pulmonary disease. Am J Clin Nutr. 2005;82(1):53–9. https://doi.org/10.1093/ajcn.82.1.53.

    Article  CAS  PubMed  Google Scholar 

  17. Lee DH, Keum N, Hu FB, Orav EJ, Rimm EB, Sun Q, et al. Development and validation of anthropometric prediction equations for lean body mass, fat mass and percent fat in adults using the National Health and Nutrition Examination Survey (NHANES) 1999–2006. Br J Nutr. 2017;118(10):858–66. https://doi.org/10.1017/s0007114517002665.

    Article  CAS  PubMed  Google Scholar 

  18. Lee DH, Keum N, Hu FB, Orav EJ, Rimm EB, Willett WC, et al. Comparison of the association of predicted fat mass, body mass index, and other obesity indicators with type 2 diabetes risk: two large prospective studies in US men and women. Eur J Epidemiol. 2018;33(11):1113–23. https://doi.org/10.1007/s10654-018-0433-5.

    Article  CAS  PubMed  Google Scholar 

  19. Lee DH, Keum N, Hu FB, Orav EJ, Rimm EB, Willett WC, et al. Predicted lean body mass, fat mass, and all cause and cause specific mortality in men: prospective US cohort study. BMJ. 2018;362:k2575. https://doi.org/10.1136/bmj.k2575.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Hanyuda A, Lee DH, Ogino S, Wu K, Giovannucci EL. Long-term status of predicted body fat percentage, body mass index, and other anthropometric factors with risk of colorectal carcinoma: Two large prospective cohort studies in the US. Int J Cancer. 2019.

  21. Rich-Edwards JW, Corsano KA, Stampfer MJ. Test of the National death index and Equifax nationwide death search. Am J Epidemiol. 1994;140(11):1016–9. https://doi.org/10.1093/oxfordjournals.aje.a117191.

    Article  CAS  PubMed  Google Scholar 

  22. Duan P, Hu C, Quan C, Yi X, Zhou W, Yuan M, et al. Body mass index and risk of lung cancer: systematic review and dose-response meta-analysis. Sci Rep. 2015;5:16938. https://doi.org/10.1038/srep16938.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Yang Y, Dong J, Sun K, Zhao L, Zhao F, Wang L, et al. Obesity and incidence of lung cancer: a meta-analysis. Int J Cancer. 2013;132(5):1162–9. https://doi.org/10.1002/ijc.27719.

    Article  CAS  PubMed  Google Scholar 

  24. Zhu H, Zhang S. Body mass index and lung cancer risk in never smokers: a meta-analysis. BMC Cancer. 2018;18(1):635. https://doi.org/10.1186/s12885-018-4543-y.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Lam TK, Moore SC, Brinton LA, Smith L, Hollenbeck AR, Gierach GL, et al. Anthropometric measures and physical activity and the risk of lung cancer in never-smokers: a prospective cohort study. PLoS ONE. 2013;8(8):e70672. https://doi.org/10.1371/journal.pone.0070672.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Kark JD, Yaari S, Rasooly I, Goldbourt U. Are lean smokers at increased risk of lung cancer? The Israel Civil Servant Cancer Study. Arch Intern Med. 1995;155(22):2409–16.

    Article  CAS  Google Scholar 

  27. Petersen AMW, Magkos F, Atherton P, Selby A, Smith K, Rennie MJ, et al. Smoking impairs muscle protein synthesis and increases the expression of myostatin and MAFbx in muscle. Am J Physiol Endocrinol Metab. 2007;293(3):E843–8. https://doi.org/10.1152/ajpendo.00301.2007.

    Article  CAS  PubMed  Google Scholar 

  28. Rom O, Kaisari S, Aizenbud D, Reznick AZ. Sarcopenia and smoking: a possible cellular model of cigarette smoke effects on muscle protein breakdown. Ann N Y Acad Sci. 2012;1259(1):47–53. https://doi.org/10.1111/j.1749-6632.2012.06532.x.

    Article  CAS  PubMed  Google Scholar 

  29. Mizoue T, Kasai H, Kubo T, Tokunaga S. Leanness, smoking, and enhanced oxidative DNA damage. Cancer Epidemiol Biomark Prev. 2006;15(3):582–5. https://doi.org/10.1158/1055-9965.epi-05-0658.

    Article  CAS  Google Scholar 

  30. Flanders WD, Lally CA, Zhu B-P, Henley SJ, Thun MJ. Lung cancer mortality in relation to age, duration of smoking, and daily cigarette consumption. Results from Cancer Prevention Study II. Cancer Res. 2003;63(19):6556–62.

    CAS  PubMed  Google Scholar 

  31. Zhang X, Liu Y, Shao H, Zheng X. Obesity paradox in lung cancer prognosis: evolving biological insights and clinical implications. J Thorac Oncol. 2017;12(10):1478–88. https://doi.org/10.1016/j.jtho.2017.07.022.

    Article  PubMed  Google Scholar 

  32. Carreras-Torres R, Johansson M, Haycock PC, Wade KH, Relton CL, Martin RM, et al. Obesity, metabolic factors and risk of different histological types of lung cancer: a Mendelian randomization study. PLoS ONE. 2017;12(6):e0177875. https://doi.org/10.1371/journal.pone.0177875.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Karastergiou K, Smith SR, Greenberg AS, Fried SK. Sex differences in human adipose tissues—the biology of pear shape. Biol Sex Differ. 2012;3(1):13. https://doi.org/10.1186/2042-6410-3-13.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Ntikoudi E, Kiagia M, Boura P, Syrigos KN. Hormones of adipose tissue and their biologic role in lung cancer. Cancer Treat Rev. 2014;40(1):22–30. https://doi.org/10.1016/j.ctrv.2013.06.005.

    Article  CAS  PubMed  Google Scholar 

  35. Creutzberg EC, Schols AM, Bothmer-Quaedvlieg FC, Wouters EF. Prevalence of an elevated resting energy expenditure in patients with chronic obstructive pulmonary disease in relation to body composition and lung function. Eur J Clin Nutr. 1998;52(6):396–401.

    Article  CAS  Google Scholar 

  36. Goldkorn T, Filosto S. Lung injury and cancer: mechanistic insights into ceramide and EGFR signaling under cigarette smoke. Am J Respir Cell Mol Biol. 2010;43(3):259–68. https://doi.org/10.1165/rcmb.2010-0220RT.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Khuder SA. Effect of cigarette smoking on major histological types of lung cancer: a meta-analysis. Lung Cancer. 2001;31(2–3):139–48.

    Article  CAS  Google Scholar 

  38. Rimm EB, Stampfer MJ, Colditz GA, Chute CG, Litin LB, Willett WC. Validity of self-reported waist and hip circumferences in men and women. Epidemiology. 1990;1(6):466–73. https://doi.org/10.1097/00001648-199011000-00009.

    Article  CAS  PubMed  Google Scholar 

  39. Baracos VE, Reiman T, Mourtzakis M, Gioulbasanis I, Antoun S. Body composition in patients with non-small cell lung cancer: a contemporary view of cancer cachexia with the use of computed tomography image analysis. Am J Clin Nutr. 2010;91(4):1133s–7s. https://doi.org/10.3945/ajcn.2010.28608C.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgment

We would like to thank the participants and staff of the NHS and HPFS for their valuable contributions as well as the following state cancer registries for their help: AL, AZ, AR, CA, CO, CT, DE, FL, GA, ID, IL, IN, IA, KY, LA, ME, MD, MA, MI, NE, NH, NJ, NY, NC, ND, OH, OK, OR, PA, RI, SC, TN, TX, VA, WA, WY. The authors assume full responsibility for analyses and interpretation of these data.

Funding

This work was supported by the National Institutes of Health (UM1 CA167552, R01 HL35464, UM1 CA186107, P01 CA87969, and R03 CA223619).

Author information

Authors and Affiliations

Authors

Contributions

DHL and ELG contributed to the study design and conception. S-MJ, DHL and ELG drafted the manuscript and the tables. DHL and ELG contributed to the data acquisition and analysis. DHL contributed to the statistical analysis. S-MJ, DHL and ELG critically revised the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Edward L. Giovannucci.

Ethics declarations

Conflicts of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 68 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jeong, SM., Lee, D.H. & Giovannucci, E.L. Predicted lean body mass, fat mass and risk of lung cancer: prospective US cohort study. Eur J Epidemiol 34, 1151–1160 (2019). https://doi.org/10.1007/s10654-019-00587-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10654-019-00587-2

Keywords

Navigation