Skip to main content

Advertisement

Log in

Dietary inflammatory index, Mediterranean diet score, and lung cancer: a prospective study

  • Original Paper
  • Published:
Cancer Causes & Control Aims and scope Submit manuscript

Abstract

Purpose

To investigate prospectively the associations of Dietary Inflammatory Index (DII) and Mediterranean Diet Score (MDS) with lung cancer.

Methods

We used data from men and women aged 40–69 years at recruitment in 1990–1994, who were participants in the Melbourne Collaborative Cohort Study (n = 35,303). A total of 403 incident lung cancer cases were identified over an average 18-year follow-up. Hazard ratios (HR) were estimated using Cox regression, adjusting for smoking status and other risk factors, with age as the time metric.

Results

An inverse correlation was observed between the DII and MDS (ρ = −0.45), consistent with a higher DII being pro-inflammatory and less ‘healthy,’ while a high MDS reflects a ‘healthier’ diet. The DII was positively associated with risk of lung cancer in current smokers [HRQ4 vs Q1 = 1.70 (1.02, 2.82); Ptrend = 0.008] (p interaction between DII quartiles and smoking status = 0.03). The MDS was inversely associated with lung cancer risk overall [HR7–9 vs 0–3 = 0.64 (0.45, 0.90); Ptrend = 0.005] and for current smokers (HR7–9 vs 0–3 = 0.38 (0.19, 0.75); Ptrend = 0.005) (p interaction between MDS categories and smoking status = 0.31).

Conclusions

The MDS showed an inverse association with lung cancer risk, especially for current smokers. A high DII, indicating a more pro-inflammatory diet, was associated with risk of lung cancer only for current smokers. A healthy diet may reduce the risk of lung cancer, especially in smokers.

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.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A (2015) Global cancer statistics, 2012. CA Cancer J Clin. doi:10.3322/caac.21262

    PubMed  Google Scholar 

  2. Shiels MS, Katki HA, Freedman ND, Purdue MP, Wentzensen N, Trabert B, Kitahara CM, Furr M, Li Y, Kemp TJ et al (2014) Cigarette smoking and variations in systemic immune and inflammation markers. J Natl Cancer Inst. doi:10.1093/jnci/dju294

    PubMed  PubMed Central  Google Scholar 

  3. Arnson Y, Shoenfeld Y, Amital H (2010) Effects of tobacco smoke on immunity, inflammation and autoimmunity. J Autoimmun 34:J258–J265. doi:10.1016/j.jaut.2009.12.003

    Article  CAS  PubMed  Google Scholar 

  4. Chaturvedi AK, Caporaso NE, Katki HA, Wong HL, Chatterjee N, Pine SR, Chanock SJ, Goedert JJ, Engels EA (2010) C-reactive protein and risk of lung cancer. J Clin Oncol 28:2719–2726. doi:10.1200/JCO.2009.27.0454

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Pine SR, Mechanic LE, Enewold L, Chaturvedi AK, Katki HA, Zheng YL, Bowman ED, Engels EA, Caporaso NE, Harris CC (2011) Increased levels of circulating interleukin 6, interleukin 8, C-reactive protein, and risk of lung cancer. J Natl Cancer Inst 103:1112–1122. doi:10.1093/jnci/djr216

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Shiels MS, Pfeiffer RM, Hildesheim A, Engels EA, Kemp TJ, Park JH, Katki HA, Koshiol J, Shelton G, Caporaso NE et al (2013) Circulating inflammation markers and prospective risk for lung cancer. J Natl Cancer Inst 105:1871–1880. doi:10.1093/jnci/djt309

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Cavicchia PP, Steck SE, Hurley TG, Hussey JR, Ma Y, Ockene IS, Hebert JR (2009) A new dietary inflammatory index predicts interval changes in serum high-sensitivity C-reactive protein. J Nutr 139:2365–2372. doi:10.3945/jn.109.114025

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Shivappa N, Steck SE, Hurley TG, Hussey JR, Hebert JR (2014) Designing and developing a literature-derived, population-based dietary inflammatory index. Public Health Nutr 17:1689–1696. doi:10.1017/S1368980013002115

    Article  PubMed  Google Scholar 

  9. Shivappa N, Steck SE, Hurley TG, Hussey JR, Ma Y, Ockene IS, Tabung F, Hebert JR (2014) A population-based dietary inflammatory index predicts levels of C-reactive protein in the seasonal variation of blood cholesterol study (SEASONS). Public Health Nutr 17:1825–1833. doi:10.1017/S1368980013002565

    Article  PubMed  Google Scholar 

  10. van Woudenbergh GJ, Theofylaktopoulou D, Kuijsten A, Ferreira I, van Greevenbroek MM, van der Kallen CJ, Schalkwijk CG, Stehouwer CD, Ocke MC, Nijpels G et al (2013) Adapted dietary inflammatory index and its association with a summary score for low-grade inflammation and markers of glucose metabolism: the cohort study on diabetes and atherosclerosis maastricht (CODAM) and the Hoorn study. Am J Clin Nutr 98:1533–1542. doi:10.3945/ajcn.112.056333

    Article  PubMed  Google Scholar 

  11. Shivappa N, Prizment AE, Blair CK, Jacobs DR Jr, Steck SE, Hebert JR (2014) Dietary inflammatory index and risk of colorectal cancer in the Iowa women’s health study. Cancer Epidemiol Biomarkers Prev 23:2383–2392. doi:10.1158/1055-9965.EPI-14-0537

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Zamora-Ros R, Shivappa N, Steck SE, Canzian F, Landi S, Alonso MH, Hebert JR, Moreno V (2015) Dietary inflammatory index and inflammatory gene interactions in relation to colorectal cancer risk in the Bellvitge colorectal cancer case–control study. Genes Nutr 10:447. doi:10.1007/s12263-014-0447-x

    Article  PubMed  Google Scholar 

  13. Tabung FK, Steck SE, Ma Y, Liese AD, Zhang J, Caan B, Hou L, Johnson KC, Mossavar-Rahmani Y, Shivappa N et al (2015) The association between dietary inflammatory index and risk of colorectal cancer among postmenopausal women: results from the women’s health initiative. Cancer Causes Control 26:399–408. doi:10.1007/s10552-014-0515-y

    Article  PubMed  Google Scholar 

  14. Shivappa N, Bosetti C, Zucchetto A, Montella M, Serraino D, La Vecchia C, Hebert JR (2014) Association between dietary inflammatory index and prostate cancer among Italian men. Br J Nutr. doi:10.1017/S0007114514003572

    Google Scholar 

  15. Shivappa N, Bosetti C, Zucchetto A, Serraino D, La Vecchia C, Hebert JR (2014) Dietary inflammatory index and risk of pancreatic cancer in an Italian case–control study. Br J Nutr. doi:10.1017/S0007114514003626

    Google Scholar 

  16. Shivappa N, Hebert JR, Rietzschel ER, De Buyzere ML, Langlois M, Debruyne E, Marcos A, Huybrechts I (2015) Associations between dietary inflammatory index and inflammatory markers in the Asklepios study. Br J Nutr 113:665–671. doi:10.1017/S000711451400395X

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Tabung FK, Steck SE, Zhang J, Ma Y, Liese AD, Agalliu I, Hingle M, Hou L, Hurley TG, Jiao L et al (2015) Construct validation of the dietary inflammatory index among postmenopausal women. Ann Epidemiol 25:398–405. doi:10.1016/j.annepidem.2015.03.009

    Article  PubMed  PubMed Central  Google Scholar 

  18. Wirth MD, Burch J, Shivappa N, Violanti JM, Burchfiel CM, Fekedulegn D, Andrew ME, Hartley TA, Miller DB, Mnatsakanova A et al (2014) Association of a dietary inflammatory index with inflammatory indices and metabolic syndrome among police officers. J Occup Environ Med 56:986–989. doi:10.1097/JOM.0000000000000213

    Article  PubMed  PubMed Central  Google Scholar 

  19. Shivappa N, Steck SE, Hussey JR, Ma Y, Hebert JR (2015) Inflammatory potential of diet and all-cause, cardiovascular, and cancer mortality in National Health and Nutrition Examination Survey III study. Eur J Nutr. doi:10.1007/s00394-015-1112-x

    PubMed Central  Google Scholar 

  20. Turner-McGrievy GM, Wirth MD, Shivappa N, Wingard EE, Fayad R, Wilcox S, Frongillo EA, Hebert JR (2015) Randomization to plant-based dietary approaches leads to larger short-term improvements in Dietary Inflammatory Index scores and macronutrient intake compared with diets that contain meat. Nutr Res 35:97–106. doi:10.1016/j.nutres.2014.11.007

    Article  CAS  PubMed  Google Scholar 

  21. Martinez-Gonzalez MA, Salas-Salvado J, Estruch R, Corella D, Fito M, Ros E (2015) Benefits of the Mediterranean diet: insights from the PREDIMED study. Prog Cardiovasc Dis 58:50–60. doi:10.1016/j.pcad.2015.04.003

    Article  PubMed  Google Scholar 

  22. Maisonneuve P, Shivappa N, Hebert JR, Bellomi M, Rampinelli C, Bertolotti R, Spaggiari L, Palli D, Veronesi G, Gnagnarella P (2015) Dietary inflammatory index and risk of lung cancer and other respiratory conditions among heavy smokers in the COSMOS screening study. Eur J Nutr. doi:10.1007/s00394-015-0920-3

    PubMed  Google Scholar 

  23. Giles GG, English DR (2002) The Melbourne collaborative cohort study. IARC Sci Publ 156:69–70

    CAS  PubMed  Google Scholar 

  24. Ireland P, Jolley D, Giles G, O’Dea K, Powles J, Rutishauser I, Wahlqvist M, Williams J (1994) Development of the Melbourne FFQ: a food frequency questionnaire for use in an Australian prospective study involving an ethnically diverse cohort. Asia Pac J Clin Nutr 3:19–31

    CAS  PubMed  Google Scholar 

  25. Lewis J, Milligan G, Hunt A (1995) NUTTAB 95 nutrient data table for use in Australia. Australian Government Publishing Service, Canberra

    Google Scholar 

  26. Holland B, Welch AA, Unwin ID, Buss DHPA, Southgate DAT (1993) McCance and Widdowson’s the composition of foods. Royal Society of Chemistry Cambridge, Cambridge

    Google Scholar 

  27. Royal Melbourne Institute of Technology University Lipid Research Group (2001) Fatty acid compositional data base. Xyris software, Brisbane

    Google Scholar 

  28. US Department of Agriculture, Agricultural Research Service, Nutrient Data Laboratory (2003) USDA-NCC Carotenoid database for US foods-1998. http://www.nal.usda.gov/fnic/foodcomp/Data/car98/car98.html. Accessed Mar 2009

  29. Trichopoulou A, Costacou T, Bamia C, Trichopoulos D (2003) Adherence to a Mediterranean diet and survival in a Greek population. N Engl J Med 348:2599–2608. doi:10.1056/NEJMoa025039

    Article  PubMed  Google Scholar 

  30. Baghurst KI, Record SJ, Leppard P (2000) Red meat consumption in Australia: intakes, nutrient contribution and changes over time. Aust J Nutr Diet 57:S1–S36

    Google Scholar 

  31. Martinez-Gonzalez MA, de la Fuente-Arrillaga C, Nunez-Cordoba JM, Basterra-Gortari FJ, Beunza JJ, Vazquez Z, Benito S, Tortosa A, Bes-Rastrollo M (2008) Adherence to Mediterranean diet and risk of developing diabetes: prospective cohort study. BMJ 336:1348–1351. doi:10.1136/bmj.39561.501007.BE

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. MacInnis RJ, English DR, Hopper JL, Haydon AM, Gertig DM, Giles GG (2004) Body size and composition and colon cancer risk in men. Cancer Epidemiol Biomarkers Prev 13:553–559

    PubMed  Google Scholar 

  33. Pink B (2013) Socio-economic indexes for areas. 2011. Australian Bureau of Statistics, Canberra

    Google Scholar 

  34. Hodge AM, English DR, O’Dea K, Giles GG (2004) Glycemic index and dietary fiber and the risk of type 2 diabetes. Diabetes Care 27:2701–2706

    Article  PubMed  Google Scholar 

  35. Liu S, Manson JE, Buring JE, Stampfer MJ, Willett WC, Ridker PM (2002) Relation between a diet with a high glycemic load and plasma concentrations of high-sensitivity C-reactive protein in middle-aged women. Am J Clin Nutr 75:492–498

    CAS  PubMed  Google Scholar 

  36. Willett WC, Howe GR, Kushi LH (1997) Adjustment for total energy intake in epidemiologic studies. Am J Clin Nutr 65:1220S–1228S (discussion 1229S-1231S)

    CAS  PubMed  Google Scholar 

  37. Korn EL, Graubard BI, Midthune D (1997) Time-to-event analysis of longitudinal follow-up of a survey: choice of the time-scale. Am J Epidemiol 145:72–80

    Article  CAS  PubMed  Google Scholar 

  38. Rothman K, Greenland S, Lash T (2008) Modern Epidemiology, 3rd edn. Lipincott Williams and Wilkins, Philadelphia

    Google Scholar 

  39. Kirkwood BR, Sterne JAC (2003) Essential Medical Statistics, 2nd edn. Blackwell Science, Malden

    Google Scholar 

  40. World Cancer Reserach Fund, American Institue for Cancer Research (2007) Food, nutrition, physical activity, and the prevention of cancer: a global perspective. AICR, Washington DC

    Google Scholar 

  41. Satia JA, Littman A, Slatore CG, Galanko JA, White E (2009) Long-term use of beta-carotene, retinol, lycopene, and lutein supplements and lung cancer risk: results from the vitamins and lifestyle (VITAL) study. Am J Epidemiol 169:815–828. doi:10.1093/aje/kwn409

    Article  PubMed  PubMed Central  Google Scholar 

  42. Mannisto S, Smith-Warner SA, Spiegelman D, Albanes D, Anderson K, van den Brandt PA, Cerhan JR, Colditz G, Feskanich D, Freudenheim JL et al (2004) Dietary carotenoids and risk of lung cancer in a pooled analysis of seven cohort studies. Cancer Epidemiol Biomarkers Prev 13:40–48

    Article  PubMed  Google Scholar 

  43. Gallicchio L, Boyd K, Matanoski G, Tao XG, Chen L, Lam TK, Shiels M, Hammond E, Robinson KA, Caulfield LE et al (2008) Carotenoids and the risk of developing lung cancer: a systematic review. Am J Clin Nutr 88:372–383

    CAS  PubMed  Google Scholar 

  44. Takata Y, Xiang YB, Yang G, Li H, Gao J, Cai H, Gao YT, Zheng W, Shu XO (2013) Intakes of fruits, vegetables, and related vitamins and lung cancer risk: results from the Shanghai Men’s Health Study (2002–2009). Nutr Cancer 65:51–61. doi:10.1080/01635581.2013.741757

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Xue XJ, Gao Q, Qiao JH, Zhang J, Xu CP, Liu J (2014) Red and processed meat consumption and the risk of lung cancer: a dose-response meta-analysis of 33 published studies. Int J Clin Exp Med 7:1542–1553

    PubMed  PubMed Central  Google Scholar 

  46. Australian Bureau of Statistics (1998) National Nutrition Survey nutrient intakes and physical measurements Australia. Australian Bureau of Statistics, Canberra

    Google Scholar 

  47. Smith-Warner SA, Ritz J, Hunter DJ, Albanes D, Beeson WL, van den Brandt PA, Colditz G, Folsom AR, Fraser GE, Freudenheim JL et al (2002) Dietary fat and risk of lung cancer in a pooled analysis of prospective studies. Cancer Epidemiol Biomarkers Prev 11:987–992

    PubMed  Google Scholar 

  48. Wu SH, Liu Z (2013) Soy food consumption and lung cancer risk: a meta-analysis using a common measure across studies. Nutr Cancer 65:625–632. doi:10.1080/01635581.2013.795983

    Article  CAS  PubMed  Google Scholar 

  49. Reedy J, Krebs-Smith SM, Miller PE, Liese AD, Kahle LL, Park Y, Subar AF (2014) Higher diet quality is associated with decreased risk of all-cause, cardiovascular disease, and cancer mortality among older adults. J Nutr 144:881–889. doi:10.3945/jn.113.189407

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

Melbourne Collaborative Cohort Study (MCCS) recruitment was funded by VicHealth and Cancer Council Victoria. The MCCS was further supported by Australian National Health and Medical Research Council Grants 209057, 251553, and 1050198 and by infrastructure provided by Cancer Council Victoria. Cases and their vital status were ascertained through the Victorian Cancer Registry (VCR) and the Australian Institute of Health and Welfare (AIHW), including the National Death Index and the Australian Cancer Database. Drs. Shivappa and Hébert were supported by Grant Number R44DK103377 from the United States National Institute for Diabetes and Digestive and Kidney Diseases.

Author contribution

This study was made possible by the contribution of many people, including the original investigators and the diligent team who recruited the participants and who continue working on follow-up. We would also like to express our gratitude to the many thousands of Melbourne residents who continue to participate in the study.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. M. Hodge.

Ethics declarations

Conflict of interest

Dr. James R. Hébert owns controlling interest in Connecting Health Innovations LLC (CHI), a company planning to license the right to his invention of the dietary inflammatory index (DII) from the University of South Carolina in order to develop computer and smart phone applications for patient counseling and dietary intervention in clinical settings. Dr. Nitin Shivappa is an employee of CHI.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hodge, A.M., Bassett, J.K., Shivappa, N. et al. Dietary inflammatory index, Mediterranean diet score, and lung cancer: a prospective study. Cancer Causes Control 27, 907–917 (2016). https://doi.org/10.1007/s10552-016-0770-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10552-016-0770-1

Keywords

Navigation