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Dietary inflammatory index and risk of lung cancer and other respiratory conditions among heavy smokers in the COSMOS screening study

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Abstract

Purpose

To test whether the inflammatory potential of diet, as measured using the dietary inflammatory index (DII), is associated with risk of lung cancer or other respiratory conditions and to compare results obtained with those based on the aMED score, an established dietary index that measures adherence to the traditional Mediterranean diet.

Methods

In 4336 heavy smokers enrolled in a prospective, non-randomized lung cancer screening program, we measured participants’ diets at baseline using a self-administered food frequency questionnaire from which dietary scores were calculated. Cox proportional hazards and logistic regression models were used to assess association between the dietary indices and lung cancer diagnosed during annual screening, and other respiratory outcomes that were recorded at baseline, respectively.

Results

In multivariable analysis, adjusted for baseline lung cancer risk (estimated from age, sex, smoking history, and asbestos exposure) and total energy, both DII and aMED scores were associated with dyspnoea (p trend = 0.046 and 0.02, respectively) and radiological evidence of emphysema (p trend = 0.0002 and 0.02). After mutual adjustment of the two dietary scores, only the association between DII and radiological evidence of emphysema (Q4 vs. Q1, OR 1.30, 95 % CI 1.01–1.67, p trend = 0.012) remained statistically significant. At univariate analysis, both DII and aMED were associated with lung cancer risk, but in fully adjusted multivariate analysis, only the association with aMED remained statistically significant (p trend = 0.04).

Conclusions

Among heavy smokers, a pro-inflammatory diet, as indicated by increasing DII score, is associated with dyspnoea and radiological evidence of emphysema. A traditional Mediterranean diet, which is associated with a lower DII, may lower lung cancer risk.

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References

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

    Article  Google Scholar 

  2. Veronesi G, Bellomi M, Mulshine JL, Pelosi G, Scanagatta P, Paganelli G, Maisonneuve P, Preda L, Leo F, Bertolotti R, Solli P, Spaggiari L (2008) Lung cancer screening with low-dose computed tomography: a non-invasive diagnostic protocol for baseline lung nodules. Lung Cancer 61(3):340–349

    Article  Google Scholar 

  3. Gnagnarella P, Maisonneuve P, Bellomi M, Rampinelli C, Bertolotti R, Spaggiari L, Palli D, Veronesi G (2013) Red meat, Mediterranean diet and lung cancer risk among heavy smokers in the COSMOS screening study. Ann Oncol 24(10):2606–2611

    Article  CAS  Google Scholar 

  4. Gnagnarella P, Maisonneuve P, Bellomi M, Rampinelli C, Bertolotti R, Spaggiari L, Palli D, Veronesi G (2013) Nutrient intake and nutrient patterns and risk of lung cancer among heavy smokers: results from the COSMOS screening study with annual low-dose CT. Eur J Epidemiol 28(6):503–511

    Article  CAS  Google Scholar 

  5. Ziegler RG, Mayne ST, Swanson CA (1996) Nutrition and lung cancer. Cancer Causes Control 7(1):157–177

    Article  CAS  Google Scholar 

  6. Wogan GN, Hecht SS, Felton JS, Conney AH, Loeb LA (2004) Environmental and chemical carcinogenesis. Semin Cancer Biol 14(6):473–486

    Article  CAS  Google Scholar 

  7. Shiels MS, Pfeiffer RM, Hildesheim A, Engels EA, Kemp TJ, Park JH, Katki HA, Koshiol J, Shelton G, Caporaso NE, Pinto LA, Chaturvedi AK (2013) Circulating inflammation markers and prospective risk for lung cancer. J Natl Cancer Inst 105(24):1871–1880

    Article  CAS  Google Scholar 

  8. 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(14):1112–1122

    Article  CAS  Google Scholar 

  9. Shivappa N, Hébert 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 2:1–7

    Google Scholar 

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

    Article  Google Scholar 

  11. Wood LG, Shivappa N, Berthon BS, Gibson PG, Hebert JR (2015) Dietary inflammatory index is related to asthma risk, lung function and systemic inflammation in asthma. Clin Exp Allergy 45(1):177–183

    Article  CAS  Google Scholar 

  12. Shivappa N, Prizment AE, Blair CK, Jacobs DR Jr, Steck SE, Hebert JR (2014) Dietary inflammatory index (DII) and risk of colorectal cancer in Iowa Women’s Health Study. Cancer Epidemiol Biomarkers Prev 23(11):2383–2392

    Article  CAS  Google Scholar 

  13. Shivappa N, Steck SE, Hurley TG, Hussey JR, Ma Y, Ockene IS, Tabung F, Hébert 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(8):1825–1833

    Article  Google Scholar 

  14. Wirth MD, Burch J, Shivappa N, Steck SE, Hurley TG, Vena JE, Hébert JR (2014) Dietary inflammatory index scores differ by shift work status: NHANES 2005 to 2010. J Occup Environ Med 56(2):145–148

    Article  Google Scholar 

  15. Milara J, Cortijo J (2012) Tobacco, inflammation, and respiratory tract cancer. Curr Pharm Des 18:3901–3938

    Article  CAS  Google Scholar 

  16. Fung TT, McCullough ML, Newby PK, Manson JE, Meigs JB, Rifai N, Willett WC, Hu FB (2005) Diet-quality scores and plasma concentrations of markers of inflammation and endothelial dysfunction. Am J Clin Nutr 82:163–173

    CAS  Google Scholar 

  17. Pisani P, Faggiano F, Krogh V, Palli D, Vineis P, Berrino F (1997) Relative validity and reproducibility of a food frequency dietary questionnaire for use in the Italian EPIC centres. Int J Epidemiol 26(Suppl 1):S152–S160

    Article  Google Scholar 

  18. Pala V, Sieri S, Palli D, Salvini S, Berrino F, Bellegotti M, Frasca G, Tumino R, Sacerdote C, Fiorini L, Celentano E, Galasso R, Krogh V (2003) Diet in the Italian EPIC cohorts: presentation of data and methodological issues. Tumori 89(6):594–607

    Google Scholar 

  19. Cavicchia PP, Steck SE, Hurley TG, Hussey JR, Ma Y, Ockene IS, Hébert JR (2009) A new dietary inflammatory index predicts interval changes in serum high-sensitivity C-reactive protein. J Nutr 139(12):2365–2372

    Article  CAS  Google Scholar 

  20. 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(26):2599–2608

    Article  Google Scholar 

  21. Fung TT, Rexrode KM, Mantzoros CS, Manson JE, Willett WC, Hu FB (2009) Mediterranean diet and incidence of and mortality from coronary heart disease and stroke in women. Circulation 119(8):1093–1100

    Article  Google Scholar 

  22. Maisonneuve P, Bagnardi V, Bellomi M, Spaggiari L, Pelosi G, Rampinelli C, Bertolotti R, Rotmensz N, Field JK, Decensi A, Veronesi G (2011) Lung cancer risk prediction to select smokers for screening CT—a model based on the Italian COSMOS trial. Cancer Prev Res (Phila) 4(11):1778–1789

    Article  Google Scholar 

  23. Büchner FL, Bueno-de-Mesquita HB, Ros MM, Overvad K, Dahm CC, Hansen L, Tjønneland A, Clavel-Chapelon F, Boutron-Ruault MC, Touillaud M, Kaaks R, Rohrmann S, Boeing H, Nöthlings U, Trichopoulou A, Zylis D, Dilis V, Palli D, Sieri S, Vineis P, Tumino R, Panico S, Peeters PH, van Gils CH, Lund E, Gram IT, Braaten T, Sánchez MJ, Agudo A, Larrañaga N, Ardanaz E, Navarro C, Argüelles MV, Manjer J, Wirfält E, Hallmans G, Rasmuson T, Key TJ, Khaw KT, Wareham N, Slimani N, Vergnaud AC, Xun WW, Kiemeney LA, Riboli E (2010) Variety in fruit and vegetable consumption and the risk of lung cancer in the European prospective investigation into cancer and nutrition. Cancer Epidemiol Biomarkers Prev 19(9):2278–2286

    Article  Google Scholar 

  24. Linseisen J, Rohrmann S, Bueno-de-Mesquita B, Büchner FL, Boshuizen HC, Agudo A, Gram IT, Dahm CC, Overvad K, Egeberg R, Tjønneland A, Boeing H, Steffen A, Kaaks R, Lukanova A, Berrino F, Palli D, Panico S, Tumino R, Ardanaz E, Dorronsoro M, Huerta JM, Rodríguez L, Sánchez MJ, Rasmuson T, Hallmans G, Manjer J, Wirfält E, Engeset D, Skeie G, Katsoulis M, Oikonomou E, Trichopoulou A, Peeters PH, Khaw KT, Wareham N, Allen N, Key T, Brennan P, Romieu I, Slimani N, Vergnaud AC, Xun WW, Vineis P, Riboli E (2011) Consumption of meat and fish and risk of lung cancer: results from the European Prospective Investigation into Cancer and Nutrition. Cancer Causes Control 22(6):909–918

    Article  Google Scholar 

  25. Yang WS, Wong MY, Vogtmann E, Tang RQ, Xie L, Yang YS, Wu QJ, Zhang W, Xiang YB (2012) Meat consumption and risk of lung cancer: evidence from observational studies. Ann Oncol 23(12):3163–3170

    Article  CAS  Google Scholar 

  26. 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(6):1542–1553

    Google Scholar 

  27. Lim WY, Chuah KL, Eng P, Leong SS, Lim E, Lim TK, Ng A, Poh WT, Tee A, Teh M, Salim A, Seow A (2011) Meat consumption and risk of lung cancer among never-smoking women. Nutr Cancer 63(6):850–859

    Article  Google Scholar 

  28. Sofi F, Macchi C, Abbate R, Gensini GF, Casini A (2013) Mediterranean diet and health. Biofactors 39(4):335–342

    Article  CAS  Google Scholar 

  29. MacNee W (2013) Systemic inflammatory biomarkers and co-morbidities of chronic obstructive pulmonary disease. Ann Med 45(3):291–300

    Article  CAS  Google Scholar 

  30. Visioli F, Galli C (2001) The role of antioxidants in the Mediterranean diet. Lipids 36(Suppl):S49–S52

    Article  CAS  Google Scholar 

  31. Fonseca Wald EL, van den Borst B, Gosker HR, Schols AM (2014) Dietary fibre and fatty acids in chronic obstructive pulmonary disease risk and progression: a systematic review. Respirology 19(2):176–184

    Article  Google Scholar 

  32. di Giuseppe R, Arcari A, Serafini M, Di Castelnuovo A, Zito F, De Curtis A, Sieri S, Krogh V, Pellegrini N, Schünemann HJ, Donati MB, de Gaetano G, Iacoviello L, Moli-sani Project Investigators (2012) Total dietary antioxidant capacity and lung function in an Italian population: a favorable role in premenopausal/never smoker women. Eur J Clin Nutr 66(1):61–68

    Article  Google Scholar 

  33. Schwartz J (2000) Role of polyunsaturated fatty acids in lung disease. Am J Clin Nutr 71(1 Suppl):393S–396S

    CAS  Google Scholar 

  34. Gomes M, Teixeira AL, Coelho A, Araujo A, Medeiros R (2014) The role of inflammation in lung cancer. Adv Exp Med Biol 816:1–23

    Article  CAS  Google Scholar 

  35. Shiels MS, Katki HA, Freedman ND, Purdue MP, Wentzensen N, Trabert B, Kitahara CM, Furr M, Li Y, Kemp TJ, Goedert JJ, Chang CM, Engels EA, Caporaso NE, Pinto LA, Hildesheim A, Chaturvedi AK (2014) Cigarette smoking and variations in systemic immune and inflammation markers. J Natl Cancer Inst. doi:10.1093/jnci/dju294

    Google Scholar 

  36. Wood AD, Strachan AA, Thies F, Aucott LS, Reid DM, Hardcastle AC, Mavroeidi A, Simpson WG, Duthie GG, Macdonald HM (2014) Patterns of dietary intake and serum carotenoid and tocopherol status are associated with biomarkers of chronic low-grade systemic inflammation and cardiovascular risk. Br J Nutr 112(8):1341–1352

    Article  CAS  Google Scholar 

  37. Egan MB, Fragodt A, Raats MM, Hodgkins C, Lumbers M (2007) The importance of harmonizing food composition data across Europe. Eur J Clin Nutr 61(7):813–821

    Article  CAS  Google Scholar 

  38. Kelemen LE (2006) Food frequency questionnaires: not irrelevant yet. Cancer Epidemiol Biomarkers Prev 15(5):1054

    Article  Google Scholar 

  39. Hebert JR, Clemow L, Pbert L, Ockene IS, Ockene JK (1995) Social desirability bias in dietary self-report may compromise the validity of dietary intake measures. Int J Epidemiol 24(2):389–398

    Article  CAS  Google Scholar 

  40. Hebert JR, Ma Y, Clemow L, Ockene IS, Saperia G, Stanek EJ 3rd, Merriam PA, Ockene JK (1997) Gender differences in social desirability and social approval bias in dietary self report. Am J Epidemiol 146(12):1046–1055

    Article  CAS  Google Scholar 

  41. Hebert JR, Ebbeling CB, Matthews CE, Hurley TG, Ma Y, Druker S, Clemow L (2002) Systematic errors in middle-aged women’s estimates of energy intake: comparing three self-report measures to total energy expenditure from doubly labeled water. Ann Epidemiol 12(8):577–586

    Article  Google Scholar 

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Acknowledgments

This work was in part supported by the Italian Association for Cancer Research (AIRC), the Italian Foundation for Cancer Research (FIRC), and the European Institute of Oncology (IEO). Dr. Hébert was supported by an Established Investigator Award in Cancer Prevention and Control from the Cancer Training Branch of the National Cancer Institute (K05 CA136975).

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 a paid employee of CHI. The subject matter of this paper will not have any direct bearing on that work, nor has that activity exerted any influence on this project. On behalf of all other co-authors, the corresponding author states that there is no conflict of interest.

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Correspondence to Patrick Maisonneuve.

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Patrick Maisonneuve and Nitin Shivappa have contributed equally to this article and therefore share first-authorship.

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Maisonneuve, P., Shivappa, N., Hébert, J.R. et al. Dietary inflammatory index and risk of lung cancer and other respiratory conditions among heavy smokers in the COSMOS screening study. Eur J Nutr 55, 1069–1079 (2016). https://doi.org/10.1007/s00394-015-0920-3

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