Skip to main content
Top
Published in: European Journal of Nutrition 7/2019

01-10-2019 | Original Contribution

Association between inflammatory potential of diet and risk of lung cancer among smokers in a prospective study in Singapore

Authors: Nitin Shivappa, Renwei Wang, James R. Hébert, Aizhen Jin, Woon-Puay Koh, Jian Min Yuan

Published in: European Journal of Nutrition | Issue 7/2019

Login to get access

Abstract

Background

Diet and inflammation have been suggested to be important risk factors for lung cancer. We examined the ability of the dietary inflammatory index (DII®) to predict lung cancer in the Singapore Chinese Health Study (SCHS). The DII is a diet quality index based on the literature linking foods and nutrients with inflammatory biomarkers.

Patients and methods

Using data from the SCHS for 60,232 participants, including 1851 lung cancer cases, we investigated the associations of baseline DII scores calculated from a food frequency questionnaire with risk of developing lung cancer over an average of 17.6 years of follow-up. Hazard ratios (HR) were estimated using Cox regression, adjusting for smoking status and other risk factors.

Results

After excluding cancers diagnosed in the first 2 years of follow-up, the DII was non-significantly associated with risk of lung cancer (HRQ5vsQ1 = 1.13; 95% CI 0.94–1.35; P-trend = 0.24) after adjusting for age, dialect group, sex, interview year, education, body mass index, total calorie intake, physical activity and various smoking variables. In stratified analysis, stronger, statistically significant associations were evident in current smokers (HR 1.44; 95% CI 1.11–1.86; Ptrend = 0.03, P for interaction = 0.003) and in male ever-smokers (HRQ5vsQ1 = 1.37; 95% CI 1.07–1.77; P-trend = 0.03).

Conclusion

A pro-inflammatory diet, as shown by higher DII scores, is associated with an elevated risk of lung cancer for subjects with a history of smoking. Public health measures should be adopted to promote consumption of a healthy, anti-inflammatory diet to reduce the risk of lung cancer, especially in current and former smokers.
Appendix
Available only for authorised users
Literature
2.
go back to reference Singapore Cancer Registry, Interim Annual Report (Trends in Cancer Incidence in Singapore 2010–2014) Singapore Cancer Registry, Interim Annual Report (Trends in Cancer Incidence in Singapore 2010–2014)
7.
go back to reference Monographs on the evaluation of carcinogenic risks to humans (2004) International Agency for Research on Cancer (IARC) volume 83 (Tobacco smoke and involuntary smoking, Lyon, France) Monographs on the evaluation of carcinogenic risks to humans (2004) International Agency for Research on Cancer (IARC) volume 83 (Tobacco smoke and involuntary smoking, Lyon, France)
10.
go back to reference de Mello VD, Schwab U, Kolehmainen M, Koenig W, Siloaho M, Poutanen K, Mykkanen H, Uusitupa M (2011) A diet high in fatty fish, bilberries and wholegrain products improves markers of endothelial function and inflammation in individuals with impaired glucose metabolism in a randomised controlled trial: the Sysdimet study. Diabetologia 54(11):2755–2767CrossRef de Mello VD, Schwab U, Kolehmainen M, Koenig W, Siloaho M, Poutanen K, Mykkanen H, Uusitupa M (2011) A diet high in fatty fish, bilberries and wholegrain products improves markers of endothelial function and inflammation in individuals with impaired glucose metabolism in a randomised controlled trial: the Sysdimet study. Diabetologia 54(11):2755–2767CrossRef
11.
go back to reference Khoo J, Piantadosi C, Duncan R, Worthley SG, Jenkins A, Noakes M, Worthley MI, Lange K, Wittert GA (2011) Comparing effects of a low-energy diet and a high-protein low-fat diet on sexual and endothelial function, urinary tract symptoms, and inflammation in obese diabetic men. J Sex Med 8(10):2868–2875CrossRef Khoo J, Piantadosi C, Duncan R, Worthley SG, Jenkins A, Noakes M, Worthley MI, Lange K, Wittert GA (2011) Comparing effects of a low-energy diet and a high-protein low-fat diet on sexual and endothelial function, urinary tract symptoms, and inflammation in obese diabetic men. J Sex Med 8(10):2868–2875CrossRef
13.
go back to reference Estruch R, Martinez-Gonzalez MA, Corella D, Salas-Salvado J, Ruiz-Gutierrez V, Covas MI, Fiol M, Gomez-Gracia E, Lopez-Sabater MC, Vinyoles E, Aros F, Conde M, Lahoz C, Lapetra J, Saez G, Ros E (2006) Effects of a Mediterranean-style diet on cardiovascular risk factors: a randomized trial. Ann Intern Med 145(1):1–11CrossRef Estruch R, Martinez-Gonzalez MA, Corella D, Salas-Salvado J, Ruiz-Gutierrez V, Covas MI, Fiol M, Gomez-Gracia E, Lopez-Sabater MC, Vinyoles E, Aros F, Conde M, Lahoz C, Lapetra J, Saez G, Ros E (2006) Effects of a Mediterranean-style diet on cardiovascular risk factors: a randomized trial. Ann Intern Med 145(1):1–11CrossRef
14.
go back to reference Johansson-Persson A, Ulmius M, Cloetens L, Karhu T, Herzig KH, Onning G (2013) A high intake of dietary fiber influences C-reactive protein and fibrinogen, but not glucose and lipid metabolism, in mildly hypercholesterolemic subjects. Eur J Nutr 7:7 Johansson-Persson A, Ulmius M, Cloetens L, Karhu T, Herzig KH, Onning G (2013) A high intake of dietary fiber influences C-reactive protein and fibrinogen, but not glucose and lipid metabolism, in mildly hypercholesterolemic subjects. Eur J Nutr 7:7
17.
go back to reference Cavicchia PP, Steck SE, Hurley TG, Hussey JR, Ma Y, Ockene IS, Hébert JR (2009) A new dietary inflammatory index predicts interval changes in high-sensitivity c-reactive protein. J Nutr 139(12):2365–2372CrossRef Cavicchia PP, Steck SE, Hurley TG, Hussey JR, Ma Y, Ockene IS, Hébert JR (2009) A new dietary inflammatory index predicts interval changes in high-sensitivity c-reactive protein. J Nutr 139(12):2365–2372CrossRef
20.
go back to reference Shivappa N, Hebert JR, Marcos A, Diaz LE, Gomez S, Nova E, Michels N, Arouca A, Gonzalez-Gil E, Frederic G, Gonzalez-Gross M, Castillo MJ, Manios Y, Kersting M, Gunter MJ, De Henauw S, Antonios K, Widhalm K, Molnar D, Moreno L, Huybrechts I (2017) Association between dietary inflammatory index and inflammatory markers in the HELENA study. Mol Nutr Res. https://doi.org/10.1002/mnfr.201600707 CrossRef Shivappa N, Hebert JR, Marcos A, Diaz LE, Gomez S, Nova E, Michels N, Arouca A, Gonzalez-Gil E, Frederic G, Gonzalez-Gross M, Castillo MJ, Manios Y, Kersting M, Gunter MJ, De Henauw S, Antonios K, Widhalm K, Molnar D, Moreno L, Huybrechts I (2017) Association between dietary inflammatory index and inflammatory markers in the HELENA study. Mol Nutr Res. https://​doi.​org/​10.​1002/​mnfr.​201600707 CrossRef
22.
go back to reference Vahid F, Shivappa N, Hekmatdoost A, Hebert JR, Davoodi SH, Sadeghi M (2017) Association between Maternal Dietary Inflammatory Index (DII) and Abortion in Iranian Women and Validation of DII with serum concentration of inflammatory factors: case–control study. Appl Physiol Nutr Metab 42 (5):511–516. https://doi.org/10.1139/apnm-2016-0274 CrossRefPubMed Vahid F, Shivappa N, Hekmatdoost A, Hebert JR, Davoodi SH, Sadeghi M (2017) Association between Maternal Dietary Inflammatory Index (DII) and Abortion in Iranian Women and Validation of DII with serum concentration of inflammatory factors: case–control study. Appl Physiol Nutr Metab 42 (5):511–516. https://​doi.​org/​10.​1139/​apnm-2016-0274 CrossRefPubMed
23.
25.
go back to reference Wirth MD, Burch J, Shivappa N, Violanti JM, Burchfiel CM, Fekedulegn D, Andrew ME, Hartley TA, Miller DB, Mnatsakanova A, Charles LE, Steck SE, Hurley TG, Vena JE, Hebert JR (2014) Association of a dietary inflammatory index with inflammatory indices and metabolic syndrome among police officers. J Occup Environ Med Am Coll Occup Environ Med 56(9):986–989. https://doi.org/10.1097/JOM.0000000000000213 CrossRef Wirth MD, Burch J, Shivappa N, Violanti JM, Burchfiel CM, Fekedulegn D, Andrew ME, Hartley TA, Miller DB, Mnatsakanova A, Charles LE, Steck SE, Hurley TG, Vena JE, Hebert JR (2014) Association of a dietary inflammatory index with inflammatory indices and metabolic syndrome among police officers. J Occup Environ Med Am Coll Occup Environ Med 56(9):986–989. https://​doi.​org/​10.​1097/​JOM.​0000000000000213​ CrossRef
27.
go back to reference Shivappa N, Godos J, Hébert J, Wirth M, Piuri G, Speciani A, Grosso G (2017) Dietary Inflammatory index and colorectal cancer risk—a meta-analysis. Nutrients 9(9):1043CrossRef Shivappa N, Godos J, Hébert J, Wirth M, Piuri G, Speciani A, Grosso G (2017) Dietary Inflammatory index and colorectal cancer risk—a meta-analysis. Nutrients 9(9):1043CrossRef
34.
go back to reference Maisonneuve P, Shivappa N, Hebert JR, Bellomi M, Rampinelli C, Bertolotti R, Spaggiari L, Palli D, Veronesi G, Gnagnarella P (2016) Dietary inflammatory index and risk of lung cancer and other respiratory conditions among heavy smokers in the COSMOS screening study. Eur J Nutr 55(3):1069–1079. https://doi.org/10.1007/s00394-015-0920-3 CrossRefPubMed Maisonneuve P, Shivappa N, Hebert JR, Bellomi M, Rampinelli C, Bertolotti R, Spaggiari L, Palli D, Veronesi G, Gnagnarella P (2016) Dietary inflammatory index and risk of lung cancer and other respiratory conditions among heavy smokers in the COSMOS screening study. Eur J Nutr 55(3):1069–1079. https://​doi.​org/​10.​1007/​s00394-015-0920-3 CrossRefPubMed
35.
go back to reference Robbins CS, Pouladi MA, Fattouh R, Dawe DE, Vujicic N, Richards CD, Jordana M, Inman MD, Stampfli MR (2005) Mainstream cigarette smoke exposure attenuates airway immune inflammatory responses to surrogate and common environmental allergens in mice, despite evidence of increased systemic sensitization. J Immunol 175(5):2834–2842CrossRef Robbins CS, Pouladi MA, Fattouh R, Dawe DE, Vujicic N, Richards CD, Jordana M, Inman MD, Stampfli MR (2005) Mainstream cigarette smoke exposure attenuates airway immune inflammatory responses to surrogate and common environmental allergens in mice, despite evidence of increased systemic sensitization. J Immunol 175(5):2834–2842CrossRef
43.
go back to reference Seow A, Shi CY, Chung FL, Jiao D, Hankin JH, Lee HP, Coetzee GA, Yu MC (1998) Urinary total isothiocyanate (ITC) in a population-based sample of middle-aged and older Chinese in Singapore: relationship with dietary total ITC and glutathione S-transferase M1/T1/P1 genotypes. Cancer Epidemiol Biomark Prev 7(9):775–781 Seow A, Shi CY, Chung FL, Jiao D, Hankin JH, Lee HP, Coetzee GA, Yu MC (1998) Urinary total isothiocyanate (ITC) in a population-based sample of middle-aged and older Chinese in Singapore: relationship with dietary total ITC and glutathione S-transferase M1/T1/P1 genotypes. Cancer Epidemiol Biomark Prev 7(9):775–781
50.
go back to reference Fosslien E (2000) Molecular pathology of cyclooxygenase-2 in neoplasia. Ann Clin Lab Sci 30(1):3–21PubMed Fosslien E (2000) Molecular pathology of cyclooxygenase-2 in neoplasia. Ann Clin Lab Sci 30(1):3–21PubMed
54.
go back to reference Palaniappan U, Starkey LJ, O’Loughlin J, Gray-Donald K (2001) Fruit and vegetable consumption is lower and saturated fat intake is higher among Canadians reporting smoking. J Nutr 131(7):1952–1958CrossRef Palaniappan U, Starkey LJ, O’Loughlin J, Gray-Donald K (2001) Fruit and vegetable consumption is lower and saturated fat intake is higher among Canadians reporting smoking. J Nutr 131(7):1952–1958CrossRef
56.
go back to reference Kiefer Ingrid R, Theres MK (June 2005) Eating and dieting differences in men and women. J Men’s Health Gender 2(2):194–201CrossRef Kiefer Ingrid R, Theres MK (June 2005) Eating and dieting differences in men and women. J Men’s Health Gender 2(2):194–201CrossRef
58.
go back to reference Yuan JM, Butler LM, Gao YT, Murphy SE, Carmella SG, Wang R, Nelson HH, Hecht SS (2014) Urinary metabolites of a polycyclic aromatic hydrocarbon and volatile organic compounds in relation to lung cancer development in lifelong never smokers in the Shanghai Cohort Study. Carcinogenesis 35(2):339–345. https://doi.org/10.1093/carcin/bgt352 CrossRefPubMed Yuan JM, Butler LM, Gao YT, Murphy SE, Carmella SG, Wang R, Nelson HH, Hecht SS (2014) Urinary metabolites of a polycyclic aromatic hydrocarbon and volatile organic compounds in relation to lung cancer development in lifelong never smokers in the Shanghai Cohort Study. Carcinogenesis 35(2):339–345. https://​doi.​org/​10.​1093/​carcin/​bgt352 CrossRefPubMed
60.
go back to reference Kennedy ET, Ohls J, Carlson S, Fleming K (1995) The healthy eating index: design and applications. J Am Diet Assoc 95(10):1103–1108CrossRef Kennedy ET, Ohls J, Carlson S, Fleming K (1995) The healthy eating index: design and applications. J Am Diet Assoc 95(10):1103–1108CrossRef
61.
go back to reference Jackson M, Tulloch-Reid M, Walker S, McFarlane-Anderson N, Bennett F, Francis D, Coard K (2013) Dietary patterns as predictors of prostate cancer in Jamaican men. Nutr Cancer 65(3):367–374CrossRef Jackson M, Tulloch-Reid M, Walker S, McFarlane-Anderson N, Bennett F, Francis D, Coard K (2013) Dietary patterns as predictors of prostate cancer in Jamaican men. Nutr Cancer 65(3):367–374CrossRef
65.
go back to reference 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):1542–1553PubMedPubMedCentral 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):1542–1553PubMedPubMedCentral
67.
go back to reference Sijtsma FP, Meyer KA, Steffen LM, Shikany JM, Van Horn L, Harnack L, Kromhout D, Jacobs DR Jr (2012) Longitudinal trends in diet and effects of sex, race, and education on dietary quality score change: the Coronary Artery Risk Development in Young Adults study. Am J Clin Nutr 95(3):580–586CrossRef Sijtsma FP, Meyer KA, Steffen LM, Shikany JM, Van Horn L, Harnack L, Kromhout D, Jacobs DR Jr (2012) Longitudinal trends in diet and effects of sex, race, and education on dietary quality score change: the Coronary Artery Risk Development in Young Adults study. Am J Clin Nutr 95(3):580–586CrossRef
69.
70.
go back to reference Hodge AM, Bassett JK, Dugue PA, Shivappa N, Hebert JR, Milne RL, English DR, Giles GG (2018) Dietary inflammatory index or Mediterranean diet score as risk factors for total and cardiovascular mortality. Nutr Metab Cardiovasc Dis 28(5):461–469CrossRef Hodge AM, Bassett JK, Dugue PA, Shivappa N, Hebert JR, Milne RL, English DR, Giles GG (2018) Dietary inflammatory index or Mediterranean diet score as risk factors for total and cardiovascular mortality. Nutr Metab Cardiovasc Dis 28(5):461–469CrossRef
71.
go back to reference Dugué P-A, Hodge AM, Brinkman MT, Bassett JK, Shivappa N, Hebert JR, Hopper JL, English DR, Milne RL, Giles GG (2016) Association between selected dietary scores and the risk of urothelial cell carcinoma: A prospective cohort study. Int J Cancer 139(6):1251–1260CrossRef Dugué P-A, Hodge AM, Brinkman MT, Bassett JK, Shivappa N, Hebert JR, Hopper JL, English DR, Milne RL, Giles GG (2016) Association between selected dietary scores and the risk of urothelial cell carcinoma: A prospective cohort study. Int J Cancer 139(6):1251–1260CrossRef
Metadata
Title
Association between inflammatory potential of diet and risk of lung cancer among smokers in a prospective study in Singapore
Authors
Nitin Shivappa
Renwei Wang
James R. Hébert
Aizhen Jin
Woon-Puay Koh
Jian Min Yuan
Publication date
01-10-2019
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Nutrition / Issue 7/2019
Print ISSN: 1436-6207
Electronic ISSN: 1436-6215
DOI
https://doi.org/10.1007/s00394-018-1825-8

Other articles of this Issue 7/2019

European Journal of Nutrition 7/2019 Go to the issue