The lung cancer incidence in Iran has increased almost ten times over the past three decades. In addition to the known causes such as smoking and certain occupational exposure, dietary quality has been suggested to play a role in lung cancer. We aim to explore the association between dietary pattern and lung cancer risk among a Middle East population.
Data came from Golestan Cohort Study which included 48,421 participants with 136 lung cancer cases diagnosed during a median follow-up of 12 years. Multivariable Cox proportional hazards regression models were used to calculate the HRs and 95% CI of lung cancer risk by tertile of the four dietary index scores—the Health Eating Index (HEI)-2015, the Alternative Health Eating Index (AHEI)-2010, the Alternative Mediterranean Diet (AMED), and the Dietary Approach to Stop Hypertension (DASH)-Fung.
A higher DASH-Fung score was inversely associated with risk of lung cancer after adjusting for potential confounders (tertile three vs. tertile one: HR = 0.59 (0.38–0.93); p for trend = 0.07), and pinteraction with smoking was 0.46. Similar findings were observed among current smokers with the HEI-2015 score (tertile three vs. tertile one: HR = 0.22 (0.08–0.60): p for trend < 0.01), and pinteraction between smoking and the HEI-2015 score was 0.03.
In the GCS, consuming a diet more closely aligned with the DASH diet was associated with a reduced risk of lung cancer, which appeared to be independent of smoking status. There was also an inverse link between the HEI-2015 score and lung cancer risk among current smokers. Our finding is particularly important for the Middle East population, as diet may play an important role in cancer prevention and overall health.
This is a preview of subscription content, access via your institution.
Buy single article
Instant access to the full article PDF.
Tax calculation will be finalised during checkout.
Subscribe to journal
Immediate online access to all issues from 2019. Subscription will auto renew annually.
Tax calculation will be finalised during checkout.
Data described in the manuscript, code book, and analytic code will be made available upon request.
Alternative Healthy Eating Index-2010
Alternate Mediterranean Diet
Dietary Approach to Stop Hypertension
Food Frequency Questionnaire
Golestan Cohort Study
Healthy Eating Index-2015
Monounsaturated fatty acid
Polyunsaturated fatty acids
Saturated fatty acid
IIAOC Registry (2020) GLOBOCAN 2020 graph production: IARC. World Health Organization, Geneva
Rajai N, Ghanbari A, Yoosefi M, Mohebi F, Mohajer B, Sheidaei A, Gohari K, Masinaei M, Haghshenas R, Kompani F, Vaezi M, Farzadfar F (2020) National and subnational trends in incidence and mortality of lung cancer in Iran from 1990 to 2016. Asia Pac J Clin Oncol. https://doi.org/10.1111/ajco.13303
Sheikh M, Shakeri R, Poustchi H, Pourshams A, Etemadi A, Islami F, Khoshnia M, Gharavi A, Roshandel G, Khademi H, Sepanlou SG, Hashemian M, Fazel A, Zahedi M, Abedi-Ardekani B, Boffetta P, Dawsey SM, Pharoah PD, Sotoudeh M, Freedman ND, Abnet CC, Day NE, Brennan P, Kamangar F, Malekzadeh R (2020) Opium use and subsequent incidence of cancer: results from the Golestan Cohort Study. Lancet Global Health 8(5):e649–e660. https://doi.org/10.1016/s2214-109x(20)30059-0
World Cancer Research Fund/American Institute for Cancer Research (2018) Continuous update project expert report 2018. Wholegrains, vegetables and fruit and the risk of cancer. www.dietandcancerreport.org. Accessed 18 May 2020
Xue Y, Harris E, Wang W, Baybutt RC (2015) Vitamin A depletion induced by cigarette smoke is associated with an increase in lung cancer-related markers in rats. J Biomed Sci 22:84. https://doi.org/10.1186/s12929-015-0189-0
Tu H, Heymach JV, Wen CP, Ye Y, Pierzynski JA, Roth JA, Wu X (2016) Different dietary patterns and reduction of lung cancer risk: a large case-control study in the U.S. Sci Rep 6:26760. https://doi.org/10.1038/srep26760
Luo J, Shen L, Zheng D (2014) Association between vitamin C intake and lung cancer: a dose-response meta-analysis. Sci Rep 4:6161. https://doi.org/10.1038/srep06161
Krusinska B, Hawrysz I, Wadolowska L, Slowinska MA, Biernacki M, Czerwinska A, Golota JJ (2018) Associations of Mediterranean diet and a posteriori derived dietary patterns with breast and lung cancer risk: a case-control study. Nutrients. https://doi.org/10.3390/nu10040470
Schwingshackl L, Schwedhelm C, Galbete C, Hoffmann G (2017) Adherence to Mediterranean diet and risk of cancer: an updated systematic review and meta-analysis. Nutrients. https://doi.org/10.3390/nu9101063
Hashemian M, Farvid MS, Poustchi H, Murphy G, Etemadi A, Hekmatdoost A, Kamangar F, Sheikh M, Pourshams A, Sepanlou SG, Fazeltabar Malekshah A, Khoshnia M, Gharavi A, Brennan PJ, Boffetta P, Dawsey SM, Reedy J, Subar AF, Abnet CC, Malekzadeh R (2019) The application of six dietary scores to a Middle Eastern population: a comparative analysis of mortality in a prospective study. Eur J Epidemiol. https://doi.org/10.1007/s10654-019-00508-3
Ma Y, Yang W, Simon TG, Smith-Warner SA, Fung TT, Sui J, Chong D, VoPham T, Meyerhardt JA, Wen D, Giovannucci EL, Chan AT, Zhang X (2019) Dietary patterns and risk of hepatocellular carcinoma among U.S. men and women. Hepatology 70(2):577–586. https://doi.org/10.1002/hep.30362
Fung TT, Chiuve SE, McCullough ML, Rexrode KM, Logroscino G, Hu FB (2008) Adherence to a DASH-style diet and risk of coronary heart disease and stroke in women. Arch Intern Med 168(7):713–720. https://doi.org/10.1001/archinte.168.7.713
Milajerdi A, Namazi N, Larijani B, Azadbakht L (2018) The association of dietary quality indices and cancer mortality: a systematic review and meta-analysis of cohort studies. Nutr Cancer 70(7):1091–1105. https://doi.org/10.1080/01635581.2018.1502331
Schulpen M, van den Brandt PA (2018) Adherence to the Mediterranean diet and risk of lung cancer in the Netherlands Cohort Study. Br J Nutr 119(6):674–684. https://doi.org/10.1017/s0007114517003737
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
Hodge AM, Bassett JK, Shivappa N, Hebert JR, English DR, Giles GG, Severi G (2016) Dietary inflammatory index, Mediterranean diet score, and lung cancer: a prospective study. Cancer Causes Control 27(7):907–917. https://doi.org/10.1007/s10552-016-0770-1
Anic GM, Park Y, Subar AF, Schap TE, Reedy J (2016) Index-based dietary patterns and risk of lung cancer in the NIH-AARP diet and health study. Eur J Clin Nutr 70(1):123–129. https://doi.org/10.1038/ejcn.2015.122
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. https://doi.org/10.1093/annonc/mdt302
Dinu M, Pagliai G, Casini A, Sofi F (2018) Mediterranean diet and multiple health outcomes: an umbrella review of meta-analyses of observational studies and randomised trials. Eur J Clin Nutr 72(1):30–43. https://doi.org/10.1038/ejcn.2017.58
Guillermo C, Boushey CJ, Franke AA, Monroe KR, Lim U, Wilkens LR, Le Marchand L, Maskarinec G (2020) Diet quality and biomarker profiles related to chronic disease prevention: the Multiethnic Cohort Study. J Am Coll Nutr 39(3):216–223. https://doi.org/10.1080/07315724.2019.1635921
Fung TT, McCullough ML, Newby P, 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(1):163–173. https://doi.org/10.1093/ajcn.82.1.163
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(16):2719–2726. https://doi.org/10.1200/JCO.2009.27.0454
Office on Smoking and Health, National Center for Chronic Disease Prevention and Health Promotion (2019) Current cigarette smoking among adults in the United States. Center for Disease Control and Prevention, Atlanta
Pourshams A, Khademi H, Malekshah AF, Islami F, Nouraei M, Sadjadi AR, Jafari E, Rakhshani N, Salahi R, Semnani S, Kamangar F, Abnet CC, Ponder B, Day N, Dawsey SM, Boffetta P, Malekzadeh R (2010) Cohort profile: the Golestan Cohort Study–a prospective study of oesophageal cancer in northern Iran. Int J Epidemiol 39(1):52–59. https://doi.org/10.1093/ije/dyp161
Kafeshani O, Sarrafzadegan N, Nouri F, Mohammadifard N (2015) Major dietary patterns in Iranian adolescents: Isfahan Healthy Heart Program. Iran ARYA Atheroscler 11(Suppl 1):61–68
Sheikh M, Poustchi H, Pourshams A, Etemadi A, Islami F, Khoshnia M, Gharavi A, Hashemian M, Roshandel G, Khademi H, Zahedi M, Abedi-Ardekani B, Boffetta P, Kamangar F, Dawsey SM, Pharaoh PD, Abnet CC, Day NE, Brennan P, Malekzadeh R (2019) Individual and combined effects of environmental risk factors for esophageal cancer based on results from the Golestan Cohort Study. Gastroenterology. https://doi.org/10.1053/j.gastro.2018.12.024
Malekshah AF, Kimiagar M, Saadatian-Elahi M, Pourshams A, Nouraie M, Goglani G, Hoshiarrad A, Sadatsafavi M, Golestan B, Yoonesi A, Rakhshani N, Fahimi S, Nasrollahzadeh D, Salahi R, Ghafarpour A, Semnani S, Steghens JP, Abnet CC, Kamangar F, Dawsey SM, Brennan P, Boffetta P, Malekzadeh R (2006) Validity and reliability of a new food frequency questionnaire compared to 24 h recalls and biochemical measurements: pilot phase of Golestan cohort study of esophageal cancer. Eur J Clin Nutr 60(8):971–977. https://doi.org/10.1038/sj.ejcn.1602407
Fazel-Tabar Malekshah A, Zaroudi M, Etemadi A, Islami F, Sepanlou S, Sharafkhah M, Keshtkar AA, Khademi H, Poustchi H, Hekmatdoost A, Pourshams A, Feiz Sani A, Jafari E, Kamangar F, Dawsey SM, Abnet CC, Pharoah PD, Berennan PJ, Boffetta P, Esmaillzadeh A, Malekzadeh R (2016) The combined effects of healthy lifestyle behaviors on all-cause mortality: the Golestan Cohort Study. Archiv Iran Med 19(11):752–761
Division of Cancer Control and Population Sciences, National Cancer Institute (2020) Developing the healthy eating index. National Cancer Institute, Rockville
National Cancer Institute Epidemology and Genomics Research Program (2021) HEI-2015 dietary components, constituents, and scoring standards. https://www.fns.usda.gov/how-hei-scored. Accessed Jan 2021
Chiuve SE, Fung TT, Rimm EB, Hu FB, McCullough ML, Wang M, Stampfer MJ, Willett WC (2012) Alternative dietary indices both strongly predict risk of chronic disease. J Nutr 142(6):1009–1018. https://doi.org/10.3945/jn.111.157222
Varraso R, Chiuve SE, Fung TT, Barr RG, Hu FB, Willett WC, Camargo CA (2015) Alternate Healthy Eating Index 2010 and risk of chronic obstructive pulmonary disease among US women and men: prospective study. BMJ 350:h286–h286. https://doi.org/10.1136/bmj.h286
Andrianasolo RM, Kesse-Guyot E, Adjibade M, Hercberg S, Galan P, Varraso R (2018) Associations between dietary scores with asthma symptoms and asthma control in adults. Eur Respir J. https://doi.org/10.1183/13993003.02572-2017
Bosire C, Stampfer MJ, Subar AF, Park Y, Kirkpatrick SI, Chiuve SE, Hollenbeck AR, Reedy J (2013) Index-based Dietary patterns and the risk of prostate cancer in the NIH-AARP Diet and Health Study. Am J Epidemiol 177(6):504–513. https://doi.org/10.1093/aje/kws261
Petimar J, Park YM, Smith-Warner SA, Fung TT, Sandler DP (2019) Dietary index scores and invasive breast cancer risk among women with a family history of breast cancer. Am J Clin Nutr 109(5):1393–1401. https://doi.org/10.1093/ajcn/nqy392
Lavalette C, Adjibade M, Srour B, Sellem L, Fiolet T, Hercberg S, Latino-Martel P, Fassier P, Deschasaux M, Kesse-Guyot E, Touvier M (2018) Cancer-specific and general nutritional scores and cancer risk: results from the Prospective NutriNet-Sante Cohort. Can Res 78(15):4427–4435. https://doi.org/10.1158/0008-5472.CAN-18-0155
Etemadi A, Khademi H, Kamangar F, Freedman ND, Abnet CC, Brennan P, Malekzadeh R (2017) Hazards of cigarettes, smokeless tobacco and waterpipe in a Middle Eastern Population: a Cohort Study of 50 000 individuals from Iran. Tobacco Control 26(6):674–682. https://doi.org/10.1136/tobaccocontrol-2016-053245
Ma J, Strub P, Lv N, Xiao L, Camargo CA Jr, Buist AS, Lavori PW, Wilson SR, Nadeau KC, Rosas LG (2016) Pilot randomised trial of a healthy eating behavioural intervention in uncontrolled asthma. Eur Respir J 47(1):122–132. https://doi.org/10.1183/13993003.00591-2015
Qu YL, Liu J, Zhang LX, Wu CM, Chu AJ, Wen BL, Ma C, Yan XY, Zhang X, Wang DM, Lv X, Hou SJ (2017) Asthma and the risk of lung cancer: a meta-analysis. Oncotarget 8(7):11614–11620. https://doi.org/10.18632/oncotarget.14595
Crawford DC, Sanders CL, Qin X, Smith JD, Shephard C, Wong M, Witrak L, Rieder MJ, Nickerson DA (2006) Genetic variation is associated with C-reactive protein levels in the Third National Health and Nutrition Examination Survey. Circulation 114(23):2458–2465. https://doi.org/10.1161/CIRCULATIONAHA.106.615740
We thank all participants of the Golestan Cohort study for agreeing to be enrolled in the study and providing biological samples and follow-up data over many years. We also thank all the professionals including medical doctors, nurses, epidemiologists, and nutritionists involved in the recruitment of participants and collection and storage of biospecimens for their precious expertise; the Golestan Cohort Study Center staff; the local health networks and health workers (Behvarzes) in the study area; the Golestan University of Medical Sciences (Gorgan, Iran); and the chiefs of the Maraveh-tappeh, Gonbad, Kalaleh, and Aq-qala health districts for their assistance and support.
Golestan cohort study was funded by the Cancer Research UK (Grant Number: C20/A5860), Tehran University of Medical Sciences (Grant Number: 81/15), the International Agency for Research on Cancer, and the Intramural Research Program of the U.S. National Cancer Institute. The funders had no role in study design, collection, analysis, and interpretation of data, in manuscript writing or in submission process for publication.
Conflict of interest
The authors declare no conflict of interest.
The GCS was approved by the institutional review boards (IRB) of the Digestive Disease Research Institute of the Tehran University of Medical Sciences (reference number: FWA00001331), the International Agency for Research on Cancer (reference number: CN/23/3), and the US National Cancer Institute.
A written informed consent was obtained from all study participants.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Below is the link to the electronic supplementary material.
About this article
Cite this article
Wang, Q., Hashemian, M., Sepanlou, S.G. et al. Dietary quality using four dietary indices and lung cancer risk: the Golestan Cohort Study (GCS). Cancer Causes Control (2021). https://doi.org/10.1007/s10552-021-01400-w
- Dietary quality index
- Lung cancer
- Golestan cohort study
- Cohort study
- Opium consumption
- Cigarette smoking