Dietary quality using four dietary indices and lung cancer risk: the Golestan Cohort Study (GCS)

Abstract

Purpose

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.

Methods

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.

Results

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.

Conclusion

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.

Fig. 1

Data availability

Data described in the manuscript, code book, and analytic code will be made available upon request.

Abbreviations

AHEI-2010:

Alternative Healthy Eating Index-2010

AMED:

Alternate Mediterranean Diet

CI:

Confidence interval

CRP:

C-Reactive Protein

DASH:

Dietary Approach to Stop Hypertension

FFQ:

Food Frequency Questionnaire

GCS:

Golestan Cohort Study

HEI-2015:

Healthy Eating Index-2015

HR:

Hazard ratio

IL:

Interleukin

MUFAs:

Monounsaturated fatty acid

PUFAs:

Polyunsaturated fatty acids

SFA:

Saturated fatty acid

SSB:

Sugary-sweetened beverage

References

  1. 1.

    IIAOC Registry (2020) GLOBOCAN 2020 graph production: IARC. World Health Organization, Geneva

    Google Scholar 

  2. 2.

    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

    Article  PubMed  Google Scholar 

  3. 3.

    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

    Article  PubMed  Google Scholar 

  4. 4.

    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

  5. 5.

    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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  6. 6.

    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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  7. 7.

    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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  8. 8.

    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

    Article  PubMed  PubMed Central  Google Scholar 

  9. 9.

    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

    Article  PubMed  PubMed Central  Google Scholar 

  10. 10.

    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

    Article  PubMed  PubMed Central  Google Scholar 

  11. 11.

    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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  12. 12.

    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

    Article  PubMed  Google Scholar 

  13. 13.

    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

    Article  PubMed  Google Scholar 

  14. 14.

    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

    CAS  Article  PubMed  Google Scholar 

  15. 15.

    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

    CAS  Article  PubMed  Google Scholar 

  16. 16.

    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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  17. 17.

    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

    CAS  Article  PubMed  Google Scholar 

  18. 18.

    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

    CAS  Article  PubMed  Google Scholar 

  19. 19.

    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

    CAS  Article  PubMed  Google Scholar 

  20. 20.

    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

    CAS  Article  PubMed  Google Scholar 

  21. 21.

    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

    CAS  Article  PubMed  Google Scholar 

  22. 22.

    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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  23. 23.

    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

    Google Scholar 

  24. 24.

    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

    Article  PubMed  Google Scholar 

  25. 25.

    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

    PubMed  Google Scholar 

  26. 26.

    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

    Article  PubMed  PubMed Central  Google Scholar 

  27. 27.

    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

    CAS  Article  PubMed  Google Scholar 

  28. 28.

    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

    Google Scholar 

  29. 29.

    Division of Cancer Control and Population Sciences, National Cancer Institute (2020) Developing the healthy eating index. National Cancer Institute, Rockville

    Google Scholar 

  30. 30.

    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

  31. 31.

    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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  32. 32.

    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

    Article  PubMed  PubMed Central  Google Scholar 

  33. 33.

    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

    Article  PubMed  Google Scholar 

  34. 34.

    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

    Article  PubMed  PubMed Central  Google Scholar 

  35. 35.

    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

    Article  PubMed  PubMed Central  Google Scholar 

  36. 36.

    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

    CAS  Article  Google Scholar 

  37. 37.

    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

    Article  PubMed  Google Scholar 

  38. 38.

    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

    Article  PubMed  Google Scholar 

  39. 39.

    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

    Article  PubMed  PubMed Central  Google Scholar 

  40. 40.

    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

    CAS  Article  PubMed  Google Scholar 

Download references

Acknowledgments

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.

Funding

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.

Author information

Affiliations

Authors

Contributions

QW: Contributed to the data analysis and interpretation, and wrote the initial draft of the manuscript. MH: Contributed to the data analysis, dietary score calculation, and reviewed provided feedback to the manuscript. HP: Contributed to the intellectual input for design of GCS, field officer of GCS for data acquisition, and provided review and confirmation of the final version of the manuscript. MS: Contributed to the data analysis, dietary score calculation, and reviewed provided feedback to the manuscript. AP: Contributed to the intellectual input for design of GCS, field officer of GCS for data acquisition, and provided review and confirmation of the final version of the manuscript. SS: Contributed to the intellectual input for design of GCS follow-up, data cleaning and follow-up data acquisition, and provided review and confirmation of the final version of the manuscript. MK: Contributed to outcome assessment by collecting and reviewing file to make the final diagnosis during GCS follow-up, and provided review and confirmation of the final version of the manuscript. AG: Contributed to outcome assessment by collecting and reviewing file to make the final diagnosis during GCS follow-up, and provided review and confirmation of the final version of the manuscript. AFM: Contributed by design and validation of food frequency questioner for GCS, and provided review and confirmation of the final version of the manuscript. AE: Contributed to the intellectual input into the design and follow-up of GCS, and provided review and confirmation of the final version of the manuscript. FK: Contributed to the intellectual input into the design and follow-up of GCS, and provided review and confirmation of the final version of the manuscript. RM: Contributed to the intellectual input for the design of the experiments as well as accomplishment of Golestan cohort study. He supervised all data and biospecimen collection, and provided review and confirmation of the final version of the manuscript. PB: Contributed to the intellectual input for the design of the experiments as well as accomplishment of Golestan cohort study, and provided review and confirmation of the final version of the manuscript.

Corresponding author

Correspondence to Qian Wang.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Ethical approval

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.

Informed consent

A written informed consent was obtained from all study participants.

Additional information

Publisher's Note

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

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 51 KB)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

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

Download citation

Keywords

  • Dietary quality index
  • Lung cancer
  • Golestan cohort study
  • Cohort study
  • Opium consumption
  • Cigarette smoking