Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Dietary inflammatory index and breast cancer risk: an updated meta-analysis of observational studies

European Journal of Clinical Nutrition volume 76, pages 1073–1087 (2022)Cite this article

Subjects

Abstract

This updated meta-analysis sought to determine whether the pro-inflammatory potential of diet is a risk factor for breast cancer (BrCa) development, for the first time focusing on the effects of design heterogeneity. The search was performed using Scopus, PubMed, and Embase databases. Data were extracted from twenty-one eligible studies, including eleven cohorts (336,085 participants/20,033 incidence cases), and ten case-control studies (9,833 cases/12,752controls). The random-effect was used to calculate the relative risk (RR) using STATA 16 software. The highest dietary inflammatory index (DII) vs. the lowest category showed 16% increased risk of BrCa (95% CI: 1.06–1.26; I2 = 62.8%, P (I2) < 0.001). This was notable in post-menopausal status (RR = 1.13, 95% CI: 1.04–1.22), women with body mass index (BMI) ≥ 30 kg/m2 (RR = 1.35, 95% CI: 1.07–1.63), and study populations from developing countries (RR = 1.79, 95% CI: 1.12–2.47). Methodological covariates were subject to subgroup meta-analyses and showed stronger results among case-control studies (RR = 1.50, 95% CI: 1.20–1.80), studies considered age-matched controls (RR = 1.56, 95% CI: 1.19–1.93) and hospital-based controls (RR = 2.11, 95% CI: 1.58–2.64), and cohort studies identified by prolong follow-up durations (RR = 1.13, 95% CI: 1.03–1.22). This updated meta-analysis highlighted the pro-inflammatory diet as a risk factor for BrCa, especially among women in post-menopausal status, obese groups, and developing countries. Meta-analysis in methodological subgroups could improve results, less affected by heterogeneity, and suggested subclassification with important implications for future epidemiological designs and even clinical management.

Access through your institution
Buy or subscribe

This is a preview of subscription content, access via your institution

Access options

Access through your institution

Buy this article

  • Purchase on SpringerLink
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: The PRISMA flowchart.
Fig. 2: Forest plot of the pooled meta-analysis for DII and breast cancer risk.
Fig. 3: Forest plots of pooled RRs for DII and breast cancer risk in strata of methodological covariates.
Fig. 4: Forest plots of pooled RRs for DII and breast cancer risk in strata of nutritional methodological covariates.
Fig. 5: Forest plots of the subgroup analyses for association between DII and breast cancer risk in strata of general, anthropometric, and physiologic covariates.
Fig. 6

Similar content being viewed by others

References

  1. McPherson K, Steel C, Dixon J. ABC of breast diseases: breast cancer—epidemiology, risk factors, and genetics. BMJ. 2000;321:624.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Tobias DK, Akinkuolie AO, Chandler PD, Lawler PR, Manson JE, Buring JE, et al. Markers of inflammation and incident breast cancer risk in the women’s health study. Am J Epidemiol. 2018;187:705–16.

    Article  PubMed  Google Scholar 

  3. Wang K, Karin M Tumor-elicited inflammation and colorectal cancer. Adv Cancer Res. 128: Elsevier; 2015. p. 173-96.

  4. Macciò A, Madeddu C. Inflammation and ovarian cancer. Cytokine. 2012;58:133–47.

    Article  PubMed  CAS  Google Scholar 

  5. Aggarwal BB, Vijayalekshmi R, Sung B. Targeting inflammatory pathways for prevention and therapy of cancer: short-term friend, long-term foe. Clin Cancer Res. 2009;15:425–30.

    Article  CAS  PubMed  Google Scholar 

  6. Multhoff G, Molls M, Radons J. Chronic inflammation in cancer development. Front Immunol. 2012;2:98.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Sollie S, Michaud DS, Sarker D, Karagiannis SN, Josephs DH, Hammar N, et al. Chronic inflammation markers are associated with risk of pancreatic cancer in the Swedish AMORIS cohort study. BMC Cancer. 2019;19:1–6.

    Article  CAS  Google Scholar 

  8. van’t Klooster CC, Ridker PM, Hjortnaes J, van Der Graaf Y, Asselbergs FW, Westerink J, et al. The relation between systemic inflammation and incident cancer in patients with stable cardiovascular disease: a cohort study. Eur Heart J. 2019;40:3901–9.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  9. Demb J, Wei EK, Izano M, Kritchevsky S, Swede H, Newman AB, et al. Chronic inflammation and risk of lung cancer in older adults in the health, aging and body composition cohort study. J Geriatr Oncol. 2019;10:265–71.

    Article  PubMed  Google Scholar 

  10. Taams LS. Inflammation and immune resolution. Clin Exp Immunol. 2018;193:1–2.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Perwez Hussain S, Harris CC. Inflammation and cancer: an ancient link with novel potentials. Int J Cancer. 2007;121:2373–80.

    Article  PubMed  CAS  Google Scholar 

  12. Jiang X, Shapiro DJ. The immune system and inflammation in breast cancer. Mol Cell Endocrinol. 2014;382:673–82.

    Article  CAS  PubMed  Google Scholar 

  13. Bhatelia K, Singh K, Singh R. TLRs: linking inflammation and breast cancer. Cell Signal. 2014;26:2350–7.

    Article  CAS  PubMed  Google Scholar 

  14. Cevenini E, Caruso C, Candore G, Capri M, Nuzzo D, Duro G, et al. Age-related inflammation: the contribution of different organs, tissues and systems. How to face it for therapeutic approaches. Curr Pharm Des. 2010;16:609–18.

    Article  CAS  PubMed  Google Scholar 

  15. Ferrante A Jr. Obesity‐induced inflammation: a metabolic dialogue in the language of inflammation. J Intern Med. 2007;262:408–14.

    Article  CAS  PubMed  Google Scholar 

  16. Chrysohoou C, Panagiotakos DB, Pitsavos C, Das UN, Stefanadis C. Adherence to the Mediterranean diet attenuates inflammation and coagulation process in healthy adults: The ATTICA Study. J Am Coll Cardiol. 2004;44:152–8.

    Article  PubMed  Google Scholar 

  17. Barbaresko J, Koch M, Schulze MB, Nöthlings U. Dietary pattern analysis and biomarkers of low-grade inflammation: a systematic literature review. Nutr Rev. 2013;71:511–27.

    Article  PubMed  Google Scholar 

  18. Shivappa N, Steck SE, Hurley TG, Hussey JR, Hébert JR. Designing and developing a literature-derived, population-based dietary inflammatory index. Public Health Nutr. 2014;17:1689–96.

    Article  PubMed  Google Scholar 

  19. Jang H, Chung M, Kang S, Park Y. Association between the dietary inflammatory index and risk for cancer recurrence and mortality among patients with breast cancer. Nutrients 2018;10:1095.

    Article  PubMed Central  CAS  Google Scholar 

  20. Huang W-Q, Mo X-F, Ye Y-B, Shivappa N, Lin F-Y, Huang J, et al. A higher Dietary Inflammatory Index score is associated with a higher risk of breast cancer among Chinese women: a case–control study. Br J Nutr. 2017;117:1358–67.

    Article  CAS  PubMed  Google Scholar 

  21. Ge I, Rudolph A, Shivappa N, Flesch-Janys D, Hebert JR, Chang-Claude J. Dietary inflammation potential and postmenopausal breast cancer risk in a German case-control study. Breast. 2015;24:491–6.

    Article  PubMed  Google Scholar 

  22. Zucchetto A, Serraino D, Shivappa N, Hébert JR, Stocco C, Puppo A, et al. Dietary inflammatory index before diagnosis and survival in an Italian cohort of women with breast cancer. Br J Nutr. 2017;117:1456–62.

    Article  CAS  PubMed  Google Scholar 

  23. Shivappa N, Sandin S, Löf M, Hébert JR, Adami H-O, Weiderpass E. Prospective study of dietary inflammatory index and risk of breast cancer in Swedish women. Br J Cancer. 2015;113:1099.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Shivappa N, Blair CK, Prizment AE, Jacobs DR, Hébert JR. Prospective study of the dietary inflammatory index and risk of breast cancer in postmenopausal women. Mol Nutr Food Res. 2017;61:1600592.

    Article  CAS  Google Scholar 

  25. Tabung FK, Steck SE, Liese AD, Zhang J, Ma Y, Johnson KC, et al. Patterns of change over time and history of the inflammatory potential of diet and risk of breast cancer among postmenopausal women. Breast Cancer Res Treat. 2016;159:139–49.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Tabung FK, Steck SE, Liese AD, Zhang J, Ma Y, Caan B, et al. Association between dietary inflammatory potential and breast cancer incidence and death: results from the Women’s Health Initiative. Br J Cancer. 2016;114:1277.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Shivappa N, Hébert JR, Rosato V, Montella M, Serraino D, La Vecchia C. Association between the dietary inflammatory index and breast cancer in a large Italian case–control study. Mol Nutr Food Res. 2017;61:1600500.

    Article  CAS  Google Scholar 

  28. Wang L, Liu C, Zhou C, Zhuang J, Tang S, Yu J, et al. Meta-analysis of the association between the dietary inflammatory index (DII) and breast cancer risk. Eur J Clin Nutr. 2019;73:509–17.

    Article  PubMed  Google Scholar 

  29. Jayedi A, Emadi A, Shab-Bidar S. Dietary inflammatory index and site-specific cancer risk: a systematic review and dose-response meta-analysis. Adv Nutr. 2018;9:388–403.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Zahedi H, Djalalinia S, Sadeghi O, Asayesh H, Noroozi M, Gorabi AM, et al. Dietary inflammatory potential score and risk of breast cancer: systematic review and meta-analysis. Clin Breast Cancer. 2018;18:e561–e70.

    Article  PubMed  Google Scholar 

  31. Liu Z-Y, Gao X-P, Zhu S, Liu Y-H, Wang L-J.JingC-X, et al. Dietary inflammatory index and risk of gynecological cancers: a systematic review and meta-analysis of observational studies. Gynecol Oncol. 2018;30:1–14.

    Google Scholar 

  32. Moradi S, Issah A, Mohammadi H, Mirzaei K. Associations between dietary inflammatory index and incidence of breast and prostate cancer: a systematic review and meta-analysis. Nutrition 2018;55:168–78.

    Article  PubMed  Google Scholar 

  33. Namazi N, Larijani B, Azadbakht L. Association between the dietary inflammatory index and the incidence of cancer: a systematic review and meta-analysis of prospective studies. Public Health. 2018;164:148–56.

    Article  CAS  PubMed  Google Scholar 

  34. Chen H, Gao Y, Wei N, Du K, Jia Q. Strong association between the dietary inflammatory index (DII) and breast cancer: a systematic review and meta-analysis. Aging. 2021;13:13039.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Aghababayan S, Mobarakeh ZS, Qorbani M, Tiznobeyk Z, Aminianfar A, Sotoudeh G. Higher dietary inflammatory index scores are associated with increased odds of Benign breast diseases in a case–control study. J Inflamm Res. 2020;13:61.

    Article  PubMed  PubMed Central  Google Scholar 

  36. Gardeazabal I, Ruiz-Canela M, Sánchez-Bayona R, Romanos-Nanclares A, Aramendía-Beitia J, Shivappa N, et al. Dietary inflammatory index and incidence of breast cancer in the SUN project. Clin Nutr. 2019;38:2259–68.

    Article  CAS  PubMed  Google Scholar 

  37. Graffouillere L, Deschasaux M, Mariotti F, Neufcourt L, Shivappa N, Hébert JR, et al. The dietary inflammatory index is associated with prostate cancer risk in French middle-aged adults in a prospective study. J Nutr. 2015;146:785–91.

    Article  CAS  Google Scholar 

  38. Jalali S, Shivappa N, Hébert JR, Heidari Z, Hekmatdoost A, Rashidkhani B. Dietary inflammatory index and odds of breast cancer in a case-control study from Iran. Nutr Cancer. 2018;70:1034–42.

    Article  PubMed  Google Scholar 

  39. Lee S, Quiambao AL, Lee J, Ro J, Lee E-S, Jung S-Y, et al. Dietary inflammatory index and risk of breast cancer based on hormone receptor status: a case-control study in Korea. Nutrients 2019;11:1949.

    Article  CAS  PubMed Central  Google Scholar 

  40. Niclis C, Shivappa N, Hébert JR, Tumas N, Díaz MDP. The inflammatory potential of diet is associated with breast cancer risk in urban Argentina: a multilevel analysis. Nutr Cancer. 2020;73:1–10.

    Google Scholar 

  41. Obón-Santacana M, Romaguera D, Gracia-Lavedan E, Molinuevo A, Molina-Montes E, Shivappa N, et al. Dietary inflammatory index, dietary non-enzymatic antioxidant capacity, and colorectal and breast cancer risk (MCC-Spain Study). Nutrients. 2019;11:1406.

    Article  PubMed Central  CAS  Google Scholar 

  42. Vahid F, Shivappa N, Hatami M, Sadeghi M, Ameri F, Naeini YJ, et al. Association between dietary inflammatory index (DII) and risk of breast cancer: a case-control study. Asian Pac J Cancer Prev. 2018;19:1215.

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Wang K, Sun J-Z, Wu Q-X, Li Z-Y, Li D-X, Xiong Y-F, et al. Long-term anti-inflammatory diet in relation to improved breast cancer prognosis: a prospective cohort study. NPJ Breast Cancer. 2020;6:1–11.

    Article  CAS  Google Scholar 

  44. Zheng J, Tabung FK, Zhang J, Liese AD, Shivappa N, Ockene JK, et al. Association between post-cancer diagnosis dietary inflammatory potential and mortality among invasive breast cancer survivors in the Women’s Health Initiative. Cancer Epidemiol Biomark Prev. 2018;27:454–63.

    Article  CAS  Google Scholar 

  45. Park YMM, Shivappa N, Petimar J, Hodgson ME, Nichols HB, Steck SE. et al. Dietary inflammatory potential, oxidative balance score, and risk of breast cancer: findings from the Sister Study. Int J Cancer. 2021;149:615–26.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Hajji-Louati M, Cordina-Duverger E, Laouali N, Mancini F-R, Guénel P. A case–control study in France showing that a pro-inflammatory diet is associated with a higher risk of breast cancer. Sci Rep. 2021;11:1–10.

    Article  CAS  Google Scholar 

  47. Schröder J. Face-to-Face Surveys (Version 2.0). 2016.

  48. Shim J-S, Oh K, Kim HC. Dietary assessment methods in epidemiologic studies. Epidemiol Health. 2014;36:1–8.

    Article  Google Scholar 

  49. Kuo C-L, Duan Y, Grady J. Unconditional or conditional logistic regression model for age-matched case–control data? Front Public Health. 2018;6:57.

    Article  PubMed  PubMed Central  Google Scholar 

  50. Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ. 2003;327:557–60.

    Article  PubMed  PubMed Central  Google Scholar 

  51. Honma S, Shimodaria K, Shimizu Y, Tsuchiya N, Saito H, Yanaihara T, et al. The influence of inflammatory cytokines on estrogen production and cell proliferation in human breast cancer cells. Endocr J. 2002;49:371–7.

    Article  CAS  PubMed  Google Scholar 

  52. Macciò A, CObesity Madeddu. inflammation, and postmenopausal breast cancer: therapeutic implications. Sci World J. 2011;11:2020–36.

    Article  Google Scholar 

  53. Yue W, Wang JP, Li Y, Fan P, Liu G, Zhang N, et al. Effects of estrogen on breast cancer development: role of estrogen receptor independent mechanisms. Int J Cancer. 2010;127:1748–57.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Livesey G, Taylor R, Livesey HF, Buyken AE, Jenkins DJ, Augustin LS, et al. Dietary glycemic index and load and the risk of type 2 diabetes: a systematic review and updated meta-analyses of prospective cohort studies. Nutrients. 2019;11:1280.

    Article  CAS  PubMed Central  Google Scholar 

  55. Fowler ME, Akinyemiju TF. Meta‐analysis of the association between dietary inflammatory index (DII) and cancer outcomes. Int J Cancer. 2017;141:2215–27.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Moher D, Liberati A, Tetzlaff J, Altman DG, Group P. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLOS Med. 2009;6:e1000097.

    Article  PubMed  PubMed Central  Google Scholar 

  57. Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol. 2010;25:603–5.

    Article  PubMed  Google Scholar 

  58. Higgins JP, Thomas J, Chandler J, Cumpston M, Li T, Page MJ, et al. Cochrane handbook for systematic reviews of interventions. Chichester (UK); John Wiley & Sons; 2019.

  59. Sterne JA Meta-analysis in Stata: an updated collection from the Stata Journal: StataCorp LP; 2009.

  60. Duval S, Tweedie R. Trim and fill: a simple funnel‐plot–based method of testing and adjusting for publication bias in meta‐analysis. Biometrics. 2000;56:455–63.

    Article  CAS  PubMed  Google Scholar 

  61. Nordmann AJ, Kasenda B, Briel M. Meta-analyses: what they can and cannot do. Swiss Med Wkly. 2012;142:1–11.

    Google Scholar 

  62. Swan SH, Shaw GM, Schulman J. Reporting and selection bias in case-control studies of congenital malformations. Epidemiology. 1992;3:356–63.

    Article  CAS  PubMed  Google Scholar 

  63. Song JW, Chung KC. Observational studies: cohort and case-control studies. Plast Reconstr Surg. 2010;126:2234.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Neupane B, Walter SD, Krueger P, Loeb M. Community controls were preferred to hospital controls in a case–control study where the cases are derived from the hospital. J Clin Epidemiol. 2010;63:926–31.

    Article  PubMed  Google Scholar 

  65. Li L, Zhang M. Population versus hospital controls for case-control studies on cancers in Chinese hospitals. BMC Med Res Methodol. 2011;11:167.

    Article  PubMed  PubMed Central  Google Scholar 

  66. Savy M, Martin-Prével Y, Traissac P, Eymard-Duvernay S, Delpeuch F. Dietary diversity scores and nutritional status of women change during the seasonal food shortage in rural Burkina Faso. J Nutr. 2006;136:2625–32.

    Article  CAS  PubMed  Google Scholar 

  67. Betensky RA. Measures of follow-up in time-to-event studies: why provide them and what should they be? Clin Trials. 2015;12:403–8.

    Article  PubMed  PubMed Central  Google Scholar 

  68. Sun Y-S, Zhao Z, Yang Z-N, Xu F, Lu H-J, Zhu Z-Y, et al. Risk factors and preventions of breast cancer. Int J Biol Sci. 2017;13:1387.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Shivappa N, Steck SE, Hurley TG, Hussey JR, Ma Y, Ockene IS, et al. A population-based dietary inflammatory index predicts levels of C-reactive protein in the Seasonal Variation of Blood Cholesterol Study (SEASONS). Public Health Nutr. 2014;17:1825–33.

    Article  PubMed  Google Scholar 

  70. Capellino S, Straub RH, Cutolo M. Aromatase and regulation of the estrogen‐to‐androgen ratio in synovial tissue inflammation: common pathway in both sexes. Ann NY Acad Sci. 2014;1317:24–31.

    Article  CAS  PubMed  Google Scholar 

  71. West KM, Blacksher E, Burke W. Genomics, health disparities, and missed opportunities for the nation’s research agenda. JAMA. 2017;317:1831–2.

    Article  PubMed  PubMed Central  Google Scholar 

  72. IntHout J, Ioannidis JP, Borm GF, Goeman JJ. Small studies are more heterogeneous than large ones: a meta-meta-analysis. J Clin Epidemiol. 2015;68:860–9.

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Molecular Medicine Research Center, Biomedicine Institute, Tabriz University of Medical Sciences, Tabriz, 5166614711, Iran

    Zahra Hayati & Saeed Pirouzpanah

  2. Department of Biochemistry and Dietetics, Faculty of Nutrition and Food Sciences, Tabriz University of Medical Sciences, Tabriz, 5166614711, Iran

    Zahra Hayati & Saeed Pirouzpanah

  3. Department of Statistics and Epidemiology, School of Medicine, Zanjan University of Medical Sciences, Zanjan 4513956111, Iran

    Mohammad Asghari Jafarabadi

  4. Road Traffic Injury Research Center, Tabriz University of Medical Sciences, Tabriz, 5166614711, Iran

    Mohammad Asghari Jafarabadi

Authors
  1. Zahra Hayati
    View author publications

    Search author on:PubMed Google Scholar

  2. Mohammad Asghari Jafarabadi
    View author publications

    Search author on:PubMed Google Scholar

  3. Saeed Pirouzpanah
    View author publications

    Search author on:PubMed Google Scholar

Contributions

S.P. and Z.H. contributed to the conception of the study, design, data collections, statistical analysis, data interpretation, and drafting of this manuscript. M.A.J. contributed to the statistical analysis. All authors read and approved the final version of the manuscript.

Corresponding author

Correspondence to Saeed Pirouzpanah.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

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

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hayati, Z., Jafarabadi, M.A. & Pirouzpanah, S. Dietary inflammatory index and breast cancer risk: an updated meta-analysis of observational studies. Eur J Clin Nutr 76, 1073–1087 (2022). https://doi.org/10.1038/s41430-021-01039-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue date:

  • DOI: https://doi.org/10.1038/s41430-021-01039-5

This article is cited by

Search

Advanced search

Quick links