Document Type : Review Article

Authors

1 Department of Internal Medicine, School of Medicine, Hazrat-e Rasool General Hospital, Iran University of Medical Sciences, Tehran, Iran

2 Department of Public Health, Torbat Jam Faculty of Medical Sciences, Torbat Jam, Iran

3 Department of Food Hygiene and Quality Control, Division of Epidemiology and Zoonoses, Faculty of Veterinary Medicine, University of Tehran, Tehran, Iran

4 Faculty of Medicine, Iran University of Medical Sciences, Tehran, Iran

Abstract

Background: Breast cancer (BC) is the most prevalent neoplasm in females globally, with an increasing incidence trend almost in all regions. Previous studies have indicated that non-alcoholic fatty liver disease (NAFLD) may be an emerging risk factor for extrahepatic cancers, including BC. This systematic review and meta-analysis study aimed to determine the association between NAFLD and the development of BC.
Method: Data were systematically collected without time limitation until 21 April 2022, from the following electronic databases: Pub Med, Scopus, Embase, Web of Science, and Google Scholar. The association between NAFLD and BC with odds ratio (OR) was calculated with a 95% confidence interval and presented via forest plots. Hazard ratios along with incidence rate ratios in the cohort studies transformed into OR.
Results: According to the preferred reporting items for systematic reviews and meta-analyses (PRISMA) and the inclusion criteria herein, 11 eligible studies were obtained from various countries. The pooled OR of NAFLD as a risk of developing BC, using a random-effects model, was estimated at 1.61 (95% CI: 1.30-2.00) (Q-value: 51.35, I2 = 80.52%, P < 0.0001). Multivariate meta-regression analysis showed that the publication year-, country-, detection method-, study design-, and body mass index-adjusted status did not cause heterogeneity. The Egger's regression (P = 0.32) and the symmetry in the funnel plot showed no publication bias in the studies.
Conclusion: The present research revealed that NAFLD had a significant association with BC independent of traditional risk factors.

Keywords

This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination, and proofreading process, which may lead to differences between this version and the Version of Record. Please cite this article as doi:10.30476/mejc.2023.95903.1795

  1. Chen Z, Xu L, Shi W, Zeng F, Zhuo R, Hao X, et al. Trends of female and male breast cancer incidence at the global, regional, and national levels, 1990-2017. Breast Cancer Res Treat. 2020;180(2):481-90. doi: 10.1007/s10549-020-05561-1.
  2. Abulkhair O, Saghir N, Sedky L, Saadedin A, Elzahwary H, Siddiqui N, et al. Modification and implementation of NCCN guidelines on breast cancer in the Middle East and North Africa region. J Natl Compr Canc Netw. 2010;8 Suppl 3:S8-S15. doi: 10.6004/jnccn.2010.0126.
  3. Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;68(6):394-424. doi: 10.3322/caac.21492. Erratum in: CA Cancer J Clin. 2020;70(4):313.
  4. Azamjah N, Soltan-Zadeh Y, Zayeri F. Global trend of breast cancer mortality rate: a 25-year study. Asian Pac J Cancer Prev. 2019;20(7):2015-2020. doi: 10.31557/APJCP.2019.20.7.2015.
  5. Hong C, Yan Y, Su L, Chen D, Zhang C. Development of a risk-stratification scoring system for predicting risk of breast cancer based on non-alcoholic fatty liver disease, non-alcoholic fatty pancreas disease, and uric acid. Open Med (Wars). 2022;17(1):619-25. doi: 10.1515/med-2022-0462.
  6. Govindan R, DeVita VT. DeVita, Hellman, and Rosenberg's cancer: principles & practice of oncology review. In: DePinho RA, Weinberg RA, editors. 8th ed. Lippincott Williams & Wilkins; 2009. 2448p.
  7. Kwak MS, Yim JY, Yi A, Chung GE, Yang JI, Kim D, et al. Nonalcoholic fatty liver disease is associated with breast cancer in nonobese women. Dig Liver Dis. 2019;51(7):1030-5. doi: 10.1016/j.dld.2018.12.024.
  8. Nelson HD, Zakher B, Cantor A, Fu R, Griffin J, O'Meara ES, et al. Risk factors for breast cancer for women aged 40 to 49 years: a systematic review and meta-analysis. Ann Intern Med. 2012;156(9):635-48. doi: 10.7326/0003-4819-156-9-201205010-00006.
  9. Kim GA, Lee HC, Choe J, Kim MJ, Lee MJ, Chang HS, et al. Association between non-alcoholic fatty liver disease and cancer incidence rate. J Hepatol. 2017; 2: S0168-8278(17)32294-8. doi: 10.1016/j.jhep.2017.09.012.
  10. Byrne CD, Targher G. NAFLD: a multisystem disease. J Hepatol. 2015;62(1 Suppl):S47-64. doi: 10.1016/j.jhep.2014.12.012.
  11. Targher G, Tilg H, Byrne CD. Non-alcoholic fatty liver disease: a multisystem disease requiring a multidisciplinary and holistic approach. Lancet Gastroenterol Hepatol. 2021;6(7):578-88. doi: 10.1016/S2468-1253(21)00020-0.
  12. Sanna C, Rosso C, Marietti M, Bugianesi E. Non-alcoholic fatty liver disease and extra-hepatic cancers. Int J Mol Sci. 2016;17(5):717. doi: 10.3390/ijms17050717.
  13. European Association For The Study Of The Liver; European Organisation For Research And Treatment Of Cancer. EASL-EORTC clinical practice guidelines: management of hepatocellular carcinoma. J Hepatol. 2012;56(4):908-43. doi: 10.1016/j.jhep.2011.12.001. Erratum in: J Hepatol. 2012;56(6):1430.
  14. Liu SS, Ma XF, Zhao J, Du SX, Zhang J, Dong MZ, et al. Association between nonalcoholic fatty liver disease and extrahepatic cancers: a systematic review and meta-analysis. Lipids Health Dis. 2020;19(1):118. doi: 10.1186/s12944-020-01288-6.
  15. Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gøtzsche PC, Ioannidis JP, et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. J Clin Epidemiol. 2009;62(10):e1-34. doi: 10.1016/j.jclinepi.2009.06.006.
  16. 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(9):603-5. doi: 10.1007/s10654-010-9491-z.
  17. Bilici A, Ozguroglu M, Mihmanlı I, Turna H, Adaletli I. A case–control study of non-alcoholic fatty liver disease in breast cancer. Med Oncol. 2007;24(4):367-71. doi: 10.1007/s12032-007-0034-8.
  18. Lee CH, Choi SH, Chung GE, Park B, Kwak MS. Nonalcoholic fatty liver disease is associated with decreased lung function. Liver Int. 2018;38(11):2091-100. doi: 10.1111/liv.13860.
  19. FIRAT SN, Durhan A, Serap E, Çulha C. The relationship between non-alcoholic fatty liver disease and breast cancer: a retrospective case-control study. J Health Scie Med. 2020;5(1): 109-13. doi.org/10.32322/jhsm.993960.
  20. Huber Y, Labenz C, Michel M, Wörns MA, Galle PR, Kostev K, et al. Tumor incidence in patients with non-alcoholic fatty liver disease. Dtsch Arztebl Int. 2020;117(43):719-24. doi: 10.3238/arztebl.2020.0719.
  21. Sutandyo N, Kardinah K, Joko DJeKI. Non-alcoholic fatty liver as a risk factor for breast cancer among Indonesian pre-menopausal women: a case-control study. eJKI. 2020; 8(1):10-4. doi: 10.23886/ejki.8.11441.
  22. Sørensen HT, Mellemkjaer L, Jepsen P, Thulstrup AM, Baron J, Olsen JH, et al. Risk of cancer in patients hospitalized with fatty liver: a Danish cohort study. J Clin Gastroenterol. 2003;36(4):356-9. doi: 10.1097/00004836-200304000-00015.
  23. Allen AM, Hicks SB, Mara KC, Larson JJ, Therneau TM. The risk of incident extrahepatic cancers is higher in non-alcoholic fatty liver disease than obesity–a longitudinal cohort study. J Hepatol. 2019;71(6): 1229-36. doi: 10.1016/j.jhep.2019.08.018.
  24. Nseir W, Abu-Rahmeh Z, Tsipis A, Mograbi J, Mahamid M. Relationship between non-alcoholic fatty liver disease and breast cancer. Isr Med Assoc J. 2017;19(4):242-5.
  25. Ming C, Viassolo V, Probst-Hensch N, Chappuis PO, Dinov ID, Katapodi MC. Machine learning techniques for personalized breast cancer risk prediction: comparison with the BCRAT and BOADICEA models. Breast Cancer Res. 2019;21(1):75. doi: 10.1186/s13058-019-1158-4.
  26. Terry MB, Liao Y, Whittemore AS, Leoce N, Buchsbaum R, Zeinomar N, et al. 10-year performance of four models of breast cancer risk: a validation study. Lancet Oncol. 2019;20(4):504-17. doi: 10.1016/S1470-2045(18)30902-1.
  27. Hong C, Yan Y, Su L, Chen D, Zhang C. Development of a risk-stratification scoring system for predicting risk of breast cancer based on non-alcoholic fatty liver disease, non-alcoholic fatty pancreas disease, and uric acid. Open Med (Wars). 2022;17(1):619-25. doi: 10.1515/med-2022-0462.
  28. Gathani T, Ali R, Balkwill A, Green J, Reeves G, Beral V, et al. Ethnic differences in breast cancer incidence in England are due to differences in known risk factors for the disease: prospective study. Br J Cancer. 2014;110(1):224-9. doi: 10.1038/bjc.2013.632.
  29. Lee YS, Lee HS, Chang SW, Lee CU, Kim JS, Jung YK, et al. Underlying nonalcoholic fatty liver disease is a significant factor for breast cancer recurrence after curative surgery. Medicine (Baltimore). 2019;98(39):e17277. doi: 10.1097/MD.0000000000017277.
  30. Roxburgh CS, McMillan DC. Role of systemic inflammatory response in predicting survival in patients with primary operable cancer. Future Oncol. 2010;6(1):149-63. doi: 10.2217/fon.09.136.
  31. Eskandari D, Khodabandehloo N, Gholami A, Samadanifard H, Hejrati A. Investigation of the association between metabolic syndrome and breast cancer patients. Eur J Transl Myol. 2020;30(1):8776. doi: 10.4081/ejtm.2019.8776.
  32. Seo HJ, Oh IH, Yoon SJ. A comparison of the cancer incidence rates between the national cancer registry and insurance claims data in Korea. Asian Pac J Cancer Prev. 2012;13(12):6163-8. doi: 10.7314/apjcp.2012.13.12.6163.
  33. Sterling RK, Lissen E, Clumeck N, Sola R, Correa MC, Montaner J, et al. Development of a simple noninvasive index to predict significant fibrosis in patients with HIV/HCV coinfection. Hepatology. 2006;43(6):1317-25. doi: 10.1002/hep.21178.
  34. Ahn JS, Sinn DH, Min YW, Hong SN, Kim HS, Jung SH, et al. Non-alcoholic fatty liver diseases and risk of colorectal neoplasia. Aliment Pharmacol Ther. 2017;45(2):345-53. doi: 10.1111/apt.13866.
  35. Murata Y, Ogawa Y, Saibara T, Nishioka A, Takeuchi N, Kariya S, et al. Tamoxifen-induced non-alcoholic steatohepatitis in patients with breast cancer: determination of a suitable biopsy site for diagnosis. Oncol Rep. 2003;10(1):97-100.
  36. Speroff L. The Million Women Study and breast cancer. Maturitas. 2003;46(1):1-6. doi: 10.1016/j.maturitas.2003.08.001.
  37. Lesmana CR, Pakasi LS, Inggriani S, Aidawati ML, Lesmana LA. Development of non-alcoholic fatty liver disease scoring system among adult medical check-up patients: a large cross-sectional and prospective validation study. Diabetes Metab Syndr Obes. 2015;8:213-8. doi: 10.2147/DMSO.S80364.
  38. Scatarige JC, Scott WW, Donovan PJ, Siegelman SS, Sanders RC. Fatty infiltration of the liver: ultrasonographic and computed tomographic correlation. J Ultrasound Med. 1984;3(1):9-14. doi: 10.7863/jum.1984.3.1.9.
  39. Ricci C, Longo R, Gioulis E, Bosco M, Pollesello P, Masutti F, et al. Noninvasive in vivo quantitative assessment of fat content in human liver. J Hepatol. 1997;27(1):108-13. doi: 10.1016/s0168-8278(97)80288-7.