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Effects of garlic intake on cancer: a systematic review of randomized clinical trials and cohort studies

  • Lee, Jounghee (Department of Food and Nutrition, Kunsan National University) ;
  • Zhao, Naisi (Department of Public Health and Community Medicine, School of Medicine, Tufts University) ;
  • Fu, Zhuxuan (Department of Epidemiology, University of Pittsburgh) ;
  • Choi, Jihee (Department of Food and Nutrition, Gachon University) ;
  • Lee, Hae-Jeung (Department of Food and Nutrition, Gachon University) ;
  • Chung, Mei (Department of Public Health and Community Medicine, School of Medicine, Tufts University)
  • Received : 2021.03.08
  • Accepted : 2021.07.21
  • Published : 2021.12.01

Abstract

BACKGROUND/OBJECTIVES: Due to the rapid increase of global cancer incidence and mortality and a high level of interest in cancer prevention, a systematic review of garlic intake and cancer risk is needed. SUBJECTS/METHODS: We implemented a systematic review to examine the effects of varying levels of garlic intake on cancer. We conducted comprehensive literature searches in three electronic databases (MEDLINE, Embase, and Web of Science) for studies published between database inception and July or September of 2018. Two investigators independently screened abstracts and full-texts, extracted data, and assessed risk of bias (RoB). A total of one medium-quality randomized controlled trial (RCT) and 13 cohort studies graded as high RoB were included. RESULTS: The 1-year follow-up results from a RCT showed that a significant decrease in the number and size of colorectal adenomas among participants with colorectal adenomas who received high-dose aged garlic extract (AGE) compared with those who received low-dose AGE (P < 0.05). The results of prospective observational studies provided inconsistent associations of colorectal cancer risk with garlic supplements and garlic intake as food. CONCLUSIONS: In summary, the AGE was effective in reducing the number and magnitude of colorectal adenomas in one RCT, but there were inconsistent associations between garlic intake and colorectal cancer in cohort studies. Therefore, we could not draw a firm conclusion regarding the effects of garlic on cancer, because the current strength of evidence is inadequate due to a lack of number of high-quality RCTs.

Keywords

Acknowledgement

This research was supported by a grant (21162MFDS076) from Ministry of Food and Drug Safety in 2021 and partly supported by Cooperative Research Program for Agriculture Science and Technology Development (project No. PJ014536022021) Rural Development Administration, Republic of Korea.

References

  1. World Health Organization. Fact sheets: Cancer [Internet]. Geneva: World Health Organization; 2018 [cited 2019 October 1]. Available from: http://www.who.int/mediacentre/factsheets/fs297/en/.
  2. Bhagyalakshmi N, Thimmaraju R, Venkatachalam L, Murthy KN, Sreedhar RV. Nutraceutical applications of garlic and the intervention of biotechnology. Crit Rev Food Sci Nutr 2005;45:607-21. https://doi.org/10.1080/10408390500455508
  3. Rivlin RS. Historical perspective on the use of garlic. J Nutr 2001;131:951S-954S. https://doi.org/10.1093/jn/131.3.951S
  4. Ngo SN, Williams DB, Cobiac L, Head RJ. Does garlic reduce risk of colorectal cancer? A systematic review. J Nutr 2007;137:2264-9. https://doi.org/10.1093/jn/137.10.2264
  5. Wu X, Kassie F, Mersch-Sundermann V. Induction of apoptosis in tumor cells by naturally occurring sulfur-containing compounds. Mutat Res 2005;589:81-102. https://doi.org/10.1016/j.mrrev.2004.11.001
  6. 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;68:394-424. https://doi.org/10.3322/caac.21492
  7. Shang A, Cao SY, Xu XY, Gan RY, Tang GY, Corke H, Mavumengwana V, Li HB. Bioactive compounds and biological functions of garlic (allium sativum l.). Foods 2019;8:246. https://doi.org/10.3390/foods8070246
  8. Miraghajani M, Rafie N, Hajianfar H, Larijani B, Azadbakht L. Aged garlic and cancer: a systematic review. Int J Prev Med 2018;9:84. https://doi.org/10.4103/ijpvm.ijpvm_437_17
  9. Karmakar S, Choudhury SR, Banik NL, Ray SK. Molecular mechanisms of anti-cancer action of garlic compounds in neuroblastoma. Anticancer Agents Med Chem 2011;11:398-407. https://doi.org/10.2174/187152011795677553
  10. Nouroz F, Mehboob M, Noreen S, Zaidi F, Mobin T. A review on anticancer activities of garlic (Allium sativum L.). Middle East J Sci Res 2015;23:1145-51.
  11. Zhang W, Ha M, Gong Y, Xu Y, Dong N, Yuan Y. Allicin induces apoptosis in gastric cancer cells through activation of both extrinsic and intrinsic pathways. Oncol Rep 2010;24:1585-92.
  12. World Cancer Research Fund; American Institute for Cancer Research. Continuous Update Project Expert Report 2018. Diet, nutrition, physical activity and colorectal cancer. London: World Cancer Research Fund; 2018 [cited 2019 December 1]. Available from: https://www.wcrf.org/diet-and-cancer/.
  13. Fleischauer AT, Poole C, Arab L. Garlic consumption and cancer prevention: meta-analyses of colorectal and stomach cancers. Am J Clin Nutr 2000;72:1047-52. https://doi.org/10.1093/ajcn/72.4.1047
  14. Hu JY, Hu YW, Zhou JJ, Zhang MW, Li D, Zheng S. Consumption of garlic and risk of colorectal cancer: an updated meta-analysis of prospective studies. World J Gastroenterol 2014;20:15413-22. https://doi.org/10.3748/wjg.v20.i41.15413
  15. Higgins JP, Thomas J, Chandler J, Cumpston M, Li T, Page MJ, Welch VA. Cochrane Handbook for Systematic Reviews of Interventions. Hoboken (NJ): John Wiley & Sons; 2019.
  16. Chiavarini M, Minelli L, Fabiani R. Garlic consumption and colorectal cancer risk in man: a systematic review and meta-analysis. Public Health Nutr 2016;19:308-17. https://doi.org/10.1017/S1368980015001263
  17. Kodali RT, Eslick GD. Meta-analysis: does garlic intake reduce risk of gastric cancer? Nutr Cancer 2015;67:1-11. https://doi.org/10.1080/01635581.2015.967873
  18. Heine-Broring RC, Winkels RM, Renkema JM, Kragt L, van Orten-Luiten AC, Tigchelaar EF, Chan DS, Norat T, Kampman E. Dietary supplement use and colorectal cancer risk: a systematic review and metaanalyses of prospective cohort studies. Int J Cancer 2015;136:2388-401. https://doi.org/10.1002/ijc.29277
  19. Wallace BC, Small K, Brodley CE, Lau J, Trikalinos TA. Deploying an interactive machine learning system in an evidence-based practice center: abstrackr. Proceedings of the 2nd ACM SIGHIT International Health Informatics Symposium; 2012 Jan 28-30; Miami (FL), USA. New York (NY): Association for Computing Machinery; 2012. p.819-24.
  20. Wells GA, O'Connell D, Peterson J, Welch V, Lossos M, Tugwell P. The Newcastle-Ottawa Scale (NOS) for Assessing the Quality of Nonrandomized Studies in Meta-Analyses. Ottawa: Ottawa Hospital Research Institute; 2011.
  21. Higgins JP, Sterne JA, Savovic J, Page MJ, Hrobjartsson A, Boutron I, Reeves B, Eldridge S. A revised tool for assessing risk of bias in randomized trials. Cochrane Database Syst Rev 2016;10:29-31.
  22. Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred Reporting Items for Systematic Reviews and Meta-Analyses: the PRISMA Statement 2009. [place unknown]: PRISMA; c2021 [cited 2020 October 11]. Available from: http://www.prisma-statement.org/.
  23. American Diabetes Association. Introduction: The American Diabetes Association's (ADA) evidence-based practice guidelines, standards, and related recommendations and documents for diabetes care. Diabetes Care 2012;35 Suppl 1:S1-2. https://doi.org/10.2337/dc12-s001
  24. Tanaka S, Haruma K, Yoshihara M, Kajiyama G, Kira K, Amagase H, Chayama K. Aged garlic extract has potential suppressive effect on colorectal adenomas in humans. J Nutr 2006;136:821S-826S. https://doi.org/10.1093/jn/136.3.821S
  25. Giovannucci E, Rimm EB, Stampfer MJ, Colditz GA, Ascherio A, Willett WC. Intake of fat, meat, and fiber in relation to risk of colon cancer in men. Cancer Res 1994;54:2390-7.
  26. Steinmetz KA, Kushi LH, Bostick RM, Folsom AR, Potter JD. Vegetables, fruit, and colon cancer in the Iowa Women's Health Study. Am J Epidemiol 1994;139:1-15. https://doi.org/10.1093/oxfordjournals.aje.a116921
  27. Dorant E, van den Brandt PA, Goldbohm RA. A prospective cohort study on the relationship between onion and leek consumption, garlic supplement use and the risk of colorectal carcinoma in the Netherlands. Carcinogenesis 1996;17:477-84. https://doi.org/10.1093/carcin/17.3.477
  28. Sellers TA, Bazyk AE, Bostick RM, Kushi LH, Olson JE, Anderson KE, Lazovich D, Folsom AR. Diet and risk of colon cancer in a large prospective study of older women: an analysis stratified on family history (Iowa, United States). Cancer Causes Control 1998;9:357-67. https://doi.org/10.1023/A:1008886715597
  29. Satia JA, Littman A, Slatore CG, Galanko JA, White E. Associations of herbal and specialty supplements with lung and colorectal cancer risk in the VITamins And Lifestyle study. Cancer Epidemiol Biomarkers Prev 2009;18:1419-28. https://doi.org/10.1158/1055-9965.EPI-09-0038
  30. McCullough ML, Jacobs EJ, Shah R, Campbell PT, Gapstur SM. Garlic consumption and colorectal cancer risk in the CPS-II Nutrition Cohort. Cancer Causes Control 2012;23:1643-51. https://doi.org/10.1007/s10552-012-0042-7
  31. Meng S, Zhang X, Giovannucci EL, Ma J, Fuchs CS, Cho E. No association between garlic intake and risk of colorectal cancer. Cancer Epidemiol 2013;37:152-5. https://doi.org/10.1016/j.canep.2012.11.002
  32. Dorant E, van den Brandt PA, Goldbohm RA. A prospective cohort study on Allium vegetable consumption, garlic supplement use, and the risk of lung carcinoma in The Netherlands. Cancer Res 1994;54:6148-53.
  33. Dorant E, van den Brandt PA, Goldbohm RA. Allium vegetable consumption, garlic supplement intake, and female breast carcinoma incidence. Breast Cancer Res Treat 1995;33:163-70. https://doi.org/10.1007/BF00682723
  34. Dorant E, van den Brandt PA, Goldbohm RA, Sturmans F. Consumption of onions and a reduced risk of stomach carcinoma. Gastroenterology 1996;110:12-20. https://doi.org/10.1053/gast.1996.v110.pm8536847
  35. Brasky TM, Kristal AR, Navarro SL, Lampe JW, Peters U, Patterson RE, White E. Specialty supplements and prostate cancer risk in the VITamins And Lifestyle (VITAL) cohort. Nutr Cancer 2011;63:573-82. https://doi.org/10.1080/01635581.2011.553022
  36. Walter RB, Brasky TM, Milano F, White E. Vitamin, mineral, and specialty supplements and risk of hematologic malignancies in the prospective VITamins And Lifestyle (VITAL) study. Cancer Epidemiol Biomarkers Prev 2011;20:2298-308. https://doi.org/10.1158/1055-9965.EPI-11-0494
  37. Kim H, Keum N, Giovannucci EL, Fuchs CS, Bao Y. Garlic intake and gastric cancer risk: results from two large prospective US cohort studies. Int J Cancer 2018;143:1047-53. https://doi.org/10.1002/ijc.31396
  38. Nicastro HL, Ross SA, Milner JA. Garlic and onions: their cancer prevention properties. Cancer Prev Res (Phila) 2015;8:181-9. https://doi.org/10.1158/1940-6207.CAPR-14-0172
  39. Arunkumar A, Vijayababu MR, Srinivasan N, Aruldhas MM, Arunakaran J. Garlic compound, diallyl disulfide induces cell cycle arrest in prostate cancer cell line PC-3. Mol Cell Biochem 2006;288:107-13. https://doi.org/10.1007/s11010-006-9126-6
  40. Schaffer EM, Liu JZ, Green J, Dangler CA, Milner JA. Garlic and associated allyl sulfur components inhibit N-methyl-N-nitrosourea induced rat mammary carcinogenesis. Cancer Lett 1996;102:199-204. https://doi.org/10.1016/0304-3835(96)04160-2
  41. Belloir C, Singh V, Daurat C, Siess MH, Le Bon AM. Protective effects of garlic sulfur compounds against DNA damage induced by direct- and indirect-acting genotoxic agents in HepG2 cells. Food Chem Toxicol 2006;44:827-34. https://doi.org/10.1016/j.fct.2005.11.005
  42. Xiao D, Pinto JT, Gundersen GG, Weinstein IB. Effects of a series of organosulfur compounds on mitotic arrest and induction of apoptosis in colon cancer cells. Mol Cancer Ther 2005;4:1388-98. https://doi.org/10.1158/1535-7163.MCT-05-0152
  43. Ueda S, Masutani H, Nakamura H, Tanaka T, Ueno M, Yodoi J. Redox control of cell death. Antioxid Redox Signal 2002;4:405-14. https://doi.org/10.1089/15230860260196209
  44. Yi L, Su Q. Molecular mechanisms for the anti-cancer effects of diallyl disulfide. Food Chem Toxicol 2013;57:362-70. https://doi.org/10.1016/j.fct.2013.04.001
  45. Fleischauer AT, Arab L. Garlic and cancer: a critical review of the epidemiologic literature. J Nutr 2001;131:1032S-1040S. https://doi.org/10.1093/jn/131.3.1032S
  46. Jacobs DR Jr, Gross MD, Tapsell LC. Food synergy: an operational concept for understanding nutrition. Am J Clin Nutr 2009;89:1543S-1548S. https://doi.org/10.3945/ajcn.2009.26736b
  47. Shim JS, Oh K, Kim HC. Dietary assessment methods in epidemiologic studies. Epidemiol Health 2014;36:e2014009. https://doi.org/10.4178/epih/e2014009
  48. Olafsdottir AS, Thorsdottir I, Gunnarsdottir I, Thorgeirsdottir H, Steingrimsdottir L. Comparison of women's diet assessed by FFQs and 24-hour recalls with and without underreporters: associations with biomarkers. Ann Nutr Metab 2006;50:450-60. https://doi.org/10.1159/000094781
  49. Prati P, Henrique CM, de Souza AS, da Silva VSN, Pacheco MTB. Evaluation of allicin stability in processed garlic of different cultivars. Food Sci Technol 2014;34:623-8. https://doi.org/10.1590/1678-457x.6397
  50. Marchese A, Barbieri R, Sanches-Silva A, Daglia M, Nabavi SF, Jafari NJ, Izadi M, Ajami M, Nabavi SM. Antifungal and antibacterial activities of allicin: a review. Trends Food Sci Technol 2016;52:49-56. https://doi.org/10.1016/j.tifs.2016.03.010
  51. Pratico G, Gao Q, Manach C, Dragsted LO. Biomarkers of food intake for Allium vegetables. Genes Nutr 2018;13:34. https://doi.org/10.1186/s12263-018-0624-4