Flavonoids, flavonoid subclasses, and esophageal cancer risk: A meta-analysis of epidemiologic studies

Nutrients

Volumn 8, Issue 6, 2016, Pages

  Cui, Lingling ^a   Liu, Xinxin ^a   Tian, Yalan ^a   Xie, Chen ^a   Li, Qianwen ^a   Cui, Han ^a   Sun, Changqing ^a  

^a ZHENGZHOU UNIVERSITY   (China)

Author keywords

Esophageal cancer; Flavonoids; Meta analysis

Indexed keywords

ANTHOCYANIN; FLAVAN 3 OL; FLAVANONE; FLAVANONE DERIVATIVE; FLAVONE; FLAVONOID; FLAVONOL; ISOFLAVONE; LIGNAN; PROANTHOCYANIDIN; QUERCETIN; RESVERATROL; THEAFLAVIN; UNCLASSIFIED DRUG; FLAVONE DERIVATIVE;

ARTICLE; BARRETT ESOPHAGUS; CALORIC INTAKE; CANCER RISK; DRINKING BEHAVIOR; ESOPHAGEAL ADENOCARCINOMA; ESOPHAGEAL SQUAMOUS CELL CARCINOMA; ESOPHAGUS CANCER; FOOD FREQUENCY QUESTIONNAIRE; GEOGRAPHIC DISTRIBUTION; HUMAN; META ANALYSIS; NUTRITIONAL ASSESSMENT; PHYSICAL ACTIVITY; PHYTOCHEMISTRY; SENSITIVITY ANALYSIS; SMOKING; STOMACH CANCER; SYSTEMATIC REVIEW; DIET; EPIDEMIOLOGY; ESOPHAGEAL NEOPLASMS; FEMALE; MALE; RISK ASSESSMENT; RISK FACTOR;

ANTHOCYANINS; DIET; EPIDEMIOLOGIC STUDIES; ESOPHAGEAL NEOPLASMS; FEMALE; FLAVANONES; FLAVONES; FLAVONOIDS; HUMANS; MALE; RISK ASSESSMENT; RISK FACTORS;

EID: 84973622276     PISSN: None     EISSN: 20726643     Source Type: Journal    
DOI: 10.3390/nu8060350     Document Type: Article

References (58)

1. Torre, L. A.; Bray, F.; Siegel, R. L.; Ferlay, J.; Lortet-Tieulent, J.; Jemal, A. Global cancer statistics, 2012. CA Cancer J. Clin. 2015, 65, 87-108.
2. Chen, W.; Zheng, R.; Baade, P. D.; Zhang, S.; Zeng, H.; Bray, F.; Jemal, A.; Yu, X. Q.; He, J. Cancer statistics in China, 2015. CA Cancer J. Clin. 2016, 66, 115-132.
3. Rasool, S.; Ganai, B. A.; Sameer, A. S.; Masood, A. Esophageal cancer: Associated factors with special reference to the kashmir valley. Tumori 2012, 98, 191-203.
4. Ibiebele, T. I.; Hughes, M. C.; Nagle, C. M.; Bain, C. J.; Whiteman, D. C.; Webb, P. M. Dietary antioxidants and risk of barrett's esophagus and adenocarcinoma of the esophagus in an australian population. Int. J. Cancer 2013, 133, 214-224.
5. Mlombe, Y. B.; Rosenberg, N. E.; Wolf, S. Mlombe, Y. B.; Rosenberg, N. E.; Wolf, L. L.; Dzamalala, C. P.; Chalulu, K.; Chisi, J.; Shaheen, N. J.; Hosseinipour, M. C.; Shores, C. G. Environmental risk factors for oesophageal cancer in malawi: A case-control study. Malawi Med. J. 2015, 27, 88-92. [CrossRef] [PubMed]
6. Liu, J.; Wang, J.; Leng, Y.; Lv, C. Intake of fruit and vegetables and risk of esophageal squamous cell carcinoma: A meta-analysis of observational studies. Int. J. Cancer 2013, 133, 473-485. [CrossRef] [PubMed]
7. Li, B.; Jiang, G.; Zhang, G.; Xue, Q.; Zhang, H.; Wang, C.; Zhao, T. Intake of vegetables and fruit and risk of esophageal adenocarcinoma: A meta-analysis of observational studies. Eur. J. Nutr. 2014, 53, 1511-1521. [CrossRef] [PubMed]
8. Bertuccio, P.; Rosato, V.; Andreano, A.; Ferraroni, M.; Decarli, A.; Edefonti, V.; La Vecchia, C. Dietary patterns and gastric cancer risk: A systematic review and meta-analysis. Ann. Oncol. 2013, 24, 1450-1458. [CrossRef] [PubMed]
9. Shimazu, T.; Wakai, K.; Tamakoshi, A.; Tsuji, I.; Tanaka, K.; Matsuo, K.; Nagata, C.; Mizoue, T.; Inoue, M.; Tsugane, S.; et al. Association of vegetable and fruit intake with gastric cancer risk among Japanese: A pooled analysis of four cohort studies. Ann. Oncol. 2014, 25, 1228-1233. [CrossRef] [PubMed]
10. Koushik, A.; Hunter, D. J.; Spiegelman, D.; Beeson, W. L.; van den Brandt, P. A.; Buring, J. E.; Calle, E. E.; Cho, E.; Fraser, G. E.; Freudenheim, J. L.; et al. Fruits, vegetables, and colon cancer risk in a pooled analysis of 14 cohort studies. J. Natl. Cancer Inst. 2007, 99, 1471-1483. [CrossRef] [PubMed]
11. Wang, X. Fruit and vegetable consumption and mortality from all causes, cardiovascular disease, and cancer: Systematic review and dose-response meta-analysis of prospective cohort studies. BMJ 2014, 349, g4490. [CrossRef] [PubMed]
12. Ververidis, F.; Trantas, E.; Douglas, C.; Vollmer, G.; Kretzschmar, G.; Panopoulos, N. Biotechnology of flavonoids and other phenylpropanoid-derived natural products. Part I: Chemical diversity, impacts on plant biology and human health. Biotechnol. J. 2007, 2, 1214-1234. [CrossRef] [PubMed]
13. Zhang, S. Z.; Yang, X. N.; Coburn, R. A.; Morris, M. E. Structure activity relationships and quantitative structure activity relationships for the flavonoid-mediated inhibition of breast cancer resistance protein. Biochem. Pharmacol. 2005, 70, 627-639. [CrossRef] [PubMed]
14. McPhail, D. B.; Hartley, R. C.; Gardner, P. T.; Duthie, G. G. Kinetic and stoichiometric assessment of the antioxidant activity of flavonoids by electron spin resonance spectroscopy. J. Agric. Food Chem. 2003, 51, 1684-1690. [CrossRef] [PubMed]
15. Lambert, J. D.; Hong, J.; Yang, G. Y.; Liao, J.; Yang, C. S. Inhibition of carcinogenesis by polyphenols: Evidence from laboratory investigations. Am. J. Clin. Nutr. 2005, 81, 284S-291S. [PubMed]
16. Woo, H. D.; Kim, J. Dietary flavonoid intake and risk of stomach and colorectal cancer. World J. Gastroenterol. 2013, 19, 1011-1019. [CrossRef] [PubMed]
17. Periyasamy, K.; Baskaran, K.; Ilakkia, A.; Vanitha, K.; Selvaraj, S.; Sakthisekaran, D. Antitumor efficacy of tangeretin by targeting the oxidative stress mediated on 7, 12-dimethylbenz(a) anthracene-induced proliferative breast cancer in sprague-dawley rats. Cancer Chemother. Pharmacol. 2015, 75, 263-272. [CrossRef] [PubMed]
18. LeJeune, T. M.; Tsui, H. Y.; Parsons, L. B.; Miller, G. E.; Whitted, C.; Lynch, K. E.; Ramsauer, R. E.; Patel, J. U.; Wyatt, J. E.; Street, D. S.; et al. Mechanism of action of two flavone isomers targeting cancer cells with varying cell differentiation status. PLoS ONE 2015, 10, e0142928. [CrossRef] [PubMed]
19. Wang, L.; Lu, A.; Liu, X.; Sang, M.; Shan, B.; Meng, F.; Cao, Q.; Ji, X. The flavonoid Baohuoside-I inhibits cell growth and downregulates survivin and cyclin D1 expression in esophageal carcinoma via β-catenin-dependent signaling. Oncol. Rep. 2011, 26, 1149-1156. [PubMed]
20. Shumway, B. S.; Kresty, L. A.; Larsen, P. E.; Zwick, J. C.; Lu, B.; Field, H. W.; Mumper, R. J.; Stoner, G. D.; Mallery, S. R. Effects of a topically applied bioadhesive berry gel on loss of heterozygosity indices in premalignant oral lesions. Clin. Cancer Res. 2008, 14, 2421-2430. [CrossRef] [PubMed]
21. Mallery, S. R.; Tong, M.; Shumway, B. S.; Curran, A. E.; Larsen, P. E.; Ness, G. M.; Kennedy, K. S.; Blakey, G. H.; Kushner, G. M.; Vickers, A. M.; et al. Topical application of a mucoadhesive freeze-dried black raspberry gel induces clinical and histologic regression and reduces loss of heterozygosity events in premalignant oral intraepithelial lesions: Results from a multicentered, placebo-controlled clinical trial. Clin. Cancer Res. 2014, 20, 1910-1924. [PubMed]
22. Mallery, S. R.; Zwick, J. C.; Pei, P.; Tong, M.; Larsen, P. E.; Shumway, B. S.; Lu, B.; Fields, H. W.; Mumper, R. J.; Stoner, G. D. Topical application of a bioadhesive black raspberry gel modulates gene expression and reduces cyclooxygenase 2 protein in human premalignant oral lesions. Cancer Res. 2008, 68, 4945-4957. [CrossRef] [PubMed]
23. Wang, L. S.; Burke, C. A.; Hasson, H.; Kuo, C. T.; Molmenti, C. L. S.; Seguin, C.; Liu, P. Y.; Huang, T. H. M.; Frankel, W. L.; Stoner, G. D. A phase Ib study of the effects of black raspberries on rectal polyps in patients with familial adenomatous polyposis. Cancer Prev. Res. 2014, 7, 666-674. [CrossRef] [PubMed]
24. Wang, L. S.; Arnold, M.; Huang, Y. W.; Sardo, C.; Seguin, C.; Martin, E.; Huang, T. H.; Riedl, K.; Schwartz, S.; Frankel, W.; et al. Modulation of genetic and epigenetic biomarkers of colorectal cancer in humans by black raspberries: A phase I pilot study. Clin. Cancer Res. 2011, 17, 598-610. [CrossRef] [PubMed]
25. Kresty, L. A.; Frankel, W. L.; Hammond, C. D.; Baird, M. E.; Mele, J. M.; Stoner, G. D.; Fromkes, J. J. Transitioning from preclinical to clinical chemopreventive assessments of lyophilized black raspberries: Interim results show berries modulate markers of oxidative stress in barrett's esophagus patients. Nutr. Cancer 2006, 54, 148-156. [CrossRef] [PubMed]
26. Chen, T.; Yan, F.; Qian, J.; Guo, M.; Zhang, H.; Tang, X.; Chen, F.; Stoner, G. D.; Wang, X. Randomized phase II trial of lyophilized strawberries in patients with dysplastic precancerous lesions of the esophagus. Cancer Prev. Res. (Phila.) 2012, 5, 41-50. [CrossRef] [PubMed]
27. Rathkopf, D.; Dickson, M. A.; Feldman, D. R.; Carvajal, R. D.; Shah, M. A.; Wu, N.; Lefkowitz, R.; Gonen, M.; Cane, L. M.; Dials, H. J.; et al. Phase I study of flavopiridol with oxaliplatin and fluorouracil/leucovorin in advanced solid tumors. Clin. Cancer Res. 2009, 15, 7405-7411. [CrossRef] [PubMed]
28. Schwartz, G. K.; Ilson, D.; Saltz, L.; O'Reilly, E.; Tong, W.; Maslak, P.; Werner, J.; Perkins, P.; Stoltz, M.; Kelsen, D. Phase II study of the cyclin-dependent kinase inhibitor flavopiridol administered to patients with advanced gastric carcinoma. J. Clin. Oncol. 2001, 19, 1985-1992. [PubMed]
29. Morimoto, Y.; Maskarinec, G.; Park, S. Y.; Ettienne, R.; Matsuno, R. K.; Long, C.; Steffen, A. D.; Henderson, B. E.; Kolonel, L. N.; Le Marchand, L.; et al. Dietary isoflavone intake is not statistically significantly associated with breast cancer risk in the multiethnic cohort. Br. J. Nutr. 2014, 112, 976-983. [CrossRef] [PubMed]
30. Tang, N. P.; Zhou, B.; Wang, B.; Yu, R. B.; Ma, J. Flavonoids intake and risk of lung cancer: A meta-analysis. Jpn. J. Clin. Oncol. 2009, 39, 352-359. [CrossRef] [PubMed]
31. Xie, Y.; Huang, S.; Su, Y. Dietary flavonols intake and risk of esophageal and gastric cancer: A meta-analysis of epidemiological studies. Nutrients 2016, 8, 91. [CrossRef] [PubMed]
32. Tang, L.; Lee, A. H.; Xu, F.; Zhang, T.; Lei, J.; Binns, C. W. Soya and isoflavone intakes associated with reduced risk of oesophageal cancer in north-west China. Public Health Nutr. 2015, 18, 130-134. [CrossRef] [PubMed]
33. De Stefani, E.; Ronco, A.; Mendilaharsu, M.; Deneo-Pellegrini, H. Diet and risk of cancer of the upper aerodigestive tract-II. Nutrients. Oral Oncol. 1999, 35, 22-26. [CrossRef]
34. PUBMED. Available online: http: //www. pubmed. gov (accessed on 2 June 2016).
35. EMBASE. Available online: http: //store. elsevier. com/embase (accessed on 2 June 2016).
36. Web of Science. Available online: http: //www. isiknowledge. com (accessed on 2 June 2016).
37. Stroup, D. F.; Berlin, J. A.; Morton, S. C.; Olkin, I.; Williamson, G. D.; Rennie, D.; Moher, D.; Becker, B. J.; Sipe, T. A.; Thacker, S. B. Meta-analysis of observational studies in epidemiology: A proposal for reporting. Meta-analysis of observational studies in epidemiology (moose) group. JAMA 2000, 283, 2008-2012. [CrossRef] [PubMed]
38. Greenland, S. Quantitative methods in the review of epidemiologic literature. Epidemiol. Rev. 1987, 9, 1-30. [PubMed]
39. Mantel, N.; Haenszel, W. Statistical aspects of the analysis of data from retrospective studies of disease. J. Natl. Cancer Inst. 1959, 22, 719-748. [PubMed]
40. Egger, M.; Smith, G. D.; Schneider, M.; Minder, C. Bias in meta-analysis detected by a simple, graphical test. BMJ 1997, 315, 629-634. [CrossRef] [PubMed]
41. Lin, Y.; Yngve, A.; Lagergren, J.; Lu, Y. Dietary intake of lignans and risk of adenocarcinoma of the esophagus and gastroesophageal junction. Cancer Causes Control 2012, 23, 837-844. [CrossRef] [PubMed]
42. Rossi, M.; Bosetti, C.; Negri, E.; Lagiou, P.; La Vecchia, C. Flavonoids, proanthocyanidins, and cancer risk: A network of case-control studies from Italy. Nutr. Cancer 2010, 62, 871-877. [CrossRef] [PubMed]
43. Sun, C. L.; Yuan, J. M.; Lee, M. J.; Yang, C. S.; Gao, Y. T.; Ross, R. K.; Yu, M. C. Urinary tea polyphenols in relation to gastric and esophageal cancers: A prospective study of men in Shanghai, China. Carcinogenesis 2002, 23, 1497-1503. [CrossRef] [PubMed]
44. Petrick, J. L.; Steck, S. E.; Bradshaw, P. T.; Chow, W. H.; Engel, L. S.; He, K.; Risch, H. A.; Vaughan, T. L.; Gammon, M. D. Dietary flavonoid intake and barrett's esophagus in western Washington state. Ann. Epidemiol. 2015, 25, 730. e2-735. e2. [CrossRef] [PubMed]
45. Jiao, L.; Kramer, J. R.; Rugge, M.; Parente, P.; Verstovsek, G.; Alsarraj, A.; El-Serag, H. B. Dietary intake of vegetables, folate, and antioxidants and the risk of barrett's esophagus. Cancer Causes Control 2013, 24, 1005-1014. [CrossRef] [PubMed]
46. Petrick, J. L.; Steck, S. E.; Bradshaw, P. T.; Trivers, K. F.; Abrahamson, P. E.; Engel, L. S.; He, K.; Chow, W. H.; Mayne, S. T.; Risch, H. A.; et al. Dietary intake of flavonoids and oesophageal and gastric cancer: Incidence and survival in the United States of America (USA). Br. J. Cancer 2015, 112, 1291-1300. [CrossRef] [PubMed]
47. Lin, Y.; Yngve, A.; Lagergren, J.; Lu, Y. A dietary pattern rich in lignans, quercetin and resveratrol decreases the risk of oesophageal cancer. Br. J. Nutr. 2014, 112, 2002-2009. [CrossRef] [PubMed]
48. Vermeulen, E.; Zamora-Ros, R.; Duell, E. J.; Lujan-Barroso, L.; Boeing, H.; Aleksandrova, K.; Bueno-de-Mesquita, H. B.; Scalbert, A.; Romieu, I.; Fedirko, V.; et al. Dietary flavonoid intake and esophageal cancer risk in the european prospective investigation into cancer and nutrition cohort. Am. J. Epidemiol. 2013, 178, 570-581. [CrossRef] [PubMed]
49. Bobe, G.; Peterson, J. J.; Gridley, G.; Hyer, M.; Dwyer, J. T.; Brown, L. M. Flavonoid consumption and esophageal cancer among black and white men in the United States. Int. J. Cancer 2009, 125, 1147-1154. [CrossRef] [PubMed]
50. Rossi, M.; Garavello, W.; Talamini, R.; La Vecchia, C.; Franceschi, S.; Lagiou, P.; Zambon, P.; Dal Maso, L.; Bosetti, C.; Negri, E. Flavonoids and risk of squamous cell esophageal cancer. Int. J. Cancer 2007, 120, 1560-1564. [CrossRef] [PubMed]
51. Martinez, R. M.; Pinho-Ribeiro, F. A.; Steffen, V. S.; Caviglione, C. V.; Vignoli, J. A.; Barbosa, D. S.; Baracat, M. M.; Georgetti, S. R.; Verri, W. A., Jr.; Casagrande, R. Naringenin inhibits UVB irradiation-induced inflammation and oxidative stress in the skin of hairless mice. J. Nat. Prod. 2015, 78, 1647-1655. [CrossRef] [PubMed]
52. Huang, C. Q.; Chen, X. G.; Guo, B. L.; Huang, W. H.; Shen, T.; Sun, X. G.; Xiao, P. G.; Zhou, Q. Induction of apoptosis by icariside II through extrinsic and intrinsic signaling pathways in human breast cancer MCF7 cells. Biosci. Biotechnol. Biochem. 2012, 76, 1322-1328. [CrossRef] [PubMed]
53. Chang, H.; Xie, Q.; Zhang, Q. Y.; Peng, X. L.; Zhu, J. D.; Mi, M. T. Flavonoids, flavonoid subclasses and breast cancer risk: A meta-analysis of epidemiologic studies. PLoS ONE 2013, 8, e54318.
54. Chen, M. N.; Rao, Y. H.; Zheng, Y.; Wei, S. Q.; Li, Y.; Guo, T.; Yin, P. Association between soy isoflavone intake and breast cancer risk for pre-and post-menopausal women: A meta-analysis of epidemiological studies. PLoS ONE 2014, 9, e89288. [CrossRef] [PubMed]
55. Wang, L. S.; Stoner, G. D. Anthocyanins and their role in cancer prevention. Cancer Lett. 2008, 269, 281-290. [CrossRef] [PubMed]
56. Zikri, N. N.; Riedl, K. M.; Wang, L. S.; Lechner, J.; Schwartz, S. J.; Stoner, G. D. Black raspberry components inhibit proliferation, induce apoptosis, and modulate gene expression in rat esophageal epithelial cells. Nutr. Cancer 2009, 61, 816-826. [CrossRef] [PubMed]
57. Wang, L. S.; Hecht, S. S.; Carmella, S. G.; Yu, N.; Larue, B.; Henry, C.; McIntyre, C.; Rocha, C.; Lechner, J. F.; Stoner, G. D. Anthocyanins in black raspberries prevent esophageal tumors in rats. Cancer Prev. Res. (Phila.) 2009, 2, 84-93. [CrossRef] [PubMed]
58. Peiffer, D. S.; Zimmerman, N. P.; Wang, L. S.; Ransom, B. W. S.; Carmella, S. G.; Kuo, C. T.; Siddiqui, J.; Chen, J. H.; Oshima, K.; Huang, Y. W.; et al. Chemoprevention of esophageal cancer with black raspberries, their component anthocyanins, and a major anthocyanin metabolite, protocatechuic acid. Cancer Prev. Res. (Phila.) 2014, 7, 574-584. [CrossRef] [PubMed]