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Gastric cancer and family history

  • Choi, Yoon Jin (Department of Internal Medicine, Seoul National University Bundang Hospital) ;
  • Kim, Nayoung (Department of Internal Medicine, Seoul National University Bundang Hospital)
  • Received : 2016.05.11
  • Accepted : 2016.10.22
  • Published : 2016.11.01

Abstract

Gastric cancer is associated with high morbidity and mortality rates worldwide. Identifying individuals at high risk is important for surveillance and prevention of gastric cancer. Having first-degree relatives diagnosed with gastric cancer is a strong and consistent risk factor for gastric cancer, but the pathogenic mechanisms behind this familial aggregation are unclear. Against this background, we reviewed the risk factors for gastric cancer in those with a first-degree relative with gastric cancer, and the possible causes for familial clustering of gastric cancer including bacterial factors, inherited genetic susceptibility, environmental factors or a combination thereof. Among individuals with a family history, current or past Helicobacter pylori infection, having two or more first-degree affected relatives or female gender was associated with an increased risk of developing gastric cancer. To date, no specific single nucleotide polymorphism has been shown to be associated with familial clustering of gastric cancer. H. pylori eradication is the most important strategy for preventing gastric cancer in first-degree relatives of gastric cancer patients, particularly those in their 20s and 30s. Early H. pylori eradication could prevent the progression to intestinal metaplasia and reduce the synergistic effect on gastric carcinogenesis in individuals with both H. pylori infection and a family history. Endoscopic surveillance is also expected to benefit individuals with a family history. Further large-scale, prospective studies are warranted to evaluate the cost-effectiveness and optimal time point for endoscopy in this population. Moreover, genome-wide association studies that incorporate environmental and dietary factors on a 'big data' basis will increase our understanding of the pathogenesis of gastric cancer.

Keywords

References

  1. Ferlay J, Soerjomataram I, Ervik M, et al. GLOBOCAN 2012 v1.0, Cancer Incidence and Mortality Worldwide: IARC CancerBase No. 11 [Internet]. Lyon (FR): International Agency for Research on Cancer, c2016 [cited 2016 Oct 17]. Available from: http://globocan.iarc.fr.
  2. Inoue M, Tsugane S. Epidemiology of gastric cancer in Japan. Postgrad Med J 2005;81:419-424. https://doi.org/10.1136/pgmj.2004.029330
  3. Shin HR, Won YJ, Jung KW, et al. Nationwide cancer incidence in Korea, 1999-2001; first result using the national cancer incidence database. Cancer Res Treat 2005;37:325-331. https://doi.org/10.4143/crt.2005.37.6.325
  4. Lauren P. The two histological main types of gastric carcinoma: diffuse and so-called intestinal-type carcinoma. An attempt at a histo-clinical classification. Acta Pathol Microbiol Scand 1965;64:31-49. https://doi.org/10.1111/apm.1965.64.1.31
  5. Suzuki H, Iwasaki E, Hibi T. Helicobacter pylori and gastric cancer. Gastric Cancer 2009;12:79-87. https://doi.org/10.1007/s10120-009-0507-x
  6. Huang JQ, Sridhar S, Chen Y, Hunt RH. Meta-analysis of the relationship between Helicobacter pylori seropositivity and gastric cancer. Gastroenterology 1998;114:1169-1179. https://doi.org/10.1016/S0016-5085(98)70422-6
  7. Yaghoobi M, Bijarchi R, Narod SA. Family history and the risk of gastric cancer. Br J Cancer 2010;102:237-242. https://doi.org/10.1038/sj.bjc.6605380
  8. Oliveira C, Pinheiro H, Figueiredo J, Seruca R, Carneiro F. Familial gastric cancer: genetic susceptibility, pathology, and implications for management. Lancet Oncol 2015;16:e60-e70. https://doi.org/10.1016/S1470-2045(14)71016-2
  9. Lee HJ, Yang HK, Ahn YO. Gastric cancer in Korea. Gastric Cancer 2002;5:177-182. https://doi.org/10.1007/s101200200031
  10. McLean MH, El-Omar EM. Genetics of gastric cancer. Nat Rev Gastroenterol Hepatol 2014;11:664-674. https://doi.org/10.1038/nrgastro.2014.143
  11. Lim SH, Kwon JW, Kim N, et al. Prevalence and risk factors of Helicobacter pylori infection in Korea: nationwide multicenter study over 13 years. BMC Gastroenterol 2013;13:104. https://doi.org/10.1186/1471-230X-13-104
  12. Joo YE, Park HK, Myung DS, et al. Prevalence and risk factors of atrophic gastritis and intestinal metaplasia: a nationwide multicenter prospective study in Korea. Gut Liver 2013;7:303-310. https://doi.org/10.5009/gnl.2013.7.3.303
  13. Corso G, Marrelli D. Frequency of familial gastric cancer. In: Corso G, Roviello F, eds. Spotlight on Familial and Hereditary Gastric Cancer. Dordrecht: Springer, 2013:11-18.
  14. Zanghieri G, Di Gregorio C, Sacchetti C, et al. Familial occurrence of gastric cancer in the 2-year experience of a population-based registry. Cancer 1990;66:2047-2051. https://doi.org/10.1002/1097-0142(19901101)66:9<2047::AID-CNCR2820660934>3.0.CO;2-G
  15. Rokkas T, Sechopoulos P, Pistiolas D, Margantinis G, Koukoulis G. Helicobacter pylori infection and gastric histology in first-degree relatives of gastric cancer patients: a meta-analysis. Eur J Gastroenterol Hepatol 2010;22:1128-1133. https://doi.org/10.1097/MEG.0b013e3283398d37
  16. Chang YW, Han YS, Lee DK, et al. Role of Helicobacter pylori infection among offspring or siblings of gastric cancer patients. Int J Cancer 2002;101:469-474. https://doi.org/10.1002/ijc.10637
  17. Brenner H, Arndt V, Sturmer T, Stegmaier C, Ziegler H, Dhom G. Individual and joint contribution of family history and Helicobacter pylori infection to the risk of gastric carcinoma. Cancer 2000;88:274-279. https://doi.org/10.1002/(SICI)1097-0142(20000115)88:2<274::AID-CNCR5>3.0.CO;2-9
  18. Shin CM, Kim N, Yang HJ, et al. Stomach cancer risk in gastric cancer relatives: interaction between Helicobacter pylori infection and family history of gastric cancer for the risk of stomach cancer. J Clin Gastroenterol 2010;44:e34-e39. https://doi.org/10.1097/MCG.0b013e3181962dfa
  19. Eto K, Ohyama S, Yamaguchi T, et al. Familial clustering in subgroups of gastric cancer stratified by histology, age group and location. Eur J Surg Oncol 2006;32:743-748. https://doi.org/10.1016/j.ejso.2006.04.005
  20. Ikeguchi M, Fukuda K, Oka S, et al. Clinicopathological findings in patients with gastric adenocarcinoma with familial aggregation. Dig Surg 2001;18:439-443. https://doi.org/10.1159/000050190
  21. Huang X, Tajima K, Hamajima N, et al. Effect of life styles on the risk of subsite-specific gastric cancer in those with and without family history. J Epidemiol 1999;9:40-45. https://doi.org/10.2188/jea.9.40
  22. Lissowska J, Groves FD, Sobin LH, et al. Family history and risk of stomach cancer in Warsaw, Poland. Eur J Cancer Prev 1999;8:223-227. https://doi.org/10.1097/00008469-199906000-00010
  23. La Vecchia C, Negri E, Franceschi S, Gentile A. Family history and the risk of stomach and colorectal cancer. Cancer 1992;70:50-55. https://doi.org/10.1002/1097-0142(19920701)70:1<50::AID-CNCR2820700109>3.0.CO;2-I
  24. Garcia-Gonzalez MA, Lanas A, Quintero E, et al. Gastric cancer susceptibility is not linked to pro-and anti-inflammatory cytokine gene polymorphisms in whites: a Nationwide Multicenter Study in Spain. Am J Gastroenterol 2007;102:1878-1892. https://doi.org/10.1111/j.1572-0241.2007.01423.x
  25. Bakir T, Can G, Erkul S, Siviloglu C. Stomach cancer history in the siblings of patients with gastric carcinoma. Eur J Cancer Prev 2000;9:401-408. https://doi.org/10.1097/00008469-200012000-00005
  26. Bakir T, Can G, Siviloglu C, Erkul S. Gastric cancer and other organ cancer history in the parents of patients with gastric cancer. Eur J Cancer Prev 2003;12:183-189.
  27. Dhillon PK, Farrow DC, Vaughan TL, et al. Family history of cancer and risk of esophageal and gastric cancers in the United States. Int J Cancer 2001;93:148-152. https://doi.org/10.1002/ijc.1294
  28. Gajalakshmi CK, Shanta V. Lifestyle and risk of stomach cancer: a hospital-based case-control study. Int J Epidemiol 1996;25:1146-1153. https://doi.org/10.1093/ije/25.6.1146
  29. Minami Y, Tateno H. Associations between cigarette smoking and the risk of four leading cancers in Miyagi Prefecture, Japan: a multi-site case-control study. Cancer Sci 2003;94:540-547. https://doi.org/10.1111/j.1349-7006.2003.tb01480.x
  30. Nagase H, Ogino K, Yoshida I, et al. Family history-related risk of gastric cancer in Japan: a hospital-based case-control study. Jpn J Cancer Res 1996;87:1025-1028. https://doi.org/10.1111/j.1349-7006.1996.tb03104.x
  31. Hong SH, Kim JW, Kim HG, et al. Glutathione S-transferases (GSTM1, GSTT1 and GSTP1) and N-acetyltransferase 2 polymorphisms and the risk of gastric cancer. J Prev Med Public Health 2006;39:135-140.
  32. Chen MJ, Wu DC, Ko YC, Chiou YY. Personal history and family history as a predictor of gastric cardiac adenocarcinoma risk: a case-control study in Taiwan. Am J Gastroenterol 2004;99:1250-1257. https://doi.org/10.1111/j.1572-0241.2004.30872.x
  33. Gong EJ, Ahn JY, Jung HY, et al. Risk factors and clinical outcomes of gastric cancer identified by screening endoscopy: a case-control study. J Gastroenterol Hepatol 2014;29:301-309. https://doi.org/10.1111/jgh.12387
  34. Safaee A, Moghimi-Dehkordi B, Fatemi SR, Maserat E, Zali MR. Family history of cancer and risk of gastric cancer in Iran. Asian Pac J Cancer Prev 2011;12:3117-3120.
  35. Foschi R, Lucenteforte E, Bosetti C, et al. Family history of cancer and stomach cancer risk. Int J Cancer 2008;123:1429-1432. https://doi.org/10.1002/ijc.23688
  36. Palli D, Russo A, Saieva C, Salvini S, Amorosi A, Decarli A. Dietary and familial determinants of 10-year survival among patients with gastric carcinoma. Cancer 2000;89:1205-1213. https://doi.org/10.1002/1097-0142(20000915)89:6<1205::AID-CNCR3>3.0.CO;2-5
  37. Palli D, Russo A, Ottini L, et al. Red meat, family history, and increased risk of gastric cancer with microsatellite instability. Cancer Res 2001;61:5415-5419.
  38. Shin CM, Kim N, Lee HS, et al. Intrafamilial aggregation of gastric cancer: a comprehensive approach including environmental factors, Helicobacter pylori virulence, and genetic susceptibility. Eur J Gastroenterol Hepatol 2011;23:411-417. https://doi.org/10.1097/MEG.0b013e328343b7f5
  39. Hemminki K, Sundquist J, Ji J. Familial risk for gastric carcinoma: an updated study from Sweden. Br J Cancer 2007;96:1272-1277. https://doi.org/10.1038/sj.bjc.6603722
  40. Yim JY, Kim N, Choi SH, et al. Seroprevalence of Helicobacter pylori in South Korea. Helicobacter 2007;12:333-340. https://doi.org/10.1111/j.1523-5378.2007.00504.x
  41. Kim JH, Kim HY, Kim NY, et al. Seroepidemiological study of Helicobacter pylori infection in asymptomatic people in South Korea. J Gastroenterol Hepatol 2001;16:969-975. https://doi.org/10.1046/j.1440-1746.2001.02568.x
  42. Bures J, Kopacova M, Koupil I, et al. Epidemiology of Helicobacter pylori infection in the Czech Republic. Helicobacter 2006;11:56-65. https://doi.org/10.1111/j.0083-8703.2006.00369.x
  43. Bures J, Kopacova M, Koupil I, et al. Significant decrease in prevalence of Helicobacter pylori in the Czech Republic. World J Gastroenterol 2012;18:4412-4418. https://doi.org/10.3748/wjg.v18.i32.4412
  44. Leung WK, Ng EK, Lam CC, et al. Helicobacter pylori infection in 1st degree relatives of Chinese gastric cancer patients. Scand J Gastroenterol 2006;41:274-279. https://doi.org/10.1080/00365520510024269
  45. Brenner H, Bode G, Boeing H. Helicobacter pylori infection among offspring of patients with stomach cancer. Gastroenterology 2000;118:31-35. https://doi.org/10.1016/S0016-5085(00)70411-2
  46. Queiroz DM, Silva CI, Goncalves MH, et al. Higher frequency of cagA EPIYA-C phosphorylation sites in H. pylori strains from first-degree relatives of gastric cancer patients. BMC Gastroenterol 2012;12:107. https://doi.org/10.1186/1471-230X-12-107
  47. Siavoshi F, Asgharzadeh A, Ghadiri H, Massarrat S, Latifi-Navid S, Zamani M. Helicobacter pylori genotypes and types of gastritis in first-degree relatives of gastric cancer patients. Int J Med Microbiol 2011;301:506-512. https://doi.org/10.1016/j.ijmm.2011.03.002
  48. Yatsuya H, Toyoshima H, Tamakoshi A, et al. Individual and joint impact of family history and Helicobacter pylori infection on the risk of stomach cancer: a nested case-control study. Br J Cancer 2004;91:929-934. https://doi.org/10.1038/sj.bjc.6602067
  49. El-Omar EM, Carrington M, Chow WH, et al. Interleukin-1 polymorphisms associated with increased risk of gastric cancer. Nature 2000;404:398-402. https://doi.org/10.1038/35006081
  50. El-Omar EM, Rabkin CS, Gammon MD, et al. Increased risk of noncardia gastric cancer associated with proinflammatory cytokine gene polymorphisms. Gastroenterology 2003;124:1193-1201. https://doi.org/10.1016/S0016-5085(03)00157-4
  51. Canedo P, Figueiredo C, Machado JC. After Helicobacter pylori, genetic susceptibility to gastric carcinoma revisited. Helicobacter 2007;12 Suppl 2:45-49.
  52. Kim N, Park YS, Cho SI, et al. Prevalence and risk factors of atrophic gastritis and intestinal metaplasia in a Korean population without significant gastroduodenal disease. Helicobacter 2008;13:245-255. https://doi.org/10.1111/j.1523-5378.2008.00604.x
  53. Adamu MA, Weck MN, Rothenbacher D, Brenner H. Incidence and risk factors for the development of chronic atrophic gastritis: five year follow-up of a population-based cohort study. Int J Cancer 2011;128:1652-1658. https://doi.org/10.1002/ijc.25476
  54. Kamangar F, Cheng C, Abnet CC, Rabkin CS. Interleukin-1B polymorphisms and gastric cancer risk: a meta-analysis. Cancer Epidemiol Biomarkers Prev 2006;15:1920-1928. https://doi.org/10.1158/1055-9965.EPI-06-0267
  55. Gorouhi F, Islami F, Bahrami H, Kamangar F. Tumour-necrosis factor-A polymorphisms and gastric cancer risk: a meta-analysis. Br J Cancer 2008;98:1443-1451. https://doi.org/10.1038/sj.bjc.6604277
  56. Lee SG, Kim B, Choi W, Lee I, Choi J, Song K. Lack of association between pro-inflammatory genotypes of the interleukin-1 (IL-1B -31 C/+ and IL-1RN *2/*2) and gastric cancer/duodenal ulcer in Korean population. Cytokine 2003;21:167-171. https://doi.org/10.1016/S1043-4666(03)00032-2
  57. Kim N, Cho SI, Yim JY, et al. The effects of genetic polymorphisms of IL-1 and TNF-A on Helicobacter pylori-induced gastroduodenal diseases in Korea. Helicobacter 2006;11:105-112. https://doi.org/10.1111/j.1523-5378.2006.00384.x
  58. Savage SA, Abnet CC, Mark SD, et al. Variants of the IL8 and IL8RB genes and risk for gastric cardia adenocarcinoma and esophageal squamous cell carcinoma. Cancer Epidemiol Biomarkers Prev 2004;13:2251-2257.
  59. Song JH, Kim SG, Jung SA, Lee MK, Jung HC, Song IS. The interleukin-8-251 AA genotype is associated with angiogenesis in gastric carcinogenesis in Helicobacter pylori-infected Koreans. Cytokine 2010;51:158-165. https://doi.org/10.1016/j.cyto.2010.05.001
  60. Jin G, Wang L, Chen W, et al. Variant alleles of TGFB1 and TGFBR2 are associated with a decreased risk of gastric cancer in a Chinese population. Int J Cancer 2007;120:1330-1335. https://doi.org/10.1002/ijc.22443
  61. Okada R, Naito M, Hattori Y, et al. Matrix metalloproteinase 9 gene polymorphisms are associated with a multiple family history of gastric cancer. Gastric Cancer 2016 Apr 6 [Epub]. http://dx.doi.org/10.1007/s10120-016-0608-2.
  62. Palli D, Galli M, Caporaso NE, et al. Family history and risk of stomach cancer in Italy. Cancer Epidemiol Biomarkers Prev 1994;3:15-18.
  63. Choi YJ, Kim N, Jang W, et al. Familial clustering of gastric cancer: a retrospective study based on the number of first-degree relatives. Medicine (Baltimore) 2016;95:e3606. https://doi.org/10.1097/MD.0000000000003606
  64. Charvat H, Sasazuki S, Inoue M, et al. Prediction of the 10-year probability of gastric cancer occurrence in the Japanese population: the JPHC study cohort II. Int J Cancer 2016;138:320-331. https://doi.org/10.1002/ijc.29705
  65. Kwak HW, Choi IJ, Kim CG, et al. Individual having a parent with early-onset gastric cancer may need screening at younger age. World J Gastroenterol 2015;21:4592-4598. https://doi.org/10.3748/wjg.v21.i15.4592
  66. Lim S, Lee HS, Kim HS, Kim YI, Kim WH. Alteration of E-cadherin-mediated adhesion protein is common, but microsatellite instability is uncommon in young age gastric cancers. Histopathology 2003;42:128-136. https://doi.org/10.1046/j.1365-2559.2003.01546.x
  67. Matley PJ, Dent DM, Madden MV, Price SK. Gastric carcinoma in young adults. Ann Surg 1988;208:593-596. https://doi.org/10.1097/00000658-198811000-00008
  68. Kokkola A, Sipponen P. Gastric carcinoma in young adults. Hepatogastroenterology 2001;48:1552-1555.
  69. Correa P. Human gastric carcinogenesis: a multistep and multifactorial process: first American Cancer Society Award Lecture on Cancer Epidemiology and Prevention. Cancer Res 1992;52:6735-6740.
  70. Mansour-Ghanaei F, Joukar F, Baghaei SM, et al. Gastric precancerous lesions in first degree relatives of patients with known gastric cancer: a cross-sectional prospective study in Guilan Province, north of Iran. Asian Pac J Cancer Prev 2012;13:1779-1782. https://doi.org/10.7314/APJCP.2012.13.5.1779
  71. Oh S, Kim N, Yoon H, et al. Risk factors of atrophic gastritis and intestinal metaplasia in first-degree relatives of gastric cancer patients compared with age-sex matched controls. J Cancer Prev 2013;18:149-160. https://doi.org/10.15430/JCP.2013.18.2.149
  72. Park SH, Yu W, Chung HY. Characteristics of gastric cancer patients with family history. J Korean Surg Soc 2001;60:309-313.
  73. Han MA, Oh MG, Choi IJ, et al. Association of family history with cancer recurrence and survival in patients with gastric cancer. J Clin Oncol 2012;30:701-708. https://doi.org/10.1200/JCO.2011.35.3078
  74. Bernini M, Barbi S, Roviello F, et al. Family history of gastric cancer: a correlation between epidemiologic findings and clinical data. Gastric Cancer 2006;9:9-13. https://doi.org/10.1007/s10120-005-0350-7
  75. Yatsuya H, Toyoshima H, Mizoue T, et al. Family history and the risk of stomach cancer death in Japan: differences by age and gender. Int J Cancer 2002;97:688-694. https://doi.org/10.1002/ijc.10101
  76. Lee WJ, Hong RL, Lai IR, Chen CN, Lee PH, Huang MT. Clinicopathologic characteristics and prognoses of gastric cancer in patients with a positive familial history of cancer. J Clin Gastroenterol 2003;36:30-33. https://doi.org/10.1097/00004836-200301000-00010
  77. Oh MG, Kim JH, Han MA, Park J, Ryu SY, Choi SW. Family history and survival of patients with gastric cancer: a meta-analysis. Asian Pac J Cancer Prev 2014;15:3465-3470. https://doi.org/10.7314/APJCP.2014.15.8.3465
  78. Kang JM, Shin DW, Kwon YM, et al. Stomach cancer screening and preventive behaviors in relatives of gastric cancer patients. World J Gastroenterol 2011;17:3518-3525. https://doi.org/10.3748/wjg.v17.i30.3518
  79. Compare D, Rocco A, Nardone G. Risk factors in gastric cancer. Eur Rev Med Pharmacol Sci 2010;14:302-308.
  80. Fock KM, Talley N, Moayyedi P, et al. Asia-Pacific consensus guidelines on gastric cancer prevention. J Gastroenterol Hepatol 2008;23:351-365. https://doi.org/10.1111/j.1440-1746.2008.05314.x
  81. Dinis-Ribeiro M, Areia M, de Vries AC, et al. Management of precancerous conditions and lesions in the stomach (MAPS): guideline from the European Society of Gastrointestinal Endoscopy (ESGE), European Helicobacter Study Group (EHSG), European Society of Pathology (ESP), and the Sociedade Portuguesa de Endoscopia Digestiva (SPED). Virchows Arch 2012;460:19-46. https://doi.org/10.1007/s00428-011-1177-8
  82. Tashiro A, Sano M, Kinameri K, Fujita K, Takeuchi Y. Comparing mass screening techniques for gastric cancer in Japan. World J Gastroenterol 2006;12:4873-4874.
  83. Dan YY, So JB, Yeoh KG. Endoscopic screening for gastric cancer. Clin Gastroenterol Hepatol 2006;4:709-716. https://doi.org/10.1016/j.cgh.2006.03.025
  84. Mori Y, Arita T, Shimoda K, Yasuda K, Yoshida T, Kitano S. Effect of periodic endoscopy for gastric cancer on early detection and improvement of survival. Gastric Cancer 2001;4:132-136. https://doi.org/10.1007/PL00011735
  85. Aida K, Yoshikawa H, Mochizuki C, et al. Clinicopathological features of gastric cancer detected by endoscopy as part of annual health checkup. J Gastroenterol Hepatol 2008;23:632-637. https://doi.org/10.1111/j.1440-1746.2008.05346.x
  86. Nam SY, Choi IJ, Park KW, et al. Effect of repeated endoscopic screening on the incidence and treatment of gastric cancer in health screenees. Eur J Gastroenterol Hepatol 2009;21:855-860. https://doi.org/10.1097/MEG.0b013e328318ed42
  87. Chung SJ, Park MJ, Kang SJ, et al. Effect of annual endoscopic screening on clinicopathologic characteristics and treatment modality of gastric cancer in a high-incidence region of Korea. Int J Cancer 2012;131:2376-2384. https://doi.org/10.1002/ijc.27501
  88. Yoon H, Kim N. Diagnosis and management of high risk group for gastric cancer. Gut Liver 2015;9:5-17. https://doi.org/10.5009/gnl14118
  89. Kim GH, Bang SJ, Ende AR, Hwang JH. Is screening and surveillance for early detection of gastric cancer needed in Korean Americans? Korean J Intern Med 2015;30:747-758. https://doi.org/10.3904/kjim.2015.30.6.747

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  24. Alterations in Gastric Microbial Communities Are Associated with Risk of Gastric Cancer in a Korean Population: A Case-Control Study vol.12, pp.9, 2020, https://doi.org/10.3390/cancers12092619
  25. Reducing gastric cancer through gastritis screening vol.14, pp.3, 2020, https://doi.org/10.1515/abm-2020-0013
  26. Improving the overall diagnostic rate of early gastric cancer by managing family members with hereditary cancer syndromes vol.20, pp.6, 2016, https://doi.org/10.3892/ol.2020.12158
  27. Response to Zhu and Xu vol.115, pp.10, 2016, https://doi.org/10.14309/ajg.0000000000000721
  28. Prevalence of gastric cancer precursors in gastroscopy-screened adults by family history of gastric cancer and of cancers other than gastric vol.20, pp.1, 2020, https://doi.org/10.1186/s12885-020-07612-8
  29. CTLA-4 polymorphisms and predisposition to digestive system malignancies: a meta-analysis of 31 published studies vol.18, pp.None, 2016, https://doi.org/10.1186/s12957-020-1806-2
  30. LncRNA growth arrest-special 5 polymorphisms and predisposition to cancer: A meta-analysis vol.35, pp.4, 2020, https://doi.org/10.1177/1724600820915483
  31. Genetic associations between CYP24A1 polymorphisms and predisposition of cancer: A meta-analysis vol.35, pp.4, 2016, https://doi.org/10.1177/1724600820944408
  32. The efficacy and safety of neoadjuvant nimotuzumab for gastric cancer : A meta-analysis of randomized controlled studies vol.100, pp.50, 2016, https://doi.org/10.1097/md.0000000000027709
  33. Upregulation of Linc-ROR Promotes the Proliferation, Migration, and Invasion of Gastric Cancer Cells Through miR-212-3p/FGF7 Axis vol.13, pp.None, 2016, https://doi.org/10.2147/cmar.s287775
  34. The Emerging Role of Circ-SHPRH in Cancer vol.14, pp.None, 2021, https://doi.org/10.2147/ott.s317403
  35. Cost‑effectiveness Analysis of Helicobacter pylori Eradication Therapy in First-Degree Relatives of Patients with Gastric Cancer vol.15, pp.None, 2016, https://doi.org/10.2147/ppa.s286860
  36. Gastric cancer screening in low incidence populations: Position statement of AEG, SEED and SEAP vol.44, pp.1, 2021, https://doi.org/10.1016/j.gastre.2020.08.001
  37. Documento de posicionamiento de la AEG, la SEED y la SEAP sobre cribado de cáncer gástrico en poblaciones con baja incidencia vol.44, pp.1, 2021, https://doi.org/10.1016/j.gastrohep.2020.08.004
  38. Disruption of Wnt/β-catenin Pathway Elevates the Sensitivity of Gastric Cancer Cells to PD-1 Antibody vol.14, pp.None, 2021, https://doi.org/10.2174/1874467214666210617163821
  39. Current status of probiotics for prevention and management of gastrointestinal cancers vol.21, pp.3, 2016, https://doi.org/10.1080/14712598.2021.1828858
  40. A comprehensive update on early gastric cancer: defining terms, etiology, and alarming risk factors vol.15, pp.3, 2016, https://doi.org/10.1080/17474124.2021.1845140
  41. Histórico familiar de câncer gástrico em pacientes dispépticos indicados à triagem endoscópica vol.34, pp.None, 2016, https://doi.org/10.37689/acta-ape/2021ao001985
  42. M‐PHASE Phosphoprotein 9 upregulation associates with poor prognosis and activates MTOR signaling in gastric cancer vol.37, pp.3, 2021, https://doi.org/10.1002/kjm2.12319
  43. Recent advances in the detection and management of early gastric cancer and its precursors vol.12, pp.4, 2016, https://doi.org/10.1136/flgastro-2018-101089
  44. Family History and Gastric Cancer Risk: A Pooled Investigation in the Stomach Cancer Pooling (STOP) Project Consortium vol.13, pp.15, 2021, https://doi.org/10.3390/cancers13153844
  45. Clinical Relevance of Helicobacter pylori Infection vol.10, pp.16, 2021, https://doi.org/10.3390/jcm10163473
  46. Beta-carotene and its protective effect on gastric cancer vol.9, pp.23, 2021, https://doi.org/10.12998/wjcc.v9.i23.6591
  47. Helicobacter pylori eradication: Exploring its impacts on the gastric mucosa vol.27, pp.31, 2021, https://doi.org/10.3748/wjg.v27.i31.5152
  48. Molecular Landscapes of Gastric Pre-Neoplastic and Pre-Invasive Lesions vol.22, pp.18, 2016, https://doi.org/10.3390/ijms22189950
  49. Visfatin facilitates gastric cancer malignancy by targeting snai1 via the NF-κB signaling vol.40, pp.10, 2016, https://doi.org/10.1177/09603271211006168
  50. Revisiting Therapeutic Strategies for H. pylori Treatment in the Context of Antibiotic Resistance: Focus on Alternative and Complementary Therapies vol.26, pp.19, 2016, https://doi.org/10.3390/molecules26196078
  51. Integrated analysis identifies oxidative stress genes associated with progression and prognosis in gastric cancer vol.11, pp.1, 2021, https://doi.org/10.1038/s41598-021-82976-w
  52. Long noncoding RNA CCAT1 rs67085638 SNP contribution to the progression of gastric cancer in a Polish population vol.11, pp.1, 2016, https://doi.org/10.1038/s41598-021-94576-9
  53. Gastric cancer genetic predisposition and clinical presentations: Established heritable causes and potential candidate genes vol.65, pp.1, 2022, https://doi.org/10.1016/j.ejmg.2021.104401