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Epidemiology

Allium vegetables intake and the risk of gastric cancer in the Stomach cancer Pooling (StoP) Project

Abstract

Background

The role of allium vegetables on gastric cancer (GC) risk remains unclear.

Methods

We evaluated whether higher intakes of allium vegetables reduce GC risk using individual participant data from 17 studies participating in the “Stomach cancer Pooling (StoP) Project”, including 6097 GC cases and 13,017 controls. Study-specific odds ratios (ORs) were pooled using a two-stage modelling approach.

Results

Total allium vegetables intake was inversely associated with GC risk. The pooled OR for the highest versus the lowest study-specific tertile of consumption was 0.71 (95% confidence interval, CI, 0.56–0.90), with substantial heterogeneity across studies (I2 > 50%). Pooled ORs for high versus low consumption were 0.69 (95% CI, 0.55–0.86) for onions and 0.83 (95% CI, 0.75–0.93) for garlic. The inverse association with allium vegetables was evident in Asian (OR 0.50, 95% CI, 0.29–0.86) but not European (OR 0.96, 95% CI, 0.81–1.13) and American (OR 0.66, 95% CI, 0.39–1.11) studies. Results were consistent across all other strata.

Conclusions

In a worldwide consortium of epidemiological studies, we found an inverse association between allium vegetables and GC, with a stronger association seen in Asian studies. The heterogeneity of results across geographic regions and possible residual confounding suggest caution in results interpretation.

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Fig. 1: Forest plot of allium vegetables consumption and gastric cancer risk.
Fig. 2: Exposure-response relation between allium vegetables consumption and gastric cancer.

Data availability

The data that support the findings of our study are available from the StoP Project but restrictions apply to the availability of these data, which were used under license for this study and so are not publicly available. Data are, however, available from the authors upon reasonable request and permission of the Steering Committee of the StoP Project.

References

  1. Santucci C, Carioli G, Bertuccio P, Malvezzi M, Pastorino U, Boffetta P, et al. Progress in cancer mortality, incidence, and survival: a global overview. Eur J Cancer Prev. 2020;29:367–81.

    Article  PubMed  Google Scholar 

  2. Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2021;71:209–49.

    Article  PubMed  Google Scholar 

  3. Peleteiro B, La Vecchia C, Lunet N. The role of Helicobacter pylori infection in the web of gastric cancer causation. Eur J Cancer Prev. 2012;21:118–25.

    Article  PubMed  Google Scholar 

  4. Smyth EC, Nilsson M, Grabsch HI, van Grieken NC, Lordick F. Gastric cancer. Lancet 2020;396:635–48.

    CAS  Article  PubMed  Google Scholar 

  5. World Cancer Research Fund/American Institute for Cancer Research. Continuous Update Project Expert Report 2018. Diet, nutrition, physical activity and stomach cancer. Available at dietandcancerreport.org.

  6. Fang X, Wei J, He X, An P, Wang H, Jiang L, et al. Landscape of dietary factors associated with risk of gastric cancer: a systematic review and dose-response meta-analysis of prospective cohort studies. Eur J Cancer. 2015;51:2820–32.

    Article  PubMed  Google Scholar 

  7. Bagnardi V, Rota M, Botteri E, Tramacere I, Islami F, Fedirko V, et al. Alcohol consumption and site-specific cancer risk: a comprehensive dose-response meta-analysis. Br J Cancer. 2015;112:580–93.

    CAS  Article  PubMed  Google Scholar 

  8. Ferro A, Rosato V, Rota M, Costa AR, Morais S, Pelucchi C, et al. Meat intake and risk of gastric cancer in the Stomach cancer Pooling (StoP) project. Int J Cancer. 2020;147:45–55.

    CAS  Article  PubMed  Google Scholar 

  9. Bertuccio P, Alicandro G, Rota M, Pelucchi C, Bonzi R, Galeone C, et al. Citrus fruit intake and gastric cancer: the stomach cancer pooling (StoP) project consortium. Int J Cancer. 2019;144:2936–44.

    CAS  Article  PubMed  Google Scholar 

  10. Bertuccio P, Rosato V, Andreano A, Ferraroni M, Decarli A, Edefonti V, et al. Dietary patterns and gastric cancer risk: a systematic review and meta-analysis. Ann Oncol. 2013;24:1450–8.

    CAS  Article  PubMed  Google Scholar 

  11. Buckland G, Agudo A, Lujan L, Jakszyn P, Bueno-de-Mesquita HB, Palli D, et al. Adherence to a Mediterranean diet and risk of gastric adenocarcinoma within the European Prospective Investigation into Cancer and Nutrition (EPIC) cohort study. Am J Clin Nutr. 2010;91:381–90.

    CAS  Article  PubMed  Google Scholar 

  12. Praud D, Bertuccio P, Bosetti C, Turati F, Ferraroni M, La, et al. Adherence to the Mediterranean diet and gastric cancer risk in Italy. Int J Cancer. 2014;134:2935–41.

    CAS  Article  PubMed  Google Scholar 

  13. Guercio V, Galeone C, Turati F, La Vecchia C. Gastric cancer and allium vegetable intake: a critical review of the experimental and epidemiologic evidence. Nutr Cancer. 2014;66:757–73.

    Article  PubMed  Google Scholar 

  14. Nicastro HL, Ross SA, Milner JA. Garlic and onions: their cancer prevention properties. Cancer Prev Res. 2015;8:181–9.

    CAS  Article  Google Scholar 

  15. Galeone C, Pelucchi C, Levi F, Negri E, Franceschi S, Talamini R, et al. Onion and garlic use and human cancer. Am J Clin Nutr. 2006;84:1027–32.

    CAS  Article  PubMed  Google Scholar 

  16. Galeone C, Turati F, Zhang ZF, Guercio V, Tavani A, Serraino D, et al. Relation of allium vegetables intake with head and neck cancers: evidence from the INHANCE consortium. Mol Nutr Food Res. 2015;59:1641–50.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  17. Turati F, Guercio V, Pelucchi C, La Vecchia C, Galeone C. Colorectal cancer and adenomatous polyps in relation to allium vegetables intake: a meta-analysis of observational studies. Mol Nutr Food Res. 2014;58:1907–14.

    CAS  Article  PubMed  Google Scholar 

  18. Turati F, Pelucchi C, Guercio V, La Vecchia C, Galeone C. Allium vegetable intake and gastric cancer: a case-control study and meta-analysis. Mol Nutr Food Res. 2015;59:171–9.

    CAS  Article  PubMed  Google Scholar 

  19. Zhou Y, Zhuang W, Hu W, Liu GJ, Wu TX, Wu XT. Consumption of large amounts of Allium vegetables reduces risk for gastric cancer in a meta-analysis. Gastroenterology. 2011;141:80–9.

    CAS  Article  PubMed  Google Scholar 

  20. Kodali RT, Eslick GD. Meta-analysis: Does garlic intake reduce risk of gastric cancer? Nutr Cancer. 2015;67:1–11.

    CAS  Article  PubMed  Google Scholar 

  21. 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.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  22. Pelucchi C, Lunet N, Boccia S, Zhang ZF, Praud D, Boffetta P, et al. The stomach cancer pooling (StoP) project: study design and presentation. Eur J Cancer Prev. 2015;24:16–23.

    Article  PubMed  Google Scholar 

  23. Benetou V, Trichopoulou A, Orfanos P, Naska A, Lagiou P, Boffetta P, et al. Conformity to traditional Mediterranean diet and cancer incidence: the Greek EPIC cohort. Br J Cancer. 2008;99:191–5.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  24. Lagiou P, Samoli E, Lagiou A, Peterson J, Tzonou A, Dwyer J, et al. Flavonoids, vitamin C and adenocarcinoma of the stomach. Cancer Causes Control. 2004;15:67–72.

    CAS  Article  PubMed  Google Scholar 

  25. Lucenteforte E, Scita V, Bosetti C, Bertuccio P, Negri E, La Vecchia C. Food groups and alcoholic beverages and the risk of stomach cancer: a case-control study in Italy. Nutr Cancer. 2008;60:577–84.

    Article  PubMed  Google Scholar 

  26. Buiatti E, Palli D, Decarli A, Amadori D, Avellini C, Bianchi S, et al. A case-control study of gastric cancer and diet in Italy. Int J Cancer. 1989;44:611–6.

    CAS  Article  PubMed  Google Scholar 

  27. Castano-Vinyals G, Aragones N, Perez-Gomez B, Martin V, Llorca J, Moreno V, et al. Population-based multicase-control study in common tumors in Spain (MCC-Spain): rationale and study design. Gac Sanit. 2015;29:308–15.

    Article  PubMed  Google Scholar 

  28. Santibanez M, Alguacil J, de la Hera MG, Navarrete-Munoz EM, Llorca J, Aragones N, et al. Occupational exposures and risk of stomach cancer by histological type. Occup Environ Med. 2012;69:268–75.

    Article  PubMed  Google Scholar 

  29. Lunet N, Valbuena C, Vieira AL, Lopes C, Lopes C, David L, et al. Fruit and vegetable consumption and gastric cancer by location and histological type: case-control and meta-analysis. Eur J Cancer Prev. 2007;16:312–27.

    Article  PubMed  Google Scholar 

  30. Zaridze D, Borisova E, Maximovitch D, Chkhikvadze V. Alcohol consumption, smoking and risk of gastric cancer: case-control study from Moscow, Russia. Cancer Causes Control. 2000;11:363–71.

    CAS  Article  PubMed  Google Scholar 

  31. Pourfarzi F, Whelan A, Kaldor J, Malekzadeh R. The role of diet and other environmental factors in the causation of gastric cancer in Iran-a population based study. Int J Cancer. 2009;125:1953–60.

    CAS  Article  PubMed  Google Scholar 

  32. Pakseresht M, Forman D, Malekzadeh R, Yazdanbod A, West RM, Greenwood DC, et al. Dietary habits and gastric cancer risk in north-west Iran. Cancer Causes Control. 2011;22:725–36.

    Article  PubMed  Google Scholar 

  33. Mu LN, Lu QY, Yu SZ, Jiang QW, Cao W, You NC, et al. Green tea drinking and multigenetic index on the risk of stomach cancer in a Chinese population. Int J Cancer. 2005;116:972–83.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  34. Setiawan VW, Yu GP, Lu QY, Lu ML, Yu SZ, Mu L, et al. Allium vegetables and stomach cancer risk in China. Asian Pac J Cancer Prev. 2005;6:387–95.

    PubMed  Google Scholar 

  35. Deandrea S, Foschi R, Galeone C, La Vecchia C, Negri E, Hu J. Is temperature an effect modifier of the association between green tea intake and gastric cancer risk? Eur J Cancer Prev. 2010;19:18–22.

    CAS  Article  PubMed  Google Scholar 

  36. Machida-Montani A, Sasazuki S, Inoue M, Natsukawa S, Shaura K, Koizumi Y, et al. Association of Helicobacter pylori infection and environmental factors in non-cardia gastric cancer in Japan. Gastric Cancer. 2004;7:46–53.

    Article  PubMed  Google Scholar 

  37. Hernandez-Ramirez RU, Galvan-Portillo MV, Ward MH, Agudo A, Gonzalez CA, Onate-Ocana LF, et al. Dietary intake of polyphenols, nitrate and nitrite and gastric cancer risk in Mexico City. Int J Cancer. 2009;125:1424–30.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  38. Lopez-Carrillo L, Hernandez Avila M, Dubrow R. Chili pepper consumption and gastric cancer in Mexico: a case-control study. Am J Epidemiol. 1994;139:263–71.

    CAS  Article  PubMed  Google Scholar 

  39. Ward MH, Sinha R, Heineman EF, Rothman N, Markin R, Weisenburger DD, et al. Risk of adenocarcinoma of the stomach and esophagus with meat cooking method and doneness preference. Int J Cancer. 1997;71:14–9.

    CAS  Article  PubMed  Google Scholar 

  40. Mao Y, Hu J, Semenciw R, White K, Canadian Cancer Registries Epidemiology Research G. Active and passive smoking and the risk of stomach cancer, by subsite, in Canada. Eur J Cancer Prev. 2002;11:27–38.

    CAS  Article  PubMed  Google Scholar 

  41. Burke DL, Ensor J, Riley RD. Meta-analysis using individual participant data: one-stage and two-stage approaches, and why they may differ. Stat Med. 2017;36:855–75.

    Article  PubMed  Google Scholar 

  42. DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1986;7:177–88.

    CAS  Article  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  44. Bianchini F, Vainio H. Allium vegetables and organosulfur compounds: do they help prevent cancer? Environ Health Perspect. 2001;109:893–902.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  45. Wroblewski LE, Peek RM Jr., Wilson KT. Helicobacter pylori and gastric cancer: factors that modulate disease risk. Clin Microbiol Rev. 2010;23:713–39.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  46. Sivam GP, Lampe JW, Ulness B, Swanzy SR, Potter JD. Helicobacter pylori-in vitro susceptibility to garlic (Allium sativum) extract. Nutr Cancer. 1997;27:118–21.

    CAS  Article  PubMed  Google Scholar 

  47. Iimuro M, Shibata H, Kawamori T, Matsumoto T, Arakawa T, Sugimura T, et al. Suppressive effects of garlic extract on Helicobacter pylori-induced gastritis in Mongolian gerbils. Cancer Lett. 2002;187:61–8.

    CAS  Article  PubMed  Google Scholar 

  48. Li Z, Ying X, Shan F, Ji J. The association of garlic with Helicobacter pylori infection and gastric cancer risk: a systematic review and meta-analysis. Helicobacter. 2018;23:e12532.

    Article  PubMed  Google Scholar 

  49. Gail MH, Pfeiffer RM, Brown LM, Zhang L, Ma JL, Pan KF, et al. Garlic, vitamin, and antibiotic treatment for Helicobacter pylori: a randomized factorial controlled trial. Helicobacter. 2007;12:575–8.

    Article  PubMed  Google Scholar 

  50. Kockar C, Ozturk M, Bavbek N. Helicobacter pylori eradication with beta carotene, ascorbic acid and allicin. Acta Med (Hradec Kralove). 2001;44:97–100.

    CAS  Article  Google Scholar 

  51. Farhat Z, Hershberger PA, Freudenheim JL, Mammen MJ, Hageman Blair R, Aga DS, et al. Types of garlic and their anticancer and antioxidant activity: a review of the epidemiologic and experimental evidence. Eur J Nutr. 2021;60:3585–609.

  52. Ioku K, Aoyama Y, Tokuno A, Terao J, Nakatani N, Takei Y. Various cooking methods and the flavonoid content in onion. J Nutr Sci Vitaminol. 2001;47:78–83.

    CAS  Article  PubMed  Google Scholar 

  53. Song K, Milner JA. The influence of heating on the anticancer properties of garlic. J Nutr. 2001;131:1054S–7S.

    CAS  Article  PubMed  Google Scholar 

  54. Kim HJ, Chang WK, Kim MK, Lee SS, Choi BY. Dietary factors and gastric cancer in Korea: a case-control study. Int J Cancer. 2002;97:531–5.

    CAS  Article  PubMed  Google Scholar 

  55. Yuan P, Lin L, Zheng K, Wang W, Wu S, Huang L, et al. Risk factors for gastric cancer and related serological levels in Fujian, China: hospital-based case-control study. BMJ Open. 2020;10:e042341.

    Article  PubMed  PubMed Central  Google Scholar 

  56. Tuyns AJ, Kaaks R, Haelterman M, Riboli E. Diet and gastric cancer. A case-control study in Belgium. Int J Cancer. 1992;51:1–6.

    CAS  Article  PubMed  Google Scholar 

  57. Boeing H, Jedrychowski W, Wahrendorf J, Popiela T, Tobiasz-Adamczyk B, Kulig A. Dietary risk factors in intestinal and diffuse types of stomach cancer: a multicenter case-control study in Poland. Cancer Causes Control. 1991;2:227–33.

    CAS  Article  PubMed  Google Scholar 

  58. Gonzalez CA, Lujan-Barroso L, Bueno-de-Mesquita HB, Jenab M, Duell EJ, Agudo A, et al. Fruit and vegetable intake and the risk of gastric adenocarcinoma: a reanalysis of the European Prospective Investigation into Cancer and Nutrition (EPIC-EURGAST) study after a longer follow-up. Int J Cancer. 2012;131:2910–9.

    CAS  Article  PubMed  Google Scholar 

  59. Epplein M, Shu XO, Xiang YB, Chow WH, Yang G, Li HL, et al. Fruit and vegetable consumption and risk of distal gastric cancer in the Shanghai Women’s and Men’s Health studies. Am J Epidemiol. 2010;172:397–406.

    Article  PubMed  PubMed Central  Google Scholar 

  60. Larsson SC, Bergkvist L, Wolk A. Fruit and vegetable consumption and incidence of gastric cancer: a prospective study. Cancer Epidemiol Biomark Prev. 2006;15:1998–2001.

    Article  Google Scholar 

  61. Steevens J, Schouten LJ, Goldbohm RA, van den Brandt PA. Vegetables and fruits consumption and risk of esophageal and gastric cancer subtypes in the Netherlands Cohort Study. Int J Cancer. 2011;129:2681–93.

    CAS  Article  PubMed  Google Scholar 

  62. Ma JL, Zhang L, Brown LM, Li JY, Shen L, Pan KF, et al. Fifteen-year effects of Helicobacter pylori, garlic, and vitamin treatments on gastric cancer incidence and mortality. J Natl Cancer Inst. 2012;104:488–92.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  63. Ferro A, Costa AR, Morais S, Bertuccio P, Rota M, Pelucchi C, et al. Fruits and vegetables intake and gastric cancer risk: a pooled analysis within the Stomach cancer Pooling Project. Int J Cancer. 2020;147:3090–101.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  64. Smith SJ, Steinberg KK, Thacker SB. Methods for pooled analyses of epidemiologic studies. Epidemiology. 1994;5:381–3.

    CAS  Article  PubMed  Google Scholar 

  65. Ferro A, Morais S, Rota M, Pelucchi C, Bertuccio P, Bonzi R, et al. Alcohol intake and gastric cancer: meta-analyses of published data versus individual participant data pooled analyses (StoP Project). Cancer Epidemiol. 2018;54:125–32.

    Article  PubMed  Google Scholar 

  66. Ioannidis JP, Schully SD, Lam TK, Khoury MJ. Knowledge integration in cancer: current landscape and future prospects. Cancer Epidemiol Biomark Prev. 2013;22:3–10.

    Article  Google Scholar 

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Acknowledgements

The authors thank the European Cancer Prevention (ECP) Organization for providing support for the StoP Project meetings and all MCC-Spain study collaborators (CIBERESP, ISCIII, ISGlobal, ICO, University of Huelva, University of Oviedo, University of Cantabria, ibs.Granada, Instituto Salud Pública de Navarra, FISABIO, Murcia Regional Health Authority and cols).

Funding

This study was supported by the Fondazione AIRC per la Ricerca sul Cancro, Project no. 21378 (Investigator Grant), and by the Italian League for the Fight Against Cancer (LILT), which did not play a role in study design, data collection, data analysis, interpretation of the results or in the writing of this manuscript. The Unidade de Investigação em Epidemiologia—Instituto de Saúde Pública da Universidade do Porto (EPIUnit; UIDB/04750/2020) was funded by the Foundation for Science and Technology—FCT (Portuguese Ministry of Science, Technology and Higher Education). SM was also funded by the project “NEON-PC—Neuro-oncological complications of prostate cancer: a longitudinal study of cognitive decline” (POCI-01–0145-FEDER-032358; ref. PTDC/SAU-EPI/32358/2017), which is funded by FEDER through the Operational Programme Competitiveness and Internationalisation, national funding from FCT, and the EPIUnit – Junior Research – Prog Financing (UIDP/04750/2020). The Brasilian study was funded by Fundação de Amparo à Pesquisa do Estado de São Paulo-FAPESP number 2014/26897-0 SaoPaulo Brasil.

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Authors

Contributions

MD performed the statistical analysis, interpreted the data and revised the manuscript; FT drafted the manuscript; MR and GM contributed to the statistical analysis; MR, CP, RB and CG harmonised the data, as part of the Stomach Cancer Pooling (StoP) Project; ZFZ, NL, DP, MF, GPY, SM, RM, LLC, DZ, DM, NA, GFT, VM, JV, MGH, MPC, FJFC, PA, MP, JH, RUHR, MW, FP, LM, ST, AH, PL, AL, AT, AK, PB, MCC, EN and CLV supplied the data as part of the StoP Project; CLV and CP supervised the analysis and interpretation of data, and reviewed the manuscript for important intellectual content; CP defined the study hypotheses and designed the investigation, and had primary responsibility for final content. All authors have read and approved the final manuscript.

Corresponding author

Correspondence to Federica Turati.

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The authors declare no competing interests.

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Ethics approval and consent to participate

The participating studies were performed in accordance with laws, regulations and guidelines for the protection of human subjects (including consent from the participants) applicable at the time of study conduction, and in accordance with the Declaration of Helsinki. All identifying information was removed before data were pooled at the study coordinating centre located at the University of Milan. The StoP Project received ethical approval from the University of Milan Review Board (reference 19/15 on 01/04/2015).

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Dalmartello, M., Turati, F., Zhang, ZF. et al. Allium vegetables intake and the risk of gastric cancer in the Stomach cancer Pooling (StoP) Project. Br J Cancer 126, 1755–1764 (2022). https://doi.org/10.1038/s41416-022-01750-5

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