Skip to main content

Advertisement

SpringerLink
Log in

Intake of vegetables and fruit and risk of esophageal adenocarcinoma: a meta-analysis of observational studies

  • Original Contribution
  • Published:
European Journal of Nutrition Aims and scope Submit manuscript

Abstract

Objectives

To study the association between the intake of fruit and vegetables and risk of esophageal adenocarcinoma (EAC), we summarized the evidence from observational studies in categorical and linear dose–response meta-analyses.

Methods

Eligible studies published up to June 2013 were retrieved via computerized searches of MEDLINE and EMBASE. Random-effects models were used to calculate summary relative risks (SRRs) and the corresponding 95 % confidence intervals (CIs). Between-study heterogeneity was assessed using the Cochran’s Q and I 2 statistics.

Results

A total of 12 studies involving 1,572 cases of EAC were included in this meta-analysis. Based on the highest versus lowest analysis, inverse associations were observed between intakes of vegetable (SRRs = 0.76, 95 % CIs 0.59–0.96; P heterogeneity = 0.098, I 2 40.4 %; n = 9 studies), intakes of fruit (SRRs = 0.73, 95 % CIs, 0.55–0.98; P heterogeneity = 0.03, I 2 = 52.9 %; n = 9 studies), and intakes of total vegetables and fruit combined (SRRs = 0.68, 95 % CI 0.49–0.93; P heterogeneity = 0.162, I 2 = 38.9 %; n = 5 studies). Similar results were also observed in a linear dose–response analysis.

Conclusion

These data support the hypothesis that intakes of vegetables and fruit may significantly reduce the risk of EAC. Further investigation with prospective designs, validated questionnaires, and good control of important confounders is warranted.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

EC:

Esophageal cancer

ESCC:

Esophageal squamous cell carcinoma

EAC:

Esophageal adenocarcinoma

BMI:

Body mass index

FFQ:

Food frequency questionnaire

SRR:

Summary relative risk

CI:

Confidence interval

GERD:

Gastroesophageal reflux disease

References

  1. Thrift AP, Whiteman DC (2012) The incidence of esophageal adenocarcinoma continues to rise: analysis of period and birth cohort effects on recent trends. Ann Oncol 23:3155–3162

    Article  CAS  Google Scholar 

  2. Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM (2010) Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer 127:2893–2917

    Article  CAS  Google Scholar 

  3. Erichsen R, Robertson D, Farkas DK, Pedersen L, Pohl H, Baron JA et al (2012) Erosive reflux disease increases risk for esophageal adenocarcinoma, compared with nonerosive reflux. Clin Gastroenterol Hepatol 10(475–480):e471

    Google Scholar 

  4. Reid BJ, Li X, Galipeau PC, Vaughan TL (2010) Barrett’s oesophagus and oesophageal adenocarcinoma: time for a new synthesis. Nat Rev Cancer 10:87–101

    Article  CAS  Google Scholar 

  5. Kubo A, Corley DA (2006) Body mass index and adenocarcinomas of the esophagus or gastric cardia: a systematic review and meta-analysis. Cancer Epidemiol Biomarkers Prev 15:872–878

    Article  Google Scholar 

  6. Tramacere I, La Vecchia C, Negri E (2011) Tobacco smoking and esophageal and gastric cardia adenocarcinoma: a meta-analysis. Epidemiology 22:344–349

    Article  Google Scholar 

  7. Mayne ST, Risch HA, Dubrow R, Chow WH, Gammon MD, Vaughan TL et al (2001) Nutrient intake and risk of subtypes of esophageal and gastric cancer. Cancer Epidemiol Biomarkers Prev 10:1055–1062

    CAS  Google Scholar 

  8. Murphy SJ, Anderson LA, Ferguson HR, Johnston BT, Watson PR, McGuigan J et al (2010) Dietary antioxidant and mineral intake in humans is associated with reduced risk of esophageal adenocarcinoma but not reflux esophagitis or Barrett’s esophagus. J Nutr 140:1757–1763

    Article  CAS  Google Scholar 

  9. Coleman HG, Murray LJ, Hicks B, Bhat SK, Kubo A, Corley DA et al (2013) Dietary fiber and the risk of precancerous lesions and cancer of the esophagus: a systematic review and meta-analysis. Nutr Rev 71:474–482

    Article  Google Scholar 

  10. Zhang ZF, Kurtz RC, Yu GP, Sun M, Gargon N, Karpeh M Jr et al (1997) Adenocarcinomas of the esophagus and gastric cardia: the role of diet. Nutr Cancer 27:298–309

    Article  CAS  Google Scholar 

  11. Chen H, Ward MH, Graubard BI, Heineman EF, Markin RM, Potischman NA et al (2002) Dietary patterns and adenocarcinoma of the esophagus and distal stomach. Am J Clin Nutr 75:137–144

    CAS  Google Scholar 

  12. Gonzalez CA, Pera G, Agudo A, Bueno-de-Mesquita HB, Ceroti M, Boeing H et al (2006) Fruit and vegetable intake and the risk of stomach and oesophagus adenocarcinoma in the European Prospective Investigation into Cancer and Nutrition (EPIC-EURGAST). Int J Cancer 118:2559–2566

    Article  CAS  Google Scholar 

  13. Anderson LA, Watson RG, Murphy SJ, Johnston BT, Comber H, Mc Guigan J et al (2007) Risk factors for Barrett’s oesophagus and oesophageal adenocarcinoma: results from the FINBAR study. World J Gastroenterol 13:1585–1594

    Article  Google Scholar 

  14. Freedman ND, Park Y, Subar AF, Hollenbeck AR, Leitzmann MF, Schatzkin A et al (2007) Fruit and vegetable intake and esophageal cancer in a large prospective cohort study. Int J Cancer 121:2753–2760

    Article  CAS  Google Scholar 

  15. Ibiebele TI, Hughes MC, Nagle CM, Bain CJ, Whiteman DC, Webb PM (2013) Dietary antioxidants and risk of Barrett’s esophagus and adenocarcinoma of the esophagus in an Australian population. Int J Cancer 133:214–224

    Article  CAS  Google Scholar 

  16. Cheng KK, Sharp L, McKinney PA, Logan RF, Chilvers CE, Cook-Mozaffari P et al (2000) A case-control study of oesophageal adenocarcinoma in women: a preventable disease. Br J Cancer 83:127–132

    Article  CAS  Google Scholar 

  17. Terry P, Lagergren J, Hansen H, Wolk A, Nyren O (2001) Fruit and vegetable consumption in the prevention of oesophageal and cardia cancers. Eur J Cancer Prev 10:365–369

    Article  CAS  Google Scholar 

  18. Navarro Silvera SA, Mayne ST, Risch H, Gammon MD, Vaughan TL, Chow WH et al (2008) Food group intake and risk of subtypes of esophageal and gastric cancer. Int J Cancer 123:852–860

    Article  Google Scholar 

  19. Pohl H, Wrobel K, Bojarski C, Voderholzer W, Sonnenberg A, Rosch T et al (2013) Risk factors in the development of esophageal adenocarcinoma. Am J Gastroenterol 108:200–207

    Article  Google Scholar 

  20. Stewart BW, Kleihues P (2003) World cancer report. IARC Press, Lyon

    Google Scholar 

  21. Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D et al (2000) Meta-analysis of observational studies in epidemiology: a proposal for reporting—Meta-analysis of Observational Studies in Epidemiology (MOOSE) group. JAMA 283:2008–2012

    Article  CAS  Google Scholar 

  22. Riboli E, Norat T (2003) Epidemiologic evidence of the protective effect of fruit and vegetables on cancer risk. Am J Clin Nutr 78:559S–569S

    CAS  Google Scholar 

  23. Wells GA, Shea B, O’Connell D, Peterson J, Welch V, Losos M, Tugwell P (2000) The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp. Accessed 15 June 2012

  24. DerSimonian R, Laird N (1986) Meta-analysis in clinical trials. Control Clin Trials 7:177–188

    Article  CAS  Google Scholar 

  25. Wolfgarten E, Rosendahl U, Nowroth T, Leers J, Metzger R, Holscher AH et al (2001) Coincidence of nutritional habits and esophageal cancer in Germany. Onkologie 24:546–551

    Article  CAS  Google Scholar 

  26. Liu J, Wang J, Leng Y, Lv C (2013) Intake of fruit and vegetables and risk of esophageal squamous cell carcinoma: a meta-analysis of observational studies. Int J Cancer 133:473–485

    Article  CAS  Google Scholar 

  27. Greenland S, Longnecker MP (1992) Methods for trend estimation from summarized dose–response data, with applications to meta-analysis. Am J Epidemiol 135:1301–1309

    CAS  Google Scholar 

  28. Orsini NBR, Greenland S (2006) Generalized least squares for trend estimation of summarized dose–response data. Stata J 6:40–57

    Google Scholar 

  29. Begg CB, Mazumdar M (1994) Operating characteristics of a rank correlation test for publication bias. Biometrics 50:1088–1101

    Article  CAS  Google Scholar 

  30. Egger M, Davey Smith G, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315:629–634

    Article  CAS  Google Scholar 

  31. Duval S, Tweedie R (2000) Trim and fill: a simple funnel-plot-based method of testing and adjusting for publication bias in meta-analysis. Biometrics 56:455–463

    Article  CAS  Google Scholar 

  32. Rink SM, Mendola P, Mumford SL, Poudrier JK, Browne RW, Wactawski-Wende J et al (2013) Self-report of fruit and vegetable intake that meets the 5 a day recommendation is associated with reduced levels of oxidative stress biomarkers and increased levels of antioxidant defense in premenopausal women. J Acad Nutr Diet 113:776–785

    Article  Google Scholar 

  33. Root MM, McGinn MC, Nieman DC, Henson DA, Heinz SA, Shanely RA et al (2012) Combined fruit and vegetable intake is correlated with improved inflammatory and oxidant status from a cross-sectional study in a community setting. Nutrients 4:29–41

    Article  CAS  Google Scholar 

  34. Wilp J, Zwickenpflug W, Richter E (2002) Nitrosation of dietary myosmine as risk factor of human cancer. Food Chem Toxicol 40:1223–1228

    Article  CAS  Google Scholar 

  35. Lukic M, Segec A, Segec I, Pinotic L, Pinotic K, Atalic B et al (2012) The impact of the vitamins A, C and E in the prevention of gastroesophageal reflux disease, Barrett’s oesophagus and oesophageal adenocarcinoma. Coll Antropol 36:867–872

    Google Scholar 

  36. Ibiebele TI, Hughes MC, Pandeya N, Zhao Z, Montgomery G, Hayward N et al (2011) High intake of folate from food sources is associated with reduced risk of esophageal cancer in an Australian population. J Nutr 141:274–283

    Article  CAS  Google Scholar 

  37. Larsson SC, Giovannucci E, Wolk A (2006) Folate intake, MTHFR polymorphisms, and risk of esophageal, gastric, and pancreatic cancer: a meta-analysis. Gastroenterology 131:1271–1283

    Article  CAS  Google Scholar 

  38. Steevens J, Schouten LJ, Goldbohm RA, van den Brandt PA (2011) Vegetables and fruits consumption and risk of esophageal and gastric cancer subtypes in the Netherlands Cohort Study. Int J Cancer 129:2681–2693

    Article  CAS  Google Scholar 

  39. Prentice RL (2003) Dietary assessment and the reliability of nutritional epidemiology reports. Lancet 362:182–183

    Article  Google Scholar 

  40. Willett WC, Sampson L, Stampfer MJ, Rosner B, Bain C, Witschi J et al (1985) Reproducibility and validity of a semiquantitative food frequency questionnaire. Am J Epidemiol 122:51–65

    CAS  Google Scholar 

  41. Rubenstein JH, Taylor JB (2010) Meta-analysis: the association of oesophageal adenocarcinoma with symptoms of gastro-oesophageal reflux. Aliment Pharmacol Ther 32:1222–1227

    Article  CAS  Google Scholar 

  42. George SM, Park Y, Leitzmann MF, Freedman ND, Dowling EC, Reedy J et al (2009) Fruit and vegetable intake and risk of cancer: a prospective cohort study. Am J Clin Nutr 89:347–353

    Article  CAS  Google Scholar 

  43. van Duijnhoven FJ, Bueno-De-Mesquita HB, Ferrari P, Jenab M, Boshuizen HC, Ros MM et al (2009) Fruit, vegetables, and colorectal cancer risk: the European Prospective Investigation into Cancer and Nutrition. Am J Clin Nutr 89:1441–1452

    Article  Google Scholar 

  44. Willett WC, Howe GR, Kushi LH (1997) Adjustment for total energy intake in epidemiologic studies. Am J Clin Nutr 65:1220S–1228S discussion 1229S–1231S

    CAS  Google Scholar 

  45. Foschi R, Pelucchi C, Dal Maso L, Rossi M, Levi F, Talamini R et al (2010) Citrus fruit and cancer risk in a network of case–control studies. Cancer Causes Control 21:237–242

    Article  Google Scholar 

  46. Bosetti C, Filomeno M, Riso P, Polesel J, Levi F, Talamini R et al (2012) Cruciferous vegetables and cancer risk in a network of case-control studies. Ann Oncol 23:2198–2203

    Article  CAS  Google Scholar 

  47. Bobe G, Peterson JJ, Gridley G, Hyer M, Dwyer JT, Brown LM (2009) Flavonoid consumption and esophageal cancer among black and white men in the United States. Int J Cancer 125:1147–1154

    Article  CAS  Google Scholar 

  48. Gonzalez CA, Jakszyn P, Pera G, Agudo A, Bingham S, Palli D et al (2006) Meat intake and risk of stomach and esophageal adenocarcinoma within the European Prospective Investigation into Cancer and Nutrition (EPIC). J Natl Cancer Inst 98:345–354

    Article  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Natural Scientific Foundation of China (No. 81201780)and Science and Technology Commission of Shanghai Municipality medical guide foundation Research Grant (No. 114119a9300).

Conflict of interest

The authors disclose no conflicts of interests.

Author information

Authors and Affiliations

  1. Department of Cardiothoracic Surgery, Changhai Hospital of Second Military Medical University, 168 Changhai Road, Shanghai, 200433, China

    Bailing Li, Gengxi Jiang, Guanxin Zhang, Qing Xue, Hao Zhang, Chong Wang & Tiejun Zhao

Authors
  1. Bailing Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gengxi Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Guanxin Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Qing Xue
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hao Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Chong Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Tiejun Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tiejun Zhao.

Additional information

Bailing Li and Gengxi Jiang have contributed equally to this paper.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 31 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Li, B., Jiang, G., Zhang, G. et al. Intake of vegetables and fruit and risk of esophageal adenocarcinoma: a meta-analysis of observational studies. Eur J Nutr 53, 1511–1521 (2014). https://doi.org/10.1007/s00394-014-0656-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00394-014-0656-5

Keywords

Search

Navigation