Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Nutrition and Health (including climate and ecological aspects)

Effect of dietary consumption on the survival of esophageal squamous cell carcinoma: a prospective cohort study

European Journal of Clinical Nutrition volume 77, pages 55–64 (2023)Cite this article

Subjects

Abstract

Background/Objectives

This prospective cohort study was to assess the association of pre-diagnostic dietary intake and dietary pattern with the survival of esophageal squamous cell carcinoma (ESCC) patients.

Subjects/Methods

855 patients were recruited and successfully followed. Information on diet over past five years before diagnosis was collected using a food frequency questionnaire, and dietary patterns were extracted using principal component analysis. Hazard ratio (HR) with 95% confidence interval (95% CI) was calculated using the Cox proportional hazard model.

Results

164 (19.18%) ESCC patients survived during the follow-up. Every 25-g increment intake of pickled vegetables was associated with a 6.0% (HR: 1.060, 95% CI: 1.003–1.121) increased risk of death after adjustment for covariates. When comparing the highest with lowest tertiles of energy-adjusted intake, pickled vegetables intake was associated with a 21.9% elevated risk of death (HR: 1.219, 95% CI: 1.014–1.465), while fish and shrimp intake was associated with a 19.4% (HR: 0.816, 95% CI: 0.675–0.986) reduced risk of death. Three dietary patterns were defined and labeled as patterns I, II, and III. Every 10-score increment of dietary pattern II, characterized with a higher loading of preserved vegetables, pickled vegetables, and salted meat, was associated with a 1.7% (HR: 1.017, 95% CI: 1.003–1.032) increased risk of death.

Conclusions

A diet characterized with higher loading of preserved vegetables, pickled vegetables, and salted meat, was negatively associated with death risk among ESCC patients. Prospective studies concerning the role of post-diagnosis dietary intake in ESCC prognosis are needed.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Similar content being viewed by others

Data availability

The data used to support the findings of this study are available from the corresponding author upon request and a detailed protocol should be provided.

References

  1. Asombang AW, Kayamba V, Lisulo MM, Trinkaus K, Mudenda V, Sinkala E, et al. Esophageal squamous cell cancer in a highly endemic region. World J Gastroenterol. 2016;22:2811–7.

    Article  CAS  Google Scholar 

  2. Sheikh M, Poustchi H, Pourshams A, Etemadi A, Islami F, Khoshnia M, et al. Individual and Combined Effects of Environmental Risk Factors for Esophageal Cancer Based on Results From the Golestan Cohort Study. Gastroenterology. 2019;156:1416–27.

    Article  Google Scholar 

  3. Thrumurthy SG, Chaudry MA, Thrumurthy SSD, Mughal M. Oesophageal cancer: risks, prevention, and diagnosis. Bmj. 2019;366:l4373.

    Article  Google Scholar 

  4. 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 Clinicians. 2018;68:394–424.

    Google Scholar 

  5. Siegel RL, Miller KD, Jemal A. Cancer statistics, 2016. CA: Cancer J Clinicians. 2016;66:7–30.

    Google Scholar 

  6. Pennathur A, Gibson MK, Jobe BA, Luketich JD. Oesophageal carcinoma. Lancet (Lond, Engl). 2013;381:400–12.

    Article  Google Scholar 

  7. Cao J, Xu H, Li W, Guo Z, Lin Y, Shi Y, et al. Nutritional assessment and risk factors associated to malnutrition in patients with esophageal cancer. Curr Probl Cancer. 2021;45:100638.

    Article  Google Scholar 

  8. Anandavadivelan P, Lagergren P. Cachexia in patients with oesophageal cancer. Nat Rev Clin Oncol. 2016;13:185–98.

    Article  CAS  Google Scholar 

  9. Xiao-Bo Y, Qiang L, Xiong Q, Zheng R, Jian Z, Jian-Hua Z, et al. Efficacy of early postoperative enteral nutrition in supporting patients after esophagectomy. Minerva Chir. 2014;69:37–46.

    CAS  Google Scholar 

  10. Zheng R, Devin CL, Pucci MJ, Berger AC, Rosato EL, Palazzo F. Optimal timing and route of nutritional support after esophagectomy: A review of the literature. World J Gastroenterol. 2019;25:4427–36.

    Article  Google Scholar 

  11. Lu C, Xie H, Wang FL, Shen HB, Wang JM. Diet folate, DNA methylation and genetic polymorphisms of MTHFR C677T in association with the prognosis of esophageal squamous cell carcinoma. BMC Cancer. 2011;11:91. https://doi.org/10.1186/1471-2407-11-91.

    Article  CAS  Google Scholar 

  12. Jing C, Huang ZJ, Duan YQ, Xiao XR, Zhang R, Jiang JQ. Folate Intake, Methylenetetrahydrofolate Reductase Polymorphisms in Association with the Prognosis of Esophageal Squamous Cell Carcinoma. Asian Pac J Cancer Prev. 2012;13:647–51.

    Article  Google Scholar 

  13. Shi F, Yan FC, Jin ML, Chang H, Zhou Q, Zhao L, et al. Pre-diagnosis consumption of preserved vegetables and prognosis of invasive oesophageal squamous cell carcinoma: a prospective cohort study in one high-risk area in China. J Int Med Res. 2018;46:4306–14.

    Article  Google Scholar 

  14. Lin S, Wang X, Huang C, Liu X, Zhao J, Yu IT, et al. Consumption of salted meat and its interactions with alcohol drinking and tobacco smoking on esophageal squamous-cell carcinoma. Int J Cancer. 2015;137:582–9.

    Article  CAS  Google Scholar 

  15. Liu X, Wang X, Lin S, Lao X, Zhao J, Song Q, et al. Dietary patterns and the risk of esophageal squamous cell carcinoma: A population-based case-control study in a rural population. Clin Nutr (Edinb, Scotl). 2017;36:260–6.

    Article  CAS  Google Scholar 

  16. Chen R, Liu Y, Song G, Li B, Zhao D, Hua Z, et al. Effectiveness of one-time endoscopic screening programme in prevention of upper gastrointestinal cancer in China: a multicentre population-based cohort study. Gut. 2021;70:251–60.

    Google Scholar 

  17. Weir CB, Jan A BMI Classification Percentile And Cut Off Points. In: StatPearls: Treasure Island (FL), 2021.

  18. Liu X, Wang X, Lin S, Song Q, Lao X, Yu IT. Reproducibility and Validity of a Food Frequency Questionnaire for Assessing Dietary Consumption via the Dietary Pattern Method in a Chinese Rural Population. PloS One. 2015;10:e0134627.

    Article  Google Scholar 

  19. Liu X, Li H, Zhao Y, Li J, Zhang J, Ma L, et al. Reproducibility and relative validity of a food frequency questionnaire for a diet-related study in a rural Chinese population. Nutr J. 2022;21:3.

    Article  Google Scholar 

  20. Yang Y China Food Composition Tables (Standard Edition). In: Peking University Medical Press: Beijing, China, 2018.

  21. Agnoli C, Pounis G, Krogh V Dietary Pattern Analysis. In: Pounis G (ed) Analysis in Nutrition Research. Academic Press, 2019, pp 75–101.

  22. Smith AD, Emmett PM, Newby PK, Northstone K. Dietary patterns obtained through principal components analysis: the effect of input variable quantification. Br J Nutr. 2013;109:1881–91.

    Article  CAS  Google Scholar 

  23. Rösler F, Manzey D. Principal components and varimax-rotated components in event-related potential research: some remarks on their interpretation. Biol Psychol. 1981;13:3–26.

    Article  Google Scholar 

  24. Willett W. Nutritional epidemiology, 3rd edn Oxford University Press: New York; Oxford, 2013.

  25. Zhao J, Li Z, Gao Q, Zhao H, Chen S, Huang L, et al. A review of statistical methods for dietary pattern analysis. Nutr J. 2021;20:37.

    Article  Google Scholar 

  26. Allen M. Factor Analysis: Varimax Rotation. In: the SAGE Encyclopedia of Communication Research Methods, SAGE Publications, Inc: Thousand Oaks, CA, 2017.

  27. Kabacoff R. R in action: data analysis and graphics with R (Second edition), Manning Publications: New York, 2015.

  28. Willett WC, Howe GR, Kushi LH. Adjustment for total energy intake in epidemiologic studies. Am J Clin Nutr. 1997;65:1220S–1228S.

    Article  CAS  Google Scholar 

  29. IARC Working Group. Some naturally occurring substances: food items and constituents, heterocyclic aromatic amines and mycotoxins. IARC monographs on the evaluation of carcinogenic risks to humans, vol. 56. IARC Press: Lyon, 1993.

  30. Hou JC, Jiang CG, Long ZC. Nitrite level of pickled vegetables in Northeast China. Food Control. 2013;29:7–10.

    Article  CAS  Google Scholar 

  31. Wang P, Leng J, Wang Y. DNA replication studies of N-nitroso compound-induced O (6)-alkyl-2’-deoxyguanosine lesions in Escherichia coli. J Biol Chem. 2019;294:3899–908.

    Article  CAS  Google Scholar 

  32. Baba S, Yamada Y, Hatano Y, Miyazaki Y, Mori H, Shibata T, et al. Global DNA hypomethylation suppresses squamous carcinogenesis in the tongue and esophagus. Cancer Sci. 2009;100:1186–91.

    Article  CAS  Google Scholar 

  33. Hebels DG, Brauers KJ, van Herwijnen MH, Georgiadis PA, Kyrtopoulos SA, Kleinjans JC, et al. Time-series analysis of gene expression profiles induced by nitrosamides and nitrosamines elucidates modes of action underlying their genotoxicity in human colon cells. Toxicol Lett. 2011;207:232–41.

    Article  CAS  Google Scholar 

  34. Capilla-Gonzalez V, Gil-Perotin S, Garcia-Verdugo JM. Postnatal exposure to N-ethyl-N-nitrosurea disrupts the subventricular zone in adult rodents. Eur J Neurosci. 2010;32:1789–99.

    Article  CAS  Google Scholar 

  35. Chikan NA, Shabir N, Shaff S, Mir MR, Patel TN. N-nitrosodimethylamine in the Kashmiri diet and possible roles in the high incidence of gastrointestinal cancers. Asian Pac J Cancer Prev: APJCP. 2012;13:1077–9.

    Article  Google Scholar 

  36. Hu XF, Chan HM. Seafood Consumption and Its Contribution to Nutrients Intake among Canadians in 2004 and 2015. Nutrients. 2020;13:77.

    Article  Google Scholar 

  37. Shen Y, Zhou Y, He T, Zhuang X. Effect of Preoperative Nutritional Risk Screening and Enteral Nutrition Support in Accelerated Recovery after Resection for Esophageal Cancer. Nutr Cancer. 2021;73:596–601.

    Article  Google Scholar 

  38. Van Cutsem E, Arends J. The causes and consequences of cancer-associated malnutrition. Eur J Oncol Nurs: J Eur Oncol Nurs Soc. 2005;9:S51–63.

    Article  Google Scholar 

  39. Li W, Zhu M, Chen P, Lu W. [Study on dietary pattern and nutrients intakes of residents in areas of high and low incidence of esophageal cancer]. Wei Sheng Yan Jiu. 1997;26:351–5.

    CAS  Google Scholar 

  40. Jaskiewicz K, Marasas WF, Lazarus C, Beyers AD, Van Helden PD. Association of esophageal cytological abnormalities with vitamin and lipotrope deficiencies in populations at risk for esophageal cancer. Anticancer Res. 1988;8:711–5.

    CAS  Google Scholar 

  41. Levine ME, Suarez JA, Brandhorst S, Balasubramanian P, Cheng CW, Madia F, et al. Low protein intake is associated with a major reduction in IGF-1, cancer, and overall mortality in the 65 and younger but not older population. Cell Metab. 2014;19:407–17.

    Article  CAS  Google Scholar 

  42. Harbige LS. Fatty acids, the immune response, and autoimmunity: a question of n-6 essentiality and the balance between n-6 and n-3. Lipids. 2003;38:323–41.

    Article  CAS  Google Scholar 

  43. Calder PC. N-3 polyunsaturated fatty acids and inflammation: from molecular biology to the clinic. Lipids. 2003;38:343–52.

    Article  CAS  Google Scholar 

  44. Nabavi SF, Bilotto S, Russo GL, Orhan IE, Habtemariam S, Daglia M, et al. Omega-3 polyunsaturated fatty acids and cancer: lessons learned from clinical trials. Cancer Metastasis Rev. 2015;34:359–80.

    Article  CAS  Google Scholar 

  45. Wang JB, Fan JH, Dawsey SM, Sinha R, Freedman ND, Taylor PR, et al. Dietary components and risk of total, cancer and cardiovascular disease mortality in the Linxian Nutrition Intervention Trials cohort in China. Sci Rep. 2016;6:22619.

    Article  CAS  Google Scholar 

  46. Carr PR, Jansen L, Walter V, Kloor M, Roth W, Bläker H, et al. Associations of red and processed meat with survival after colorectal cancer and differences according to timing of dietary assessment. Am J Clin Nutr. 2016;103:192–200.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors would like to thank epidemiologists, nurses, and doctors in the Yanting Tumor Hospital, Yanting Center for Disease Control and Prevention, and the community-based health service centers for their cooperation in data collection, and thank all study subjects for their participation.

Funding

The study was supported by the Guangdong Basic and Applied Basic Research Foundation (Nos. 2019A1515011599, 2022A1515010686), the Science and Technology Program of Guangzhou City (No.202102080404), the National Key R&D Program of China (No. 2018YFE0208000). The founder had no role in the design, analysis, or writing of this manuscript.

Author information

Author notes

  1. These authors contributed equally: Yue Zhao, Wenjing Zhao, Jun Li.

Authors and Affiliations

  1. Department of Epidemiology, School of Public Health, Sun Yat-sen University, Guangzhou, China

    Yue Zhao, Zefang Ren & Jiahai Lu

  2. School of Public Health, Guangdong Pharmaceutical University, Guangzhou, China

    Yue Zhao & Xudong Liu

  3. School of Public Health and Emergency Management, Southern University of Science and Technology, Shenzhen, China

    Wenjing Zhao

  4. Department of Cancer Prevention and Treatment, Yanting Cancer Hospital, Mianyang, China

    Jun Li & Lin Li

  5. School of Management, Putian University, Putian, China

    Sihao Lin

  6. Department of Gastroenterology, the First Affiliated Hospital of Sun Yat-sen University, Guangzhou, China

    Xiangbing Xing

Authors
  1. Yue Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wenjing Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jun Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sihao Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Lin Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Zefang Ren
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jiahai Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Xiangbing Xing
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Xudong Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

XDL conceived and designed the study; YZ analyzed the data; JL, LL, SHL, XDL collected the data; YZ and WJZ drafted the manuscript; ZFR, JL, JHL, SHL, XBX, and XDL reviewed and edited the manuscript. All co-authors provided comments and approved the final version.

Corresponding author

Correspondence to Xudong Liu.

Ethics declarations

Competing interests

The authors declare no competing interests.

Ethics approval and consent to participate

The study was approved Ethical Review Committee for Biomedical Research, School of Public Health, Sun Yat-sen University (No. 2019-096). It met the requirements of the Declaration of Helsinki and Informed consent was obtained from all subjects involved in the study. Patients and/or the public were not involved in the design, conduct, reporting, or dissemination plans of this research.

Consent for publication

All authors have read and agreed to the published version of the manuscript.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhao, Y., Zhao, W., Li, J. et al. Effect of dietary consumption on the survival of esophageal squamous cell carcinoma: a prospective cohort study. Eur J Clin Nutr 77, 55–64 (2023). https://doi.org/10.1038/s41430-022-01194-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41430-022-01194-3

This article is cited by

Search

Advanced search

Quick links