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.

  • Review Article
  • Published:

Effects of enteral nutritional rich in n-3 polyunsaturated fatty acids on the nutritional status of gastrointestinal cancer patients: a systematic review and meta-analysis

Abstract

Postoperative malnutrition is a major issue among gastrointestinal cancer patients. Because n-3 polyunsaturated fatty acids (n-3 PUFAs) have immunological benefits, n-3 PUFAs are widely used in oral nutritional supplements (ONS). However, n-3 PUFAs in ONS reduced patients’ compliance with ONS and affected the role of ONS in maintaining the postoperative nutritional status of patients. The aim of this study was to systematically explore the benefits of enteral nutrition rich in n-3 PUFAs in maintaining the nutritional status of patients after gastrointestinal surgery. Databases including PubMed, Web of Science, Embase, Cochrane Library, China National Knowledge Infrastructure, Wanfang, and VIP databases were searched through March 16, 2019. The references of related reviews and studies were assessed up to March 16, 2019. The effect sizes from individual studies were calculated as the standardized mean difference (SMD), mean difference (MD), and risk ratio (RR) with 95% confidence intervals (95% CIs). A total of 11 studies (n = 977) were included. In this systematic review and meta-analysis, we observed that enteral supplementation of n-3 PUFAs had no significant effect on weight (MD, 1.09; 95% CI, −0.90, 3.08), body mass index (MD, 0.55; 95% CI, −1.45, 2.54), albumin (SMD, 0.39; 95% CI, −0.10, 0.87), wound infections (RR, 0.87, 95% CI, 0.57, 1.33), or pneumonia (RR, 0.98; 95% CI, 0.60, 1.59) in gastrointestinal cancer patients. Thus, compared with enteral nutritional without n-3 PUFAs, enteral nutritional rich in n-3 PUFAs has no significant effects on nutritional status, incidence of pneumonia, or wound infections among gastrointestinal cancer patients during postoperative convalescence.

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

Access options

Buy this article

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Correia MI, Waitzberg DL. The impact of malnutrition on morbidity, mortality, length of hospital stay and costs evaluated through a multivariate model analysis. Clin Nutr. 2003;22:235–9.

    PubMed  Google Scholar 

  2. Cederholm T, Bosaeus I, Barazzoni R, Bauer J, Van Gossum A, Klek S, et al. Diagnostic criteria for malnutrition - an ESPEN Consensus Statement. Clin Nutr. 2015;34:335–40.

    CAS  PubMed  Google Scholar 

  3. Mosquera C, Koutlas NJ, Edwards KC, Strickland A, Vohra NA, Zervos EE, et al. Impact of malnutrition on gastrointestinal surgical patients. J Surg Res. 2016;205:95–101.

    PubMed  Google Scholar 

  4. Young LS, Huong PT, Lam NT, Thu NN, Van HT, Hanh NL, et al. Nutritional status and feeding practices in gastrointestinal surgery patients at Bach Mai Hospital, Hanoi,Vietnam. Asia Pac J Clin Nutr. 2016;25:513–20.

    PubMed  PubMed Central  Google Scholar 

  5. Chunlai C, Hui L. Patients with gastrointestinal cancer chemotherapy nutritional status assessment and its impact on immune function. J Mod Oncol. 2015;23:1412–6.

    Google Scholar 

  6. Bozzetti F, Gianotti L, Braga M, Di Carlo V, Mariani L. Postoperative complications in gastrointestinal cancer patients: the joint role of the nutritional status and the nutritional support. Clin Nutr. 2007;26:698–709.

    PubMed  Google Scholar 

  7. Aguirre A, Fischer JE, Welch CE. The role of surgery and hyperalimentation in therapy of gastrointestinal-cutaneous fistulae. Ann Surg. 1974;180:393–401.

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Goiburu ME, Goiburu MM, Bianco H, Diaz JR, Alderete F, Palacios MC, et al. The impact of malnutrition on morbidity, mortality and length of hospital stay in trauma patients. Nutricion Hospitalaria. 2006;21:604–10.

    CAS  PubMed  Google Scholar 

  9. Arends J, Bachmann P, Baracos V, Barthelemy N, Bertz H, Bozzetti F, et al. ESPEN guidelines on nutrition in cancer patients. Clin Nutr. 2017;36:11–48.

    PubMed  Google Scholar 

  10. Hatao F, Chen KY, Wu JM, Wang MY, Aikou S, Onoyama H, et al. Randomized controlled clinical trial assessing the effects of oral nutritional supplements in postoperative gastric cancer patients. Langenbeck’s Arch Surg. 2017;402:203–11.

    Google Scholar 

  11. Beattie AH, Prach AT, Baxter JP, Pennington CR. A randomised controlled trial evaluating the use of enteral nutritional supplements postoperatively in malnourished surgical patients. Gut. 2000;46:813–8.

    CAS  PubMed  PubMed Central  Google Scholar 

  12. Grass F, Bertrand PC, Schafer M, Ballabeni P, Cerantola Y, Demartines N, et al. Compliance with preoperative oral nutritional supplements in patients at nutritional risk-only a question of will? Eur J Clin Nutr. 2015;69:525–9.

    CAS  PubMed  Google Scholar 

  13. Bolton J, Abbott R, Kiely M. Comparison of three oral sip-feed supplements in patients with cancer. J Hum Nutr Dietetics. 2010;5:79–84.

    Google Scholar 

  14. Tian M, Suco E, Gosses A. MON-PP089: a double-blind study comparing taste, preference and compliance of 3 oral nutrition supplements frequently consumed by oncology Patient. Clin Nut. 2015;34:S160–1.

    Google Scholar 

  15. Fearon KC, Barber MD, Moses AG, Ahmedzai SH, Taylor GS, Tisdale MJ, et al.Double-blind placebo-controlled, randomized study of eicosapentaenoic acid diester in patients with cancer cachexia. J Clin Oncol. 2006;24:3401–7.

    CAS  PubMed  Google Scholar 

  16. Read JA, Beale PJ, Volker DH, Smith N, Childs A, Clarke SJ. Nutrition intervention using an eicosapentaenoic acid (EPA)-containing supplement in patients with advanced colorectal cancer. Effects on nutritional and inflammatory status: a phase II trial. Supportive Care Cancer. 2007;15:301–7.

    Google Scholar 

  17. Fearon KC, Von Meyenfeldt MF, Moses AG, Van Geenen R, Roy A, Gouma DJ, et al. Effect of a protein and energy dense N-3 fatty acid enriched oral supplement on loss of weight and lean tissue in cancer cachexia: a randomised double blind trial. Gut. 2003;52:1479–86.

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Bruera E, Strasser F, Palmer JL, Willey J, Calder K, Amyotte G, et al. Effect of fish oil on appetite and other symptoms in patients with advanced cancer and anorexia/cachexia: a double-blind, placebo-controlled study. J Clin Oncol. 2003;21:129–34.

    CAS  PubMed  Google Scholar 

  19. Fetterman JW Jr., Zdanowicz MM. Therapeutic potential of n-3 polyunsaturated fatty acids in disease. Am J Health-Syst Pharm. 2009;66:1169–79.

    CAS  PubMed  Google Scholar 

  20. Lane KE, Derbyshire EJ. Omega-3 fatty acids - a review of existing and innovative delivery methods. Crit Rev food Sci Nutr. 2018;58:62–9.

    CAS  PubMed  Google Scholar 

  21. Hamilton E, Ravikumar R, Bartlett D, Hepburn E, Hwang MJ, Mirza N, et al. Dexamethasone reduces emesis after major gastrointestinal surgery (DREAMS). Trials. 2013;14:249.

    PubMed  PubMed Central  Google Scholar 

  22. Kris-Etherton PM, Harris WS, Appel LJ. Fish consumption, fish oil, omega-3 fatty acids, and cardiovascular disease. Circulation. 2002;106:2747–57.

    PubMed  Google Scholar 

  23. Sacks FM, Stone PH, Gibson CM, Silverman DI, Rosner B, Pasternak RC. Controlled trial of fish oil for regression of human coronary atherosclerosis. HARP Research Group. J Am Coll Cardiol. 1995;25:1492–8.

    CAS  PubMed  Google Scholar 

  24. Wallace JM, McCabe AJ, Robson PJ, Keogh MK, Murray CA, Kelly PM, et al. Bioavailability of n-3 polyunsaturated fatty acids (PUFA) in foods enriched with microencapsulated fish oil. Ann Nutr Metab. 2000;44:157–62.

    CAS  PubMed  Google Scholar 

  25. Sultan J, Griffin SM, Di Franco F, Kirby JA, Shenton BK, Seal CJ, et al. Randomized clinical trial of omega-3 fatty acid-supplemented enteral nutrition versus standard enteral nutrition in patients undergoing oesophagogastric cancer surgery. Br J Surg. 2012;99:346–55.

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Ryan AM, Reynolds JV, Healy L, Byrne M, Moore J, Brannelly N, et al. Enteral nutrition enriched with eicosapentaenoic acid (EPA) preserves lean body mass following esophageal cancer surgery: results of a double-blinded randomized controlled trial. Ann Surg. 2009;249:355–63.

    PubMed  Google Scholar 

  27. Shuster JJ. Review: Cochrane handbook for systematic reviews for interventions, version 5.1.0, published 3/2011. Julian P.T. Higgins and Sally Green, Editors. Res Synth Methods. 2011;2:126–30.

    Google Scholar 

  28. Matsuda Y, Habu D, Lee S, Kishida S, Osugi H. Enteral diet enriched with omega-3 fatty acid improves oxygenation after thoracic esophagectomy for cancer: a randomized controlled trial. World J Surg. 2017;41:1584–94.

    PubMed  Google Scholar 

  29. Healy LA, Ryan A, Doyle SL, Ni Bhuachalla EB, Cushen S, Segurado R, et al. Does prolonged enteral feeding with supplemental omega-3 fatty acids impact on recovery post-esophagectomy: results of a randomized double-blind trial. Ann Surg. 2017;266:720–8.

    PubMed  Google Scholar 

  30. Ida S, Hiki N, Cho H, Sakamaki K, Ito S, Fujitani K, et al. Randomized clinical trial comparing standard diet with perioperative oral immunonutrition in total gastrectomy for gastric cancer. Br J Surg. 2017;104:377–83.

    CAS  PubMed  Google Scholar 

  31. Silva Jde A, Trindade EB, Fabre ME, Menegotto VM, Gevaerd S, Buss Zda S, et al. Fish oil supplement alters markers of inflammatory and nutritional status in colorectal cancer patients. Nutr Cancer. 2012;64:267–73.

    PubMed  Google Scholar 

  32. Mocellin MC, Pastore e Silva Jde A, Camargo Cde Q, Fabre ME, Gevaerd S, Naliwaiko K, et al. Fish oil decreases C-reactive protein/albumin ratio improving nutritional prognosis and plasma fatty acid profile in colorectal cancer patients. Lipids. 2013;48:879–88.

    CAS  PubMed  Google Scholar 

  33. Sorensen LS, Thorlacius-Ussing O, Schmidt EB, Rasmussen HH, Lundbye-Christensen S, Calder PC, et al. Randomized clinical trial of perioperative omega-3 fatty acid supplements in elective colorectal cancer surgery. Br J Surg. 2014;101:33–42.

    CAS  PubMed  Google Scholar 

  34. Zhuang ST, Li QZ, Cai YJ, Wu SH, Chen B, Zheng K. Effects of early postoperative enteral immune nutrition on immune function and inflammatory response in patients with colorectal cancer. Chin J Clin. 2013;7:117–9.

  35. WU YX, Xia L, Wang Y. Clinical effect of preoperative administration of enteral nutrition enriched ω-3 fatty acids for gastric cancer. Chin J Bases Clin General Surg. 2015;22:312–6.

  36. Emori TG, Gaynes RP. An overview of nosocomial infections, including the role of the microbiology laboratory. Clin Microbiol Rev. 1993;6:428–42.

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Ephgrave KS, Kleiman-Wexler R, Pfaller M, Booth B, Werkmeister L, Young S. Postoperative pneumonia: a prospective study of risk factors and morbidity. Surgery. 1993;114:815–9. discussion 9-21

    CAS  PubMed  Google Scholar 

  38. Sagawa M, Yokomizo H, Yoshimatsu K, Yano Y, Okayama S, Sakuma A, et al. Relationship between surgical site infection(ssi)incidence and prognosis in colorectal cancer surgery. Gan Kagaku Ryoho Cancer Chemother. 2017;44:921–3.

    Google Scholar 

  39. Kiuchi J, Komatsu S, Ichikawa D, Kosuga T, Okamoto K, Konishi H, et al. Putative risk factors for postoperative pneumonia which affects poor prognosis in patients with gastric cancer. Int J Clin Oncol. 2016;21:920–6.

    PubMed  Google Scholar 

  40. Guo ZQ, Yu JM, Li W, Fu ZM, Lin Y, Shi YY, et al. Survey and analysis of the nutritional status in hospitalized patients with malignant gastric tumors and its influence on the quality of life. Support Care Cancer. 2019; https://doi.org/10.1007/s00520-019-04803-3 (E-pub ahead of print 3 May 2019).

    PubMed  PubMed Central  Google Scholar 

  41. Onishi S, Shiraki M, Nishimura K, Hanai T, Moriwaki H, Shimizu M. Prevalence of sarcopenia and its relationship with nutritional state and quality of life in patients with digestive diseases. J Nutr Sci Vitaminol. 2018;64:445–53.

    CAS  PubMed  Google Scholar 

  42. Sakurai K, Ohira M, Tamura T, Toyokawa T, Amano R, Kubo N, et al. Predictive potential of preoperative nutritional status in long-term outcome projections for patients with gastric cancer. Ann Surg Oncol. 2016;23:525–33.

    PubMed  Google Scholar 

  43. Aoyama T, Sato T, Maezawa Y, Kano K, Hayashi T, Yamada T, et al. Postoperative weight loss leads to poor survival through poor S-1 efficacy in patients with stage II/III gastric cancer. Int J Clin Oncol. 2017;22:476–83.

    PubMed  Google Scholar 

  44. He Y, Wang J, Bian H, Deng X, Wang Z. BMI as a predictor for perioperative outcome of laparoscopic colorectal surgery: a pooled analysis of comparative studies. Dis Colon Rectum. 2017;60:433–45.

    PubMed  Google Scholar 

  45. Aoyama T, Kawabe T, Fujikawa H, Hayashi T, Yamada T, Tsuchida K, et al. Loss of lean body mass as an independent risk factor for continuation of S-1 adjuvant chemotherapy for gastric cancer. Ann Surg Oncol. 2015;22:2560–6.

    PubMed  Google Scholar 

  46. Aoyama T, Sato T, Segami K, Maezawa Y, Kano K, Kawabe T, et al. Risk factors for the loss of lean body mass after gastrectomy for gastric cancer. Ann Surg Oncol. 2016;23:1963–70.

    PubMed  Google Scholar 

  47. Ma YJ, Liu L, Xiao J, Cao BW. Perioperative omega-3 polyunsaturated fatty acid nutritional support in gastrointestinal cancer surgical patients: a systematic evaluation. Nutr Cancer. 2016;68:568–76.

    CAS  PubMed  Google Scholar 

  48. Matsunaga T, Miyata H, Sugimura K, Motoori M, Asukai K, Yanagimoto Y, et al. Prognostic significance of sarcopenia and systemic inflammatory response in patients with esophageal cancer. Anticancer Res. 2019;39:449–58.

    PubMed  Google Scholar 

  49. Fritsche K. Fatty acids as modulators of the immune response. Annu Rev Nutr. 2006;26:45–73.

    CAS  PubMed  Google Scholar 

  50. Yu J, Liu L, Zhang Y, Wei J, Yang F. Effects of omega-3 fatty acids on patients undergoing surgery for gastrointestinal malignancy: a systematic review and meta-analysis. BMC Cancer. 2017;17:271.

    PubMed  PubMed Central  Google Scholar 

  51. Tan A, Sullenbarger B, Prakash R, McDaniel JC. Supplementation with eicosapentaenoic acid and docosahexaenoic acid reduces high levels of circulating proinflammatory cytokines in aging adults: a randomized, controlled study. Prostaglandins, Leukotrienes, Essent Fat Acids. 2018;132:23–9.

    CAS  Google Scholar 

  52. Berger MM, Delodder F, Liaudet L, Tozzi P, Schlaepfer J, Chiolero RL, et al. Three short perioperative infusions of n-3 PUFAs reduce systemic inflammation induced by cardiopulmonary bypass surgery: a randomized controlled trial. Am J Clin Nutr. 2013;97:246–54.

    CAS  PubMed  Google Scholar 

  53. van Norren K, Kegler D, Argiles JM, Luiking Y, Gorselink M, Laviano A, et al. Dietary supplementation with a specific combination of high protein, leucine, and fish oil improves muscle function and daily activity in tumour-bearing cachectic mice. Br J cancer. 2009;100:713–22.

    PubMed  PubMed Central  Google Scholar 

  54. Hayashi N, Tashiro T, Yamamori H, Takagi K, Morishima Y, Otsubo Y, et al. Effect of intravenous omega-6 and omega-3 fat emulsions on nitrogen retention and protein kinetics in burned rats. Nutrition. 1999;15:135–9.

    CAS  PubMed  Google Scholar 

  55. Aoyama T, Yoshikawa T, Ida S, Cho H, Sakamaki K, Ito Y, et al. Effects of perioperative eicosapentaenoic acid-enriched oral nutritional supplement on lean body mass after total gastrectomy for gastric cancer. J Cancer. 2019;10:1070–6.

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Noguchi Y, Tsuburaya A, Makino T, et al. Metabolic alteration in totally gastrectomised patients—caloric intake and energy con-sumption. Asian J Surg. 1992;15:97–102.

    Google Scholar 

  57. Giger-Pabst U, Lange J, Maurer C, Bucher C, Schreiber V, Schlumpf R, et al. Short-term preoperative supplementation of an immunoenriched diet does not improve clinical outcome in well-nourished patients undergoing abdominal cancer surgery. Nutrition. 2013;29:724–9.

    PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by grants from the National natural science foundation of China [31800895] to X-yZ and Youth Science and Technology Backbone Project [2017Q026] of Health Science and Technology of Jilin Province to X-yZ.

Funding

This work was supported by the National natural science foundation of China [31800895], and Youth Science and Technology Backbone Project [2017Q026] of Health Science and Technology of Jilin Province.

Author information

Authors and Affiliations

Authors

Contributions

G-yW contributed to the performance of the study, analysis and interpretation the data, and drafted the manuscript; L-yZ contributed to the supervision of the study and interpreted the data; HY contributed to the analysis and interpretation the data; H-qL contributed to the performance of the study and revised the manuscript; and X-yZ and HX contributed to the conception of the study, performed the study, interpreted the data, and significantly revised the manuscript.

Corresponding authors

Correspondence to Hui Xue or Xiu-ying Zhang.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

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

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wan, Gy., Zheng, Ly., Li, Hq. et al. Effects of enteral nutritional rich in n-3 polyunsaturated fatty acids on the nutritional status of gastrointestinal cancer patients: a systematic review and meta-analysis. Eur J Clin Nutr 74, 220–230 (2020). https://doi.org/10.1038/s41430-019-0527-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41430-019-0527-5

Search

Quick links