DOI QR코드

DOI QR Code

Dose-Dependent Impacts of Omega-3 Fatty Acids Supplementation on Anthropometric Variables in Patients With Cancer: Results From a Systematic Review and Meta-Analysis of Randomized Clinical Trials

  • Seyed Mojtaba Ghoreishy (Student Research Committee, School of Public Health, Iran University of Medical Sciences) ;
  • Sheida Zeraattalab-Motlagh (Department of Health & Human Performance, University of Houston) ;
  • Reza Amiri Khosroshahi (Department of Clinical Nutrition, School of Nutritional Sciences and Dietetics, Tehran University of Medical Sciences) ;
  • Amirhossein Hemmati (Department of Clinical Nutrition, School of Nutritional Sciences and Dietetics, Tehran University of Medical Sciences) ;
  • Morvarid Noormohammadi (Student Research Committee, School of Public Health, Iran University of Medical Sciences) ;
  • Hamed Mohammadi (Department of Clinical Nutrition, School of Nutritional Sciences and Dietetics, Tehran University of Medical Sciences)
  • 투고 : 2024.05.14
  • 심사 : 2024.07.19
  • 발행 : 2024.07.31

초록

Meta-analyses have been conducted with conflicting results on this topic. Due to missing several eligible studies in previous meta-analysis by Lam et al., we conducted an extensive systematic review and dose-response meta-analysis of randomized controlled trials in this regard. A comprehensive search was conducted across various databases, including MEDLINE/PubMed, ISI Web of Knowledge, Scopus, and Google Scholar, until November 2023. Based on the analysis of 33 studies comprising 2,047 individuals, it was found that there was a significant increase in body weight for each 1 g/day increase in omega-3 lipids (standardized MD [SMD], 0.52 kg; 95% confidence interval [CI], 0.31, 0.73; I2 = 95%; Grading of Recommendations Assessment, Development and Evaluation [GRADE] = low). Supplementation of omega-3 fatty acids did not yield a statistically significant impact on body mass index (BMI) (SMD, 0.12 kg/m2; 95% CI, -0.02, 0.27; I2 = 79%; GRADE = very low), lean body mass (LBM) (SMD, -0.02 kg; 95% CI, -0.43, 0.39; I2 = 97%; GRADE = very low), fat mass (SMD, 0.45 kg; 95% CI, -0.25, 1.15; I2 = 96%; GRADE = low), and body fat (SMD, 0.30%; 95% CI, -0.90, 1.51; I2 = 96%; GRADE = very low). After excluding 2 studies, the findings were significant for BMI. Regarding the results of the dose-response analysis, body weight increased proportionally by increasing the dose of omega-3 supplementation up to 4 g/day. Omega-3 fatty acid supplementation can improve body weight, but not BMI, LBM, fat mass, or body fat in cancer patients; large-scale randomized trials needed for more reliable results.

키워드

과제정보

The funding for this study was provided by a grant from Tehran University of Medical Sciences, Tehran, Iran (registration number: 65329).

참고문헌

  1. Arends J, Baracos V, Bertz H, Bozzetti F, Calder PC, et al. ESPEN expert group recommendations for action against cancer-related malnutrition. Clin Nutr 2017;36:1187-96. https://doi.org/10.1016/j.clnu.2017.06.017
  2. Wang Y, Zhang T, Liu R, Chang M, Wei W, et al. New perspective toward nutritional support for malnourished cancer patients: role of lipids. Compr Rev Food Sci Food Saf 2021;20:1381-421. https://doi.org/10.1111/1541-4337.12706
  3. Tsai S. Importance of lean body mass in the oncologic patient. Nutr Clin Pract 2012;27:593-8. https://doi.org/10.1177/0884533612457949
  4. Arends J, Bachmann P, Baracos V, Barthelemy N, Bertz H, et al. ESPEN guidelines on nutrition in cancer patients. Clin Nutr 2017;36:11-48. https://doi.org/10.1016/j.clnu.2016.07.015
  5. Dewey A, Baughan C, Dean T, Higgins B, Johnson I. Eicosapentaenoic acid (EPA, an omega-3 fatty acid from fish oils) for the treatment of cancer cachexia. Cochrane Database Syst Rev 2007;2007:CD004597.
  6. Freitas RDS, Campos MM. Protective effects of omega-3 fatty acids in cancer-related complications. Nutrients 2019;11:945.
  7. Huang YH, Chiu WC, Hsu YP, Lo YL, Wang YH. Effects of omega-3 fatty acids on muscle mass, muscle strength and muscle performance among the elderly: a meta-analysis. Nutrients 2020;12:3739.
  8. Werner K, Kullenberg de Gaudry D, Taylor LA, Keck T, Unger C, et al. Dietary supplementation with n-3-fatty acids in patients with pancreatic cancer and cachexia: marine phospholipids versus fish oil - a randomized controlled double-blind trial. Lipids Health Dis 2017;16:104.
  9. Gorjao R, Dos Santos CMM, Serdan TDA, Diniz VLS, Alba-Loureiro TC, et al. New insights on the regulation of cancer cachexia by N-3 polyunsaturated fatty acids. Pharmacol Ther 2019;196:117-34. https://doi.org/10.1016/j.pharmthera.2018.12.001
  10. Cheng M, Zhang S, Ning C, Huo Q. Omega-3 fatty acids supplementation improve nutritional status and inflammatory response in patients with lung cancer: a randomized clinical trial. Front Nutr 2021;8:686752.
  11. Higgins JPT, Thomas J, Chandler J, Cumpston M, Li T, et al. Cochrane handbook for systematic reviews of interventions. Hoboken: John Wiley & Sons; 2019. 
  12. Crippa A, Orsini N. Dose-response meta-analysis of differences in means. BMC Med Res Methodol 2016;16:91.
  13. Guyatt G, Oxman AD, Akl EA, Kunz R, Vist G, et al. GRADE guidelines: 1. Introduction-GRADE evidence profiles and summary of findings tables. J Clin Epidemiol 2011;64:383-94. https://doi.org/10.1016/j.jclinepi.2010.04.026
  14. Akita H, Takahashi H, Asukai K, Tomokuni A, Wada H, et al. The utility of nutritional supportive care with an eicosapentaenoic acid (EPA)-enriched nutrition agent during pre-operative chemoradiotherapy for pancreatic cancer: prospective randomized control study. Clin Nutr ESPEN 2019;33:148-53. https://doi.org/10.1016/j.clnesp.2019.06.003
  15. Aoyama T, Yoshikawa T, Ida S, Cho H, Sakamaki K, 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.  https://doi.org/10.7150/jca.29632
  16. Aredes MA, da Camara AO, de Paula NS, Fraga KYD, do Carmo MDGT, et al. Efficacy of ω-3 supplementation on nutritional status, skeletal muscle, and chemoradiotherapy toxicity in cervical cancer patients: a randomized, triple-blind, clinical trial conducted in a middle-income country. Nutrition 2019;67-68:110528.
  17. Bauer J, Capra S, Battistutta D, Davidson W, Ash S, et al. Compliance with nutrition prescription improves outcomes in patients with unresectable pancreatic cancer. Clin Nutr 2005;24:998-1004. https://doi.org/10.1016/j.clnu.2005.07.002
  18. Bonatto SJ, Oliveira HH, Nunes EA, Pequito D, Iagher F, et al. Fish oil supplementation improves neutrophil function during cancer chemotherapy. Lipids 2012;47:383-9. https://doi.org/10.1007/s11745-011-3643-0
  19. Bruera E, Strasser F, Palmer JL, Willey J, Calder K, 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. https://doi.org/10.1200/JCO.2003.01.101
  20. Cereda E, Cappello S, Colombo S, Klersy C, Imarisio I, et al. Nutritional counseling with or without systematic use of oral nutritional supplements in head and neck cancer patients undergoing radiotherapy. Radiother Oncol 2018;126:81-8. https://doi.org/10.1016/j.radonc.2017.10.015
  21. Chagas TR, Borges DS, de Oliveira PF, Mocellin MC, Barbosa AM, et al. Oral fish oil positively influences nutritional-inflammatory risk in patients with haematological malignancies during chemotherapy with an impact on long-term survival: a randomised clinical trial. J Hum Nutr Diet 2017;30:681-92. https://doi.org/10.1111/jhn.12471
  22. de la Rosa Oliva F, Meneses Garcia A, Ruiz Calzada H, Astudillo de la Vega H, Bargallo Rocha E, et al. Effects of omega-3 fatty acids supplementation on neoadjuvant chemotherapy-induced toxicity in patients with locally advanced breast cancer: a randomized, controlled, double-blinded clinical trial. Nutr Hosp 2019;36:769-76.
  23. Faber J, Uitdehaag MJ, Spaander M, van Steenbergen-Langeveld S, Vos P, et al. Improved body weight and performance status and reduced serum PGE2 levels after nutritional intervention with a specific medical food in newly diagnosed patients with esophageal cancer or adenocarcinoma of the gastro-esophageal junction. J Cachexia Sarcopenia Muscle 2015;6:32-44. https://doi.org/10.1002/jcsm.12009
  24. Fearon KCH, Von Meyenfeldt MF, Moses AGW, Van Geenen R, Roy A, 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. https://doi.org/10.1136/gut.52.10.1479
  25. Fietkau R, Lewitzki V, Kuhnt T, Holscher T, Hess CF, et al. A disease-specific enteral nutrition formula improves nutritional status and functional performance in patients with head and neck and esophageal cancer undergoing chemoradiotherapy: results of a randomized, controlled, multicenter trial. Cancer 2013;119:3343-53. https://doi.org/10.1002/cncr.28197
  26. Finocchiaro C, Segre O, Fadda M, Monge T, Scigliano M, et al. Effect of n-3 fatty acids on patients with advanced lung cancer: a double-blind, placebo-controlled study. Br J Nutr 2012;108:327-33. https://doi.org/10.1017/S0007114511005551
  27. Haidari F, Abiri B, Iravani M, Ahmadi-Angali K, Vafa M. Randomized study of the effect of vitamin D and omega-3 fatty acids cosupplementation as adjuvant chemotherapy on inflammation and nutritional status in colorectal cancer patients. J Diet Suppl 2020;17:384-400. https://doi.org/10.1080/19390211.2019.1600096
  28. Hanai N, Terada H, Hirakawa H, Suzuki H, Nishikawa D, et al. Prospective randomized investigation implementing immunonutritional therapy using a nutritional supplement with a high blend ratio of ω-3 fatty acids during the perioperative period for head and neck carcinomas. Jpn J Clin Oncol 2018;48:356-61. https://doi.org/10.1093/jjco/hyy008
  29. Healy LA, Ryan A, Doyle SL, Ni Bhuachalla EB, Cushen S, 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. https://doi.org/10.1097/SLA.0000000000002390
  30. Ida S, Hiki N, Cho H, Sakamaki K, Ito S, 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. https://doi.org/10.1002/bjs.10417
  31. Jantharapattana K, Orapipatpong O. Efficacy of EPA-enriched supplement compared with standard formula on body weight changes in malnourished patients with head and neck cancer undergone surgery: a randomized study. Head Neck 2020;42:188-97. https://doi.org/10.1002/hed.25987
  32. Kanat O, Cubukcu E, Avci N, Budak F, Ercan I, et al. Comparison of three different treatment modalities in the management of cancer cachexia. Tumori 2013;99:229-33. https://doi.org/10.1177/030089161309900218
  33. Laviano A, Calder PC, Schols AM, Lonnqvist F, Bech M, et al. Safety and tolerability of targeted medical nutrition for cachexia in non-small-cell lung cancer: a randomized, double-blind, controlled pilot trial. Nutr Cancer 2020;72:439-50.  https://doi.org/10.1080/01635581.2019.1634746
  34. Mantovani G, Maccio A, Madeddu C, Serpe R, Massa E, et al. Randomized phase III clinical trial of five different arms of treatment in 332 patients with cancer cachexia. Oncologist 2010;15:200-11. https://doi.org/10.1634/theoncologist.2009-0153
  35. Matsuda Y, Habu D, Lee S, Kishida S, Osugi H. Enteral diet enriched with ω-3 fatty acid improves oxygenation after thoracic esophagectomy for cancer: a randomized controlled trial. World J Surg 2017;41:1584-94. https://doi.org/10.1007/s00268-017-3893-y
  36. Mocellin MC, de Quadros Camargo C, de Souza Fabre ME, de Moraes Trindade EB. Fish oil effects on quality of life, body weight and free fat mass change in gastrointestinal cancer patients undergoing chemotherapy: a triple blind, randomized clinical trial. J Funct Foods 2017;31:113-22. https://doi.org/10.1016/j.jff.2017.01.041
  37. Mocellin MC, Pastore e Silva Jde A, Camargo Cde Q, Fabre ME, Gevaerd S, 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. https://doi.org/10.1007/s11745-013-3816-0
  38. Moses AW, Slater C, Preston T, Barber MD, Fearon KC. Reduced total energy expenditure and physical activity in cachectic patients with pancreatic cancer can be modulated by an energy and protein dense oral supplement enriched with n-3 fatty acids. Br J Cancer 2004;90:996-1002. https://doi.org/10.1038/sj.bjc.6601620
  39. Paixao EMDS, Oliveira ACM, Pizato N, Muniz-Junqueira MI, Magalhaes KG, et al. The effects of EPA and DHA enriched fish oil on nutritional and immunological markers of treatment naive breast cancer patients: a randomized double-blind controlled trial. Nutr J 2017;16:71.
  40. Roca-Rodriguez MM, Garcia-Almeida JM, Lupianez-Perez Y, Rico JM, Toledo M, et al. Effect of a specific supplement enriched with n-3 polyunsaturated fatty acids on markers of inflammation, oxidative stress and metabolic status of ear, nose and throat cancer patients. Oncol Rep 2014;31:405-14. https://doi.org/10.3892/or.2013.2806
  41. Sanchez-Lara K, Turcott JG, Juarez-Hernandez E, Nunez-Valencia C, Villanueva G, et al. Effects of an oral nutritional supplement containing eicosapentaenoic acid on nutritional and clinical outcomes in patients with advanced non-small cell lung cancer: randomised trial. Clin Nutr 2014;33:1017-23. https://doi.org/10.1016/j.clnu.2014.03.006
  42. Silva Jde A, Trindade EB, Fabre ME, Menegotto VM, Gevaerd S, et al. Fish oil supplement alters markers of inflammatory and nutritional status in colorectal cancer patients. Nutr Cancer 2012;64:267-73. https://doi.org/10.1080/01635581.2012.643133
  43. Solis-Martinez O, Plasa-Carvalho V, Phillips-Sixtos G, Trujillo-Cabrera Y, Hernandez-Cuellar A, et al. Effect of eicosapentaenoic acid on body composition and inflammation markers in patients with head and neck squamous cell cancer from a public hospital in Mexico. Nutr Cancer 2018;70:663-70. https://doi.org/10.1080/01635581.2018.1460678
  44. Suzumura DN, Schleder JC, Appel MH, Naliwaiko K, Tanhoffer R, et al. Fish oil supplementation enhances pulmonary strength and endurance in women undergoing chemotherapy. Nutr Cancer 2016;68:935-42. https://doi.org/10.1080/01635581.2016.1187282
  45. Wigmore SJ, Ross JA, Falconer JS, Plester CE, Tisdale MJ, et al. The effect of polyunsaturated fatty acids on the progress of cachexia in patients with pancreatic cancer. Nutrition 1996;12:S27-30. https://doi.org/10.1016/0899-9007(95)00078-X
  46. Gui L, Cheng M, Zheng M, Ning C, Huo Q. Effects of omega-3 fatty acid supplementation on nutritional status and inflammatory response in patients with stage II-III NSCLC undergoing postoperative chemotherapy: a double-blind randomized controlled trial. Front Nutr 2023;10:1266584.
  47. Lam CN, Watt AE, Isenring EA, de van der Schueren MA, van der Meij BS. The effect of oral omega-3 polyunsaturated fatty acid supplementation on muscle maintenance and quality of life in patients with cancer: a systematic review and meta-analysis. Clin Nutr 2021;40:3815-26. https://doi.org/10.1016/j.clnu.2021.04.031
  48. Delpino FM, Figueiredo LM. Effects of omega-3 supplementation on lean body mass in cancer patients: a systematic review and meta-analysis. Eur J Clin Nutr 2022;76:1636-45. https://doi.org/10.1038/s41430-022-01100-x
  49. Ma YJ, Yu J, Xiao J, Cao BW. The consumption of omega-3 polyunsaturated fatty acids improves clinical outcomes and prognosis in pancreatic cancer patients: a systematic evaluation. Nutr Cancer 2015;67:112-8. https://doi.org/10.1080/01635581.2015.976315