Clinical Nutrition Research

The Korean Society of Clinical Nutrition (한국임상영양학회)
권호 표지
DOI QR코드

DOI QR Code

Effects of Soy Bread on Cardiovascular Risk Factor, Inflammation and Oxidative Stress in Women With Active Rheumatoid Arthritis: A Randomized Double-Blind Controlled Trial

  • Afsaneh Sayyaf (Department of Nutritional Sciences, Faculty of Paramedical, Ahvaz Jundishapur University of Medical Sciences) ;
  • Ehsan Ghaedi (Department of Cellular and Molecular Nutrition, School of Nutritional Sciences and Dietetics, Tehran University of Medical Sciences) ;
  • Fatemeh Haidari (Department of Nutrition, Nutrition and Metabolic Diseases Research Center, Ahvaz Jundishapur University of Medical Sciences) ;
  • Elham Rajaei (Golestan Hospital Clinical Research Development Unit, Ahvaz Jundishapur University of Medical Sciences) ;
  • Kambiz Ahmadi-engali (Faculty of Public Health, Ahvaz Jundishapur University of Medical Sciences) ;
  • Bijan Helli (Nutrition and Metabolic Diseases Research Center, Department of Nutrition Sciences, School of Paramedical Sciences, Ahvaz Jundishapur University of Medical Sciences)
  • Received : 2023.08.04
  • Accepted : 2024.01.07
  • Published : 2024.01.31
Download PDF
⟨ Previous Next ⟩

Abstract

Rheumatoid arthritis (RA) is a systemic inflammatory autoimmune disorder with widespread synovitis. Isoflavones, the main active component of soy, have been reported to have potent anti-inflammatory effects; the previous RA animal models showed the promising effect of soy supplementation. We aimed to evaluate the effect of soy bread on inflammatory markers and lipid profiles in RA patients. The present study was designed as a randomized controlled trial. RA patients were randomly allocated to obtain soy bread (n = 22) or placebo bread (n = 22) for 8 weeks. Fasting serum levels of lipid profile, total antioxidant capacity (TAC), tumor necrosis factor-α (TNF-α), C-reactive protein (CRP), and DAS28 were checked. Findings showed that there were no significant differences between the two groups in physical activity and dietary intake at the beginning of the study and the end of the study. There were no significant differences between the two groups in measured lipid profile markers, including high-density lipoprotein, low-density lipoprotein, total cholesterol, triglyceride, and very low-density lipoprotein, at the end of the trial. In addition, TAC and CRP also were not significant at the end of the trial between the 2 groups (0.66 and 0.12, respectively). However, the serum levels of TNF-α reduced significantly in the soy bread group at the end of the intervention (p < 0.000) and compared with the control group (p < 0.019). Soy bread consumption only decreased circulating TNF-α serum concentration. Other outcome measures were not changed following supplementation. Future long-term, well-designed studies are needed to confirm these findings.

Keywords

References

  1. Kumar LD, Karthik R, Gayathri N, Sivasudha T. Advancement in contemporary diagnostic and therapeutic approaches for rheumatoid arthritis. Biomed Pharmacother 2016;79:52-61.
  2. Shrivastava AK, Pandey A. Inflammation and rheumatoid arthritis. J Physiol Biochem 2013;69:335-47.
  3. Majithia V, Geraci SA. Rheumatoid arthritis: diagnosis and management. Am J Med 2007;120:936-9.
  4. Chimenti MS, Triggianese P, Conigliaro P, Candi E, Melino G, Perricone R. The interplay between inflammation and metabolism in rheumatoid arthritis. Cell Death Dis 2015;6:e1887.
  5. Joshi P, Kabra P, Jha RK. Romatoid artritli hastalarda dislipidemi paterni ve hastalik aktivitesi ile iliskisi. Cagdas Tip Dergisi 2017;7:132-7.
  6. Mohammad Shahi M, Rashidi MR, Mahboob S, Haidari F, Rashidi B, Hanaee J. Protective effect of soy protein on collagen-induced arthritis in rat. Rheumatol Int 2012;32:2407-14.
  7. Ameri AH, Moradi Tuchayi S, Zaalberg A, Park JH, Ngo KH, Li T, Lopez E, Colonna M, Lee RT, Mino-Kenudson M, Demehri S. IL-33/regulatory T cell axis triggers the development of a tumor-promoting immune environment in chronic inflammation. Proc Natl Acad Sci U S A 2019;116:2646-51.
  8. McInnes IB, Schett G. The pathogenesis of rheumatoid arthritis. N Engl J Med 2011;365:2205-19.
  9. Rieckmann P, Tuscano JM, Kehrl JH. Tumor necrosis factor-α (TNF-α) and interleukin-6 (IL-6) in B-lymphocyte function. Methods 1997;11:128-32.
  10. Kurien BT, Scofield RH. Autoimmunity and oxidatively modified autoantigens. Autoimmun Rev 2008;7:567-73.
  11. Chandrashekara S. Complementary and alternative medicine in rheumatoid arthritis. Chin J Integr Med 2011;17:731-4.
  12. Juthani VV, Clearfield E, Chuck RS. Non-steroidal anti-inflammatory drugs versus corticosteroids for controlling inflammation after uncomplicated cataract surgery. Cochrane Database Syst Rev 2017;7:CD010516.
  13. Suchdev PS, Namaste SM, Aaron GJ, Raiten DJ, Brown KH, Flores-Ayala R; BRINDA Working Group. Overview of the biomarkers reflecting inflammation and nutritional determinants of anemia (BRINDA) project. Adv Nutr 2016;7:349-56.
  14. Gonzalez-Montoya M, Hernandez-Ledesma B, Silvan JM, Mora-Escobedo R, Martinez-Villaluenga C. Peptides derived from in vitro gastrointestinal digestion of germinated soybean proteins inhibit human colon cancer cells proliferation and inflammation. Food Chem 2018;242:75-82.
  15. Peng Y, Shi Y, Zhang H, Mine Y, Tsao R. Anti-inflammatory and anti-oxidative activities of daidzein and its sulfonic acid ester derivatives. J Funct Foods 2017;35:635-40.
  16. Meng H, Fu G, Shen J, Shen K, Xu Z, Wang Y, Jin B, Pan H. Ameliorative effect of daidzein on cisplatin-induced nephrotoxicity in mice via modulation of inflammation, oxidative stress, and cell death. Oxid Med Cell Longev 2017;2017:3140680.
  17. Holmdahl R, Sareila O, Olsson LM, Backdahl L, Wing K. Ncf1 polymorphism reveals oxidative regulation of autoimmune chronic inflammation. Immunol Rev 2016;269:228-47.
  18. Ahmad S, Alam K, Hossain MM, Fatima M, Firdaus F, Zafeer MF, Arif Z, Ahmed M, Nafees KA. Anti-arthritogenic and cardioprotective action of hesperidin and daidzein in collagen-induced rheumatoid arthritis. Mol Cell Biochem 2016;423:115-27.
  19. Yang M, Luo Y, Liu T, Zhong X, Yan J, Huang Q, Tao J, He Q, Guo M, Hu Y. The effect of puerarin on carotid intima-media thickness in patients with active rheumatoid arthritis: a randomized controlled trial. Clin Ther 2018;40:1752-1764.e1.
  20. Wang J, Zhang Q, Jin S, He D, Zhao S, Liu S. Genistein modulate immune responses in collagen-induced rheumatoid arthritis model. Maturitas 2008;59:405-12.
  21. Zhang Y, Dong J, He P, Li W, Zhang Q, Li N, Sun T. Genistein inhibit cytokines or growth factor-induced proliferation and transformation phenotype in fibroblast-like synoviocytes of rheumatoid arthritis. Inflammation 2012;35:377-87.
  22. Li J, Gang D, Yu X, Hu Y, Yue Y, Cheng W, Pan X, Zhang P. Genistein: the potential for efficacy in rheumatoid arthritis. Clin Rheumatol 2013;32:535-40.
  23. Hu Y, Li J, Qin L, Cheng W, Lai Y, Yue Y, Ren P, Pan X, Zhang P. Study in treatment of collagen-induced arthritis in DBA/1 mice model by genistein. Curr Pharm Des 2016;22:6975-81.
  24. Jia S, Zhang S, Yuan H, Chen N. Lunasin inhibits cell proliferation via apoptosis and reduces the production of proinflammatory cytokines in cultured rheumatoid arthritis synovial fibroblasts. BioMed Res Int 2015;2015:346839.
  25. Mohammadshahi M, Haidari F, Saei AA, Rashidi B, Mahboob S, Rashidi MR. Soy protein, genistein, and daidzein improve serum paraoxonase activity and lipid profiles in rheumatoid arthritis in rats. J Med Food 2013;16:147-54.
  26. Reinwald S, Akabas SR, Weaver CM. Whole versus the piecemeal approach to evaluating soy. J Nutr 2010;140:2335S-43S.
  27. Steinberg FM. Soybeans or soymilk: does it make a difference for cardiovascular protection? Does it even matter? Am J Clin Nutr 2007;85:927-8.
  28. Mohammad-Shahi M, Mowla K, Haidari F, Zarei M, Choghakhori R. Soy milk consumption, markers of inflammation and oxidative stress in women with rheumatoid arthritis: a randomised cross-over clinical trial. Nutr Diet 2016;73:139-45.
  29. IPAQ Research Committee. Guidelines for data processing and analysis of the International Physical Activity Questionnaire (IPAQ) - short and long forms. IPAQ Research Committee; 2005.
  30. Azadbakht L, Esmaillzadeh A. A cross-over trial on soy intake and serum leptin levels in women with metabolic syndrome. J Res Med Sci 2010;15:317-23.
  31. Salari Moghaddam A, Entezari MH, Iraj B, Askari G, Sharifi Zahabi E, Maracy MR. The effects of soy bean flour enriched bread intake on anthropometric indices and blood pressure in type 2 diabetic women: a crossover randomized controlled clinical trial. Int J Endocrinol 2014;2014:240760.
  32. Sharifi-Zahabi E, Entezari MH, Maracy MR. Effects of soy flour fortified bread consumption on cardiovascular risk factors according to APOE genotypes in overweight and obese adult women: a cross-over randomized controlled clinical trial. Clin Nutr Res 2015;4:225-34.
  33. Lesinski GB, Reville PK, Mace TA, Young GS, Ahn-Jarvis J, Thomas-Ahner J, Vodovotz Y, Ameen Z, Grainger E, Riedl K, Schwartz S, Clinton SK. Consumption of soy isoflavone enriched bread in men with prostate cancer is associated with reduced proinflammatory cytokines and immunosuppressive cells. Cancer Prev Res (Phila) 2015;8:1036-44.
  34. Ahn-Jarvis JH, Clinton SK, Grainger EM, Riedl KM, Schwartz SJ, Lee ML, Cruz-Cano R, Young GS, Lesinski GB, Vodovotz Y. Isoflavone pharmacokinetics and metabolism after consumption of a standardized soy and soy-almond bread in men with asymptomatic prostate cancer. Cancer Prev Res (Phila) 2015;8:1045-54.
  35. Ahmad S, Alam K, Hossain MM, Fatima M, Firdaus F, Zafeer MF, Arif Z, Ahmed M, Nafees KA. Anti-arthritogenic and cardioprotective action of hesperidin and daidzein in collagen-induced rheumatoid arthritis. Mol Cell Biochem 2016;423:115-27.
  36. Lin IC, Yamashita S, Murata M, Kumazoe M, Tachibana H. Equol suppresses inflammatory response and bone erosion due to rheumatoid arthritis in mice. J Nutr Biochem 2016;32:101-6.
  37. Xiao C, Li J, Dong X, He X, Niu X, Liu C, Zhong G, Bauer R, Yang D, Lu A. Anti-oxidative and TNF-α suppressive activities of puerarin derivative (4AC) in RAW264.7 cells and collagen-induced arthritic rats. Eur J Pharmacol 2011;666:242-50.
  38. Min HK, Kim SM, Baek SY, Woo JW, Park JS, Cho ML, Lee J, Kwok SK, Kim SW, Park SH. Anthocyanin extracted from black soybean seed coats prevents autoimmune arthritis by suppressing the development of Th17 cells and synthesis of proinflammatory cytokines by such cells, via inhibition of NF-κB. PLoS One 2015;10:e0138201.
  39. Liu ZM, Ho SC, Chen YM, Ho S, To K, Tomlinson B, Woo J. Whole soy, but not purified daidzein, had a favorable effect on improvement of cardiovascular risks: a 6-month randomized, double-blind, and placebo-controlled trial in equol-producing postmenopausal women. Mol Nutr Food Res 2014;58:709-17.
  40. Jalili M, Vahedi H, Poustchi H, Hekmatdoost A. Soy isoflavones and cholecalciferol reduce inflammation, and gut permeability, without any effect on antioxidant capacity in irritable bowel syndrome: a randomized clinical trial. Clin Nutr ESPEN 2019;34:50-4.
  41. Hematdar Z, Ghasemifard N, Phishdad G, Faghih S. Substitution of red meat with soybean but not non- soy legumes improves inflammation in patients with type 2 diabetes; a randomized clinical trial. J Diabetes Metab Disord 2018;17:111-6.
  42. Azadbakht L, Kimiagar M, Mehrabi Y, Zadeh AE. To determine the effects of soy consumption on markers of inflammation and endothelial function in postmenopausal women with the metabolic syndrome. Iran J Diabetes Lipid Disord 2007;6:81-92.
  43. Smith LJ, Kalhan R, Wise RA, Sugar EA, Lima JJ, Irvin CG, Dozor AJ, Holbrook JT; American Lung Association Asthma Clinical Research Centers. Effect of a soy isoflavone supplement on lung function and clinical outcomes in patients with poorly controlled asthma: a randomized clinical trial. JAMA 2015;313:2033-43.
  44. Reverri EJ, LaSalle CD, Franke AA, Steinberg FM. Soy provides modest benefits on endothelial function without affecting inflammatory biomarkers in adults at cardiometabolic risk. Mol Nutr Food Res 2015;59:323-33.
  45. Nadadur M, Stanczyk FZ, Tseng CC, Kim L, Wu AH. The effect of reduced dietary fat and soy supplementation on circulating adipocytokines in postmenopausal women: a randomized controlled 2-month trial. Nutr Cancer 2016;68:554-9.
  46. Liu ZM, Ho SC, Chen YM, Ho YP. The effects of isoflavones combined with soy protein on lipid profiles, C-reactive protein and cardiovascular risk among postmenopausal Chinese women. Nutr Metab Cardiovasc Dis 2012;22:712-9.
  47. Jenkins DJ, Kendall CW, Connelly PW, Jackson CJ, Parker T, Faulkner D, Vidgen E. Effects of high- and low-isoflavone (phytoestrogen) soy foods on inflammatory biomarkers and proinflammatory cytokines in middle-aged men and women. Metabolism 2002;51:919-24.
  48. Beavers KM, Serra MC, Beavers DP, Cooke MB, Willoughby DS. Soymilk supplementation does not alter plasma markers of inflammation and oxidative stress in postmenopausal women. Nutr Res 2009;29:616-22.
  49. Khodarahmi M, Jafarabadi MA, Moludi J, Abbasalizad Farhangi M. A systematic review and meta-analysis of the effects of soy on serum hs-CRP. Clin Nutr 2019;38:996-1011.
  50. Dong JY, Wang P, He K, Qin LQ. Effect of soy isoflavones on circulating C-reactive protein in postmenopausal women: meta-analysis of randomized controlled trials. Menopause 2011;18:1256-62.
  51. Llaneza P, Gonzalez C, Fernandez-Inarrea J, Alonso A, Diaz F, Arnott I, Ferrer-Barriendos J. Soy isoflavones, diet and physical exercise modify serum cytokines in healthy obese postmenopausal women. Phytomedicine 2011;18:245-50.
  52. Eo H, Ann J, Lim Y. Dietary supplementation of genistein attenuates inflammatory responses and oxidative stress during cutaneous wound healing in diabetic mice. J Agric Sci 2015;7:80-92.
  53. Dower JI, Geleijnse JM, Gijsbers L, Schalkwijk C, Kromhout D, Hollman PC. Supplementation of the pure flavonoids epicatechin and quercetin affects some biomarkers of endothelial dysfunction and inflammation in (pre)hypertensive adults: a randomized double-blind, placebo-controlled, crossover trial. J Nutr 2015;145:1459-63.
  54. Blay M, Espinel AE, Delgado MA, Baiges I, Blade C, Arola L, Salvado J. Isoflavone effect on gene expression profile and biomarkers of inflammation. J Pharm Biomed Anal 2010;51:382-90.
  55. Yu J, Bi X, Yu B, Chen D. Isoflavones: anti-inflammatory benefit and possible caveats. Nutrients 2016;8:361.
  56. Levy-Ontman O, Huleihel M, Hamias R, Wolak T, Paran E. An anti-inflammatory effect of red microalga polysaccharides in coronary artery endothelial cells. Atherosclerosis 2017;264:11-8.
  57. Cutolo M, Brizzolara R, Atzeni F, Capellino S, Straub RH, Puttini PC. The immunomodulatory effects of estrogens: clinical relevance in immune-mediated rheumatic diseases. Ann N Y Acad Sci 2010;1193:36-42.
  58. Cooke PS, Selvaraj V, Yellayi S. Genistein, estrogen receptors, and the acquired immune response. J Nutr 2006;136:704-8.
  59. Erum U, Ahsan T, Khowaja D. Lipid abnormalities in patients with rheumatoid arthritis. Pak J Med Sci 2017;33:227-30.
  60. Tokede OA, Onabanjo TA, Yansane A, Gaziano JM, Djousse L. Soya products and serum lipids: a meta-analysis of randomised controlled trials. Br J Nutr 2015;114:831-43.
  61. Jargin SV. Soy and phytoestrogens: possible side effects. Ger Med Sci 2014;12:Doc18.
  62. Van Patten CL, Olivotto IA, Chambers GK, Gelmon KA, Hislop TG, Templeton E, Wattie A, Prior JC. Effect of soy phytoestrogens on hot flashes in postmenopausal women with breast cancer: a randomized, controlled clinical trial. J Clin Oncol 2002;20:1449-55.