Skip to main content
Top
Published in: Supportive Care in Cancer 7/2021

01-07-2021 | Breast Cancer | Original Article

Effects of synbiotic supplementation on serum adiponectin and inflammation status of overweight and obese breast cancer survivors: a randomized, triple-blind, placebo-controlled trial

Authors: Mahsa Raji Lahiji, Mitra Zarrati, Safa Najafi, Bahareh Yazdani, Elhameh Cheshmazar, Elham Razmpoosh, Leila Janani, Mahtab Raji Lahiji, Farzad Shidfar

Published in: Supportive Care in Cancer | Issue 7/2021

Login to get access

Abstract

Purpose

Adipokines and inflammatory factors can affect breast cancer (BC) prognosis and recurrence among breast cancer survivors (BCSs). This study was to evaluate the effects of synbiotic supplementation along with a low-calorie diet on some recurrence-related factors such as adiponectin, tumor necrosis factor-alpha (TNF-α), and high-sensitivity C-reactive protein (hs-CRP) among obese and overweight BCSs.

Methods

We performed a randomized, triple-blind, placebo-controlled clinical trial among 76 overweight or obese postmenopausal women with a history of hormone-receptor-positive BC. Participants were randomly divided into 2 groups to intake either 109 CFU/day synbiotic supplement or placebo (n = 38 each group) for 8 weeks. All participants were given a low-calorie diet program. The primary outcome was serum concentration of adiponectin which was measured at baseline and after 8 weeks.

Results

Compared with the placebo, synbiotic intake significantly increased adiponectin (+ 13.58 (10.08, 18.17) vs. − 0.42 (− 2.90, 1.98) μg/ml; P < 0.001). In addition, synbiotic supplementation resulted in significant reduction in TNF-α levels (− 17.09 (− 32.05, − 13.60) vs. 0.20 (− 3.97, 2.00) ng/L; P < 0.001) and hs-CRP levels (− 1.14 (− 1.90, − 0.88 vs. − 0.06 (− 0.38, 0.15) mg/L; P < 0.001) compared with the placebo.

Conclusions

In conclusion, 8-week synbiotic consumption by overweight and obese postmenopausal BCSs had beneficial effects on adiponectin, TNF-α, and hs-CRP.

Trial registration

IRCT, IRCT20091114002709N49. Registered 18 May 2018, http://​www.​irct.​ir: IRCT20091114002709N49
Literature
1.
go back to reference Society AC (2018) American Cancer Society Facts & Figures 2019 Society AC (2018) American Cancer Society Facts & Figures 2019
2.
go back to reference Mayne ST, Playdon MC, Rock CL (2016) Diet, nutrition, and cancer: past, present and future. Nat Rev Clin Oncol 13(8):504–515CrossRef Mayne ST, Playdon MC, Rock CL (2016) Diet, nutrition, and cancer: past, present and future. Nat Rev Clin Oncol 13(8):504–515CrossRef
3.
go back to reference Miyoshi Y, Funahashi T, Kihara S, Taguchi T, Tamaki Y, Matsuzawa Y, Noguchi S (2003) Association of serum adiponectin levels with breast cancer risk. Clin Cancer Res 9(15):5699–5704PubMed Miyoshi Y, Funahashi T, Kihara S, Taguchi T, Tamaki Y, Matsuzawa Y, Noguchi S (2003) Association of serum adiponectin levels with breast cancer risk. Clin Cancer Res 9(15):5699–5704PubMed
4.
go back to reference Oh SW, Park C-Y, Lee ES, Yoon YS, Lee ES, Park SS, Kim Y, Sung NJ, Yun YH, Lee KS (2011) Adipokines, insulin resistance, metabolic syndrome, and breast cancer recurrence: a cohort study. Breast Cancer Res 13(2):R34CrossRef Oh SW, Park C-Y, Lee ES, Yoon YS, Lee ES, Park SS, Kim Y, Sung NJ, Yun YH, Lee KS (2011) Adipokines, insulin resistance, metabolic syndrome, and breast cancer recurrence: a cohort study. Breast Cancer Res 13(2):R34CrossRef
5.
go back to reference Cai X, Cao C, Li J, Chen F, Zhang S, Liu B, Zhang W, Zhang X, Ye L (2017) Inflammatory factor TNF-α promotes the growth of breast cancer via the positive feedback loop of TNFR1/NF-κB (and/or p38)/p-STAT3/HBXIP/TNFR1. Oncotarget 8(35):58338–58352CrossRef Cai X, Cao C, Li J, Chen F, Zhang S, Liu B, Zhang W, Zhang X, Ye L (2017) Inflammatory factor TNF-α promotes the growth of breast cancer via the positive feedback loop of TNFR1/NF-κB (and/or p38)/p-STAT3/HBXIP/TNFR1. Oncotarget 8(35):58338–58352CrossRef
6.
go back to reference Ji H, Cao R, Yang Y, Zhang Y, Iwamoto H, Lim S, Nakamura M, Andersson P, Wang J, Sun Y (2014) TNFR1 mediates TNF-α-induced tumour lymphangiogenesis and metastasis by modulating VEGF-C-VEGFR3 signalling. Nat Commun 5(1):1–17 Ji H, Cao R, Yang Y, Zhang Y, Iwamoto H, Lim S, Nakamura M, Andersson P, Wang J, Sun Y (2014) TNFR1 mediates TNF-α-induced tumour lymphangiogenesis and metastasis by modulating VEGF-C-VEGFR3 signalling. Nat Commun 5(1):1–17
7.
go back to reference Heikkilä K, Ebrahim S, Lawlor DA (2007) A systematic review of the association between circulating concentrations of C reactive protein and cancer. J Epidemiol Community Health 61(9):824–833CrossRef Heikkilä K, Ebrahim S, Lawlor DA (2007) A systematic review of the association between circulating concentrations of C reactive protein and cancer. J Epidemiol Community Health 61(9):824–833CrossRef
8.
go back to reference Lee S, Choe J-W, Kim H-K, Sung J (2011) High-sensitivity C-reactive protein and cancer. J Epidemiol:1102220216-1102220216 Lee S, Choe J-W, Kim H-K, Sung J (2011) High-sensitivity C-reactive protein and cancer. J Epidemiol:1102220216-1102220216
9.
go back to reference Nagpal R, Kumar A, Kumar M, Behare PV, Jain S, Yadav H (2012) Probiotics, their health benefits and applications for developing healthier foods: a review. FEMS Microbiol Lett 334(1):1–15CrossRef Nagpal R, Kumar A, Kumar M, Behare PV, Jain S, Yadav H (2012) Probiotics, their health benefits and applications for developing healthier foods: a review. FEMS Microbiol Lett 334(1):1–15CrossRef
10.
go back to reference Schrezenmeir J, de Vrese M (2001) Probiotics, prebiotics, and synbiotics—approaching a definition. Am J Clin Nutr 73(2):361s–364sCrossRef Schrezenmeir J, de Vrese M (2001) Probiotics, prebiotics, and synbiotics—approaching a definition. Am J Clin Nutr 73(2):361s–364sCrossRef
11.
go back to reference Gibson GR, Hutkins R, Sanders ME, Prescott SL, Reimer RA, Salminen SJ, Scott K, Stanton C, Swanson KS, Cani PD (2017) Expert consensus document: The International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nat Rev Gastroenterol Hepatol 14(8):491–502CrossRef Gibson GR, Hutkins R, Sanders ME, Prescott SL, Reimer RA, Salminen SJ, Scott K, Stanton C, Swanson KS, Cani PD (2017) Expert consensus document: The International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nat Rev Gastroenterol Hepatol 14(8):491–502CrossRef
12.
go back to reference Gareau MG, Sherman PM, Walker WA (2010) Probiotics and the gut microbiota in intestinal health and disease. Nat Rev Gastroenterol Hepatol 7(9):503–514CrossRef Gareau MG, Sherman PM, Walker WA (2010) Probiotics and the gut microbiota in intestinal health and disease. Nat Rev Gastroenterol Hepatol 7(9):503–514CrossRef
13.
go back to reference Behrouz V, Jazayeri S, Aryaeian N, Zahedi MJ, Hosseini F (2017) Effects of probiotic and prebiotic supplementation on leptin, adiponectin, and glycemic parameters in non-alcoholic fatty liver disease: a randomized clinical trial. Middle East J Dig Dis 9(3):150–157CrossRef Behrouz V, Jazayeri S, Aryaeian N, Zahedi MJ, Hosseini F (2017) Effects of probiotic and prebiotic supplementation on leptin, adiponectin, and glycemic parameters in non-alcoholic fatty liver disease: a randomized clinical trial. Middle East J Dig Dis 9(3):150–157CrossRef
14.
go back to reference Scott KP, Gratz SW, Sheridan PO, Flint HJ, Duncan SH (2013) The influence of diet on the gut microbiota. Pharmacol Res 69(1):52–60CrossRef Scott KP, Gratz SW, Sheridan PO, Flint HJ, Duncan SH (2013) The influence of diet on the gut microbiota. Pharmacol Res 69(1):52–60CrossRef
15.
go back to reference Ma LX, Bulsara MK, Tan SY, Vardy J (2016) Body weight management in overweight and obese breast cancer survivors. The Cochrane Library Ma LX, Bulsara MK, Tan SY, Vardy J (2016) Body weight management in overweight and obese breast cancer survivors. The Cochrane Library
16.
go back to reference Craig CL, Marshall AL, Sjorstrom M, Bauman AE, Booth ML, Ainsworth BE, Pratt M, Ekelund U, Yngve A, Sallis JF (2003) International physical activity questionnaire: 12-country reliability and validity. Med Sci Sports Exerc 35(8):1381–1395CrossRef Craig CL, Marshall AL, Sjorstrom M, Bauman AE, Booth ML, Ainsworth BE, Pratt M, Ekelund U, Yngve A, Sallis JF (2003) International physical activity questionnaire: 12-country reliability and validity. Med Sci Sports Exerc 35(8):1381–1395CrossRef
17.
go back to reference Duggan C, Irwin ML, Xiao L, Henderson KD, Smith AW, Baumgartner RN, Baumgartner KB, Bernstein L, Ballard-Barbash R, McTiernan A (2011) Associations of insulin resistance and adiponectin with mortality in women with breast cancer. J Clin Oncol 29(1):32–39CrossRef Duggan C, Irwin ML, Xiao L, Henderson KD, Smith AW, Baumgartner RN, Baumgartner KB, Bernstein L, Ballard-Barbash R, McTiernan A (2011) Associations of insulin resistance and adiponectin with mortality in women with breast cancer. J Clin Oncol 29(1):32–39CrossRef
18.
go back to reference Le TKC, Hosaka T, Nguyen TT, Kassu A, Dang TO, Tran HB, Pham TP, Tran QB, Le THH, Da Pham X (2015) Bifidobacterium species lower serum glucose, increase expressions of insulin signaling proteins, and improve adipokine profile in diabetic mice. Biomed Res 36(1):63–70CrossRef Le TKC, Hosaka T, Nguyen TT, Kassu A, Dang TO, Tran HB, Pham TP, Tran QB, Le THH, Da Pham X (2015) Bifidobacterium species lower serum glucose, increase expressions of insulin signaling proteins, and improve adipokine profile in diabetic mice. Biomed Res 36(1):63–70CrossRef
19.
go back to reference Kim S-W, Park K-Y, Kim B, Kim E, Hyun C-K (2013) Lactobacillus rhamnosus GG improves insulin sensitivity and reduces adiposity in high-fat diet-fed mice through enhancement of adiponectin production. Biochem Biophys Res Commun 431(2):258–263CrossRef Kim S-W, Park K-Y, Kim B, Kim E, Hyun C-K (2013) Lactobacillus rhamnosus GG improves insulin sensitivity and reduces adiposity in high-fat diet-fed mice through enhancement of adiponectin production. Biochem Biophys Res Commun 431(2):258–263CrossRef
20.
go back to reference Feizollahzadeh S, Ghiasvand R, Rezaei A, Khanahmad H, Hariri M (2017) Effect of probiotic soy milk on serum levels of adiponectin, inflammatory mediators, lipid profile, and fasting blood glucose among patients with type ii diabetes mellitus. Probiot Antimicrob Proteins 9(1):41–47CrossRef Feizollahzadeh S, Ghiasvand R, Rezaei A, Khanahmad H, Hariri M (2017) Effect of probiotic soy milk on serum levels of adiponectin, inflammatory mediators, lipid profile, and fasting blood glucose among patients with type ii diabetes mellitus. Probiot Antimicrob Proteins 9(1):41–47CrossRef
21.
go back to reference Rouhani MH, Hadi A, Ghaedi E, Salehi M, Mahdavi A, Mohammadi H (2019) Do probiotics, prebiotics and synbiotics affect adiponectin and leptin in adults? A systematic review and meta-analysis of clinical trials. Clin Nutr 38(5):2031–2037CrossRef Rouhani MH, Hadi A, Ghaedi E, Salehi M, Mahdavi A, Mohammadi H (2019) Do probiotics, prebiotics and synbiotics affect adiponectin and leptin in adults? A systematic review and meta-analysis of clinical trials. Clin Nutr 38(5):2031–2037CrossRef
22.
go back to reference Dieudonne M-N, Bussiere M, Dos Santos E, Leneveu M-C, Giudicelli Y, Pecquery R (2006) Adiponectin mediates antiproliferative and apoptotic responses in human MCF7 breast cancer cells. Biochem Biophys Res Commun 345(1):271–279CrossRef Dieudonne M-N, Bussiere M, Dos Santos E, Leneveu M-C, Giudicelli Y, Pecquery R (2006) Adiponectin mediates antiproliferative and apoptotic responses in human MCF7 breast cancer cells. Biochem Biophys Res Commun 345(1):271–279CrossRef
23.
go back to reference Kang JH, Lee YY, Yu BY, Yang B-S, Cho K-H, Yoon DK, Roh YK (2005) Adiponectin induces growth arrest and apoptosis of MDA-MB-231 breast cancer cell. Arch Pharm Res 28(11):1263–1269CrossRef Kang JH, Lee YY, Yu BY, Yang B-S, Cho K-H, Yoon DK, Roh YK (2005) Adiponectin induces growth arrest and apoptosis of MDA-MB-231 breast cancer cell. Arch Pharm Res 28(11):1263–1269CrossRef
24.
go back to reference Barb D, Pazaitou-Panayiotou K, Mantzoros CS (2006) Adiponectin: a link between obesity and cancer. Expert Opin Investig Drugs 15(8):917–931CrossRef Barb D, Pazaitou-Panayiotou K, Mantzoros CS (2006) Adiponectin: a link between obesity and cancer. Expert Opin Investig Drugs 15(8):917–931CrossRef
26.
go back to reference Guo L, Liu S, Zhang S, Chen Q, Zhang M, Quan P, Lu J, Sun X (2015) C-reactive protein and risk of breast cancer: a systematic review and meta-analysis. Sci Rep 5(1):1–8 Guo L, Liu S, Zhang S, Chen Q, Zhang M, Quan P, Lu J, Sun X (2015) C-reactive protein and risk of breast cancer: a systematic review and meta-analysis. Sci Rep 5(1):1–8
27.
go back to reference Tabrizi R, Ostadmohammadi V, Lankarani KB, Akbari M, Akbari H, Vakili S, Shokrpour M, Kolahdooz F, Rouhi V, Asemi Z (2019) The effects of probiotic and synbiotic supplementation on inflammatory markers among patients with diabetes: a systematic review and meta-analysis of randomized controlled trials. Eur J Pharmacol 852:254–264CrossRef Tabrizi R, Ostadmohammadi V, Lankarani KB, Akbari M, Akbari H, Vakili S, Shokrpour M, Kolahdooz F, Rouhi V, Asemi Z (2019) The effects of probiotic and synbiotic supplementation on inflammatory markers among patients with diabetes: a systematic review and meta-analysis of randomized controlled trials. Eur J Pharmacol 852:254–264CrossRef
28.
go back to reference Eslamparast T, Poustchi H, Zamani F, Sharafkhah M, Malekzadeh R, Hekmatdoost A (2014) Synbiotic supplementation in nonalcoholic fatty liver disease: a randomized, double-blind, placebo-controlled pilot study. Am J Clin Nutr 99(3):535–542CrossRef Eslamparast T, Poustchi H, Zamani F, Sharafkhah M, Malekzadeh R, Hekmatdoost A (2014) Synbiotic supplementation in nonalcoholic fatty liver disease: a randomized, double-blind, placebo-controlled pilot study. Am J Clin Nutr 99(3):535–542CrossRef
29.
go back to reference Loman BR, Hernández-Saavedra D, An R, Rector RS (2018) Prebiotic and probiotic treatment of nonalcoholic fatty liver disease: a systematic review and meta-analysis. Nutr Rev 76(11):822–839CrossRef Loman BR, Hernández-Saavedra D, An R, Rector RS (2018) Prebiotic and probiotic treatment of nonalcoholic fatty liver disease: a systematic review and meta-analysis. Nutr Rev 76(11):822–839CrossRef
30.
go back to reference Shi H, Kokoeva MV, Inouye K, Tzameli I, Yin H, Flier JS (2006) TLR4 links innate immunity and fatty acid–induced insulin resistance. J Clin Invest 116(11):3015–3025CrossRef Shi H, Kokoeva MV, Inouye K, Tzameli I, Yin H, Flier JS (2006) TLR4 links innate immunity and fatty acid–induced insulin resistance. J Clin Invest 116(11):3015–3025CrossRef
31.
go back to reference Shi X-Z, Lindholm PF, Sarna SK (2003) NF-κB activation by oxidative stress and inflammation suppresses contractility in colonic circular smooth muscle cells. Gastroenterology 124(5):1369–1380CrossRef Shi X-Z, Lindholm PF, Sarna SK (2003) NF-κB activation by oxidative stress and inflammation suppresses contractility in colonic circular smooth muscle cells. Gastroenterology 124(5):1369–1380CrossRef
32.
go back to reference Lee J-H, Lee B, Lee H-S, Bae E-A, Lee H, Ahn Y-T, Lim K-S, Huh C-S, Kim D-H (2009) Lactobacillus suntoryeus inhibits pro-inflammatory cytokine expression and TLR-4-linked NF-κB activation in experimental colitis. Int J Color Dis 24(2):231–237CrossRef Lee J-H, Lee B, Lee H-S, Bae E-A, Lee H, Ahn Y-T, Lim K-S, Huh C-S, Kim D-H (2009) Lactobacillus suntoryeus inhibits pro-inflammatory cytokine expression and TLR-4-linked NF-κB activation in experimental colitis. Int J Color Dis 24(2):231–237CrossRef
33.
go back to reference Anderson A, McNaught C, Jain P, MacFie J (2004) Randomised clinical trial of synbiotic therapy in elective surgical patients. Gut 53(2):241–245CrossRef Anderson A, McNaught C, Jain P, MacFie J (2004) Randomised clinical trial of synbiotic therapy in elective surgical patients. Gut 53(2):241–245CrossRef
34.
go back to reference Asemi Z, Zare Z, Shakeri H, S-s S, Esmaillzadeh A (2013) Effect of multispecies probiotic supplements on metabolic profiles, hs-CRP, and oxidative stress in patients with type 2 diabetes. Ann Nutr Metab 63(1-2):1–9CrossRef Asemi Z, Zare Z, Shakeri H, S-s S, Esmaillzadeh A (2013) Effect of multispecies probiotic supplements on metabolic profiles, hs-CRP, and oxidative stress in patients with type 2 diabetes. Ann Nutr Metab 63(1-2):1–9CrossRef
35.
go back to reference Hatakka K, Martio J, Korpela M, Herranen M, Poussa T, Laasanen T, Saxelin M, Vapaatalo H, Moilanen E, Korpela R (2003) Effects of probiotic therapy on the activity and activation of mild rheumatoid arthritis–a pilot study. Scand J Rheumatol 32(4):211–215CrossRef Hatakka K, Martio J, Korpela M, Herranen M, Poussa T, Laasanen T, Saxelin M, Vapaatalo H, Moilanen E, Korpela R (2003) Effects of probiotic therapy on the activity and activation of mild rheumatoid arthritis–a pilot study. Scand J Rheumatol 32(4):211–215CrossRef
36.
go back to reference Zhang J, Du P, Chen D, Cui L, Ying C (2010) Effect of viable Bifidobacterium supplement on the immune status and inflammatory response in patients undergoing resection for colorectal cancer. Zhonghua Wei Chang Wai Ke Za Zhi 13(1):40–43PubMed Zhang J, Du P, Chen D, Cui L, Ying C (2010) Effect of viable Bifidobacterium supplement on the immune status and inflammatory response in patients undergoing resection for colorectal cancer. Zhonghua Wei Chang Wai Ke Za Zhi 13(1):40–43PubMed
37.
go back to reference Sadrzadeh-Yeganeh H, Elmadfa I, Djazayery A, Jalali M, Heshmat R, Chamary M (2010) The effects of probiotic and conventional yoghurt on lipid profile in women. Br J Nutr 103(12):1778–1783CrossRef Sadrzadeh-Yeganeh H, Elmadfa I, Djazayery A, Jalali M, Heshmat R, Chamary M (2010) The effects of probiotic and conventional yoghurt on lipid profile in women. Br J Nutr 103(12):1778–1783CrossRef
38.
go back to reference Hegazy SK, El-Bedewy MM (2010) Effect of probiotics on pro-inflammatory cytokines and NF-κB activation in ulcerative colitis. World J Gastroenterol: WJG 16(33):4145–4151CrossRef Hegazy SK, El-Bedewy MM (2010) Effect of probiotics on pro-inflammatory cytokines and NF-κB activation in ulcerative colitis. World J Gastroenterol: WJG 16(33):4145–4151CrossRef
Metadata
Title
Effects of synbiotic supplementation on serum adiponectin and inflammation status of overweight and obese breast cancer survivors: a randomized, triple-blind, placebo-controlled trial
Authors
Mahsa Raji Lahiji
Mitra Zarrati
Safa Najafi
Bahareh Yazdani
Elhameh Cheshmazar
Elham Razmpoosh
Leila Janani
Mahtab Raji Lahiji
Farzad Shidfar
Publication date
01-07-2021
Publisher
Springer Berlin Heidelberg
Published in
Supportive Care in Cancer / Issue 7/2021
Print ISSN: 0941-4355
Electronic ISSN: 1433-7339
DOI
https://doi.org/10.1007/s00520-020-05926-8

Other articles of this Issue 7/2021

Supportive Care in Cancer 7/2021 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine