Abstract
Purpose
Increasing evidence suggests that Mediterranean Diet (MD) is correlated with reduced risk of breast cancer (BC) and cancer mortality, since it modifies patients’ serum antioxidant capacity, body composition and biochemical parameters. The aim of the study was to investigate whether a dietary intervention based on MD has a beneficial effect on these factors.
Methods
In this intervention study, seventy female BC survivors were randomly assigned to (1) the intervention group (personalized dietary intervention based on MD) and (2) the control group (received the updated American Cancer Society Guidelines on Nutrition and Physical Activity for Cancer Prevention and ad libitum diet). Both groups were assessed twice [beginning, end of study (after 6 months)] regarding their anthropometric and biochemical parameters, serum vitamin C, vitamin A, a-tocopherol and CoQ10 levels, dietary intake and adherence to MD. An additional intermediate analysis was conducted on participants’ body composition and biochemical profile.
Results
Concerning the intervention group, body weight, body fat mass, waist circumference, body mass index as well as HDL-cholesterol were significantly decreased (P < 0.2%). An increase was observed in the vitamin C levels in blood (P < 0.2%). In the control group, body weight, body fat mass and serum total cholesterol rose (P < 0.2%). At the end of the study the two groups were significantly different considering blood glucose, vitamin C, polyunsaturated fatty acids, vitamin A and a-tocopherol levels.
Conclusions
This randomized dietary intervention based on MD managed to ameliorate serum antioxidant capacity, body composition, adherence to MD and glycemic profile of postmenopausal BC survivors.
This is a preview of subscription content, access via your institution.

References
Siegel R, Naishadham D, Jemal A (2013) Cancer statistics. CA Cancer J Clin 63(1):11–30. doi:10.3322/caac.21166
Chu KC, Tarone RE, Kessler LG, Ries LA, Hankey BF, Miller BA, Edwards BK (1996) Recent trends in US breast cancer incidence, survival, and mortality rates. J Natl Cancer Inst 88(21):1571–1579
Ferlay J, Steliarova-Foucher E, Lortet-Tieulent J, Rosso S, Coebergh JW, Comber H, Forman D, Bray F (2013) Cancer incidence and mortality patterns in Europe: estimates for 40 countries in 2012. Eur J Cancer 49(6):1374–1403. doi:10.1016/j.ejca.2012.12.027
UK CR (2011). http://www.cancerresearchuk.org/health-professional/cancer-statistics/survival. Accessed 20 May 2016
Dong C, Hemminki K (2001) Second primary neoplasms in 633,964 cancer patients in Sweden, 1958–1996. Int J Cancer 93(2):155–161. doi:10.1002/ijc.1317
Soerjomataram I, Louwman WJ, Lemmens VE, de Vries E, Klokman WJ, Coebergh JW (2005) Risks of second primary breast and urogenital cancer following female breast cancer in the south of The Netherlands, 1972–2001. Eur J Cancer 41(15):2331–2337. doi:10.1016/j.ejca.2005.01.029
Rubino C, Arriagada R, Delaloge S, Le MG (2010) Relation of risk of contralateral breast cancer to the interval since the first primary tumour. Br J Cancer 102(1):213–219. doi:10.1038/sj.bjc.660543
Makari-Judson G, Braun B, Jerry DJ, Mertens WC (2014) Weight gain following breast cancer diagnosis: Implication and proposed mechanisms. World J Clin Oncol 5(3):272–282. doi:10.5306/wjco.v5.i3.272
Haque R, Prout M, Geiger AM, Kamineni A, Thwin SS, Avila C, Silliman RA, Quinn V, Yood MU (2014) Comorbidities and cardiovascular disease risk in older breast cancer survivors. Am J Manag Care 20(1):86–92
Parkin DM, Boyd L, Walker LC (2011) 16. The fraction of cancer attributable to lifestyle and environmental factors in the UK in 2010. Br J Cancer 105(Suppl 2):S77–S81. doi:10.1038/bjc.2011.489
Rock CL, Doyle C, Demark-Wahnefried W, Meyerhardt J, Courneya KS, Schwartz AL, Bandera EV, Hamilton KK, Grant B, McCullough M, Byers T, Gansler T (2012) Nutrition and physical activity guidelines for cancer survivors. CA Cancer J Clin 62(4):243–274. doi:10.3322/caac.21142
Ibrahim EM, Al-Homaidh A (2011) Physical activity and survival after breast cancer diagnosis: meta-analysis of published studies. Med Oncol 28(3):753–765. doi:10.1007/s12032-010-9536-x
Sheppard VB, Hicks J, Makambi K, Hurtado-de-Mendoza A, Demark-Wahnefried W, Adams-Campbell L (2016) The feasibility and acceptability of a diet and exercise trial in overweight and obese black breast cancer survivors: The Stepping STONE study. Contemp Clin Trials 46:106–113. doi:10.1016/j.cct.2015.12.005
Nichols HB, Trentham-Dietz A, Egan KM, Titus-Ernstoff L, Holmes MD, Bersch AJ, Holick CN, Hampton JM, Stampfe MJ, Willet WC, Newcomb PA (2009) Body mass index before and after breast cancer diagnosis: associations with all-cause, breast cancer, and cardiovascular disease mortality. Cancer Epidemiol Biomark Prev 18(5):1403–1409. doi:10.1158/1055-9965.EPI-08-1094
Goodwin PJ, Boyd NF (1990) Body size and breast cancer prognosis: a critical review of the evidence. Breast Cancer Res Treat 16(3):205–214
Protani M, Coory M, Martin JH (2010) Effect of obesity on survival of women with breast cancer: systematic review and meta-analysis. Breast Cancer Res Treat 123(3):627–635. doi:10.1007/s10549-010-0990-0
Vera-Ramirez L, Sanchez-Rovira P, Ramirez-Tortosa MC, Ramirez-Tortosa CL, Granados-Principal S, Lorente JA, Quiles JL (2011) Free radicals in breast carcinogenesis, breast cancer progression and cancer stem cells. Biological bases to develop oxidative-based therapies. Crit Rev Oncol Hematol 80(3):347–368. doi:10.1016/j.critrevonc.2011.01.004
Nourazarian AR, Kangari P, Salmaninejad A (2014) Roles of oxidative stress in the development and progression of breast cancer. Asian Pac J Cancer Prev 15(12):4745–4751
Allen RG, Tresini M (2000) Oxidative stress and gene regulation. Free Radic Biol Med 28(3):463–499
Sangeetha P, Das UN, Koratkar R, Suryaprabha P (1990) Increase in free radical generation and lipid peroxidation following chemotherapy in patients with cancer. Free Radic Biol Med 8(1):15–19
Michels KB, Mohllajee AP, Roset-Bahmanyar E, Beehler GP, Moysich KB (2007) Diet and breast cancer: a review of the prospective observational studies. Cancer 109(Suppl 12):2712–2749
Knekt P, Aromaa A, Maatela J, Aaran R-K, Nikkari T, Hakama M, Hakulinen T, Peto R, Teppo L (1990) Serum vitamin A and subsequent risk of cancer: cancer incidence follow-up of the Finnish Mobile Clinic Health Examination Survey. Am J Epidemiol 132(5):857–870. doi:10.1093/oxfordjournals.aje.a115728
Gerber M, Segala C (1992) Aging and cancer: plasma antioxidants and lipid peroxidation in young and aged breast cancer patients. EXS 62:235–246
Folkers K, Osterborg A, Nylander M, Morita M, Mellstedt H (1997) Activities of vitamin Q10 in animal models and a serious deficiency in patients with cancer. Biochem Biophys Res Commun 234(2):296–299. doi:10.1006/bbrc.1997.6522
Cooney RV, Dai Q, Gao YT, Chow WH, Franke AA, Shu XO, Li H, Ji B, Cai Q, Chai W, Zheng W (2011) Low plasma coenzyme Q(10) levels and breast cancer risk in Chinese women. Cancer Epidemiol Biomarkers Prev 20(6):1124–1130. doi:10.1158/1055-9965.EPI-10-1261
Bakker MF, Peeters PH, Klaasen VM, Bueno-de-Mesquita HB, Jansen EH, Ros MM, Travier N, Olsen A, Tjonneland A, Overvad K, Rinaldi S, Romieu I, Brennan P, Boutron-Ruault MC, Perquier F, Cadeau C, Boeing H, Aleksandrova K, Kaaks R, Kuhn T, Trichopoulou A, Lagiou P, Trichopoulos D, Vineis P, Krogh V, Panico S, Masala G, Tumino R, Weiderpass E, Skeie G, Lund E, Quiros JR, Ardanaz E, Navarro C, Amiano P, Sanchez MJ, Buckland G, Ericson U, Sonestedt E, Johansson M, Sund M, Travis RC, Key TJ, Khaw KT, Wareham N, Riboli E, van Gils CH (2016) Plasma carotenoids, vitamin C, tocopherols, and retinol and the risk of breast cancer in the European Prospective Investigation into Cancer and Nutrition cohort. Am J Clin Nutr 103(2):454–464. doi:10.3945/ajcn.114.101659
Shah FD, Patel JB, Shukla SN, Shah PM, Patel PS (2009) Evaluation of plasma non-enzymatic antioxidants in breast cancer etiology. Asian Pac J Cancer Prev 10(1):91–96
Block G, Norkus E, Hudes M, Mandel S, Helzlsouer K (2001) Which plasma antioxidants are most related to fruit and vegetable consumption? Am J Epidemiol 154(12):1113–1118
Albuquerque RC, Baltar VT, Marchioni DM (2014) Breast cancer and dietary patterns: a systematic review. Nutr Rev 72(1):1–17. doi:10.1111/nure.12083
Trichopoulos D, Lagiou P (2004) Mediterranean diet and cardiovascular epidemiology. Eur J Epidemiol 19(1):7–8
Trichopoulou A (2004) Traditional Mediterranean diet and longevity in the elderly: a review. Public Health Nutr 7(7):943–947. doi:10.1079/PHN2004558
Keys A, Menotti A, Karvonen MJ, Aravanis C, Blackburn H, Buzina R, Djordjevic BS, Dontas AS, Fidanza F, Keys MH et al (1986) The diet and 15-year death rate in the seven countries study. Am J Epidemiol 124(6):903–915
Toledo E, Salas-Salvado J, Donat-Vargas C, Buil-Cosiales P, Estruch R, Ros E, Corella D, Fito M, Hu FB, Aros F, Gomez-Gracia E, Romaguera D, Ortega-Calvo M, Serra-Majem L, Pinto X, Schroder H, Basora J, Sorli JV, Bullo M, Serra-Mir M, Martinez-Gonzalez MA (2015) Mediterranean diet and invasive breast cancer risk among women at high cardiovascular risk in the PREDIMED Trial: a randomized clinical trial. JAMA Intern Med 175(11):1752–1760. doi:10.1001/jamainternmed.2015.4838
Mourouti N, Kontogianni MD, Papavagelis C, Plytzanopoulou P, Vassilakou T, Malamos N, Linos A, Panagiotakos DB (2014) Adherence to the Mediterranean diet is associated with lower likelihood of breast cancer: a case–control study. Nutr Cancer 66(5):810–817. doi:10.1080/01635581.2014.916319
Trichopoulou A, Bamia C, Lagiou P, Trichopoulos D (2010) Conformity to traditional Mediterranean diet and breast cancer risk in the Greek EPIC (European Prospective Investigation into Cancer and Nutrition) cohort. Am J Clin Nutr 92(3):620–625. doi:10.3945/ajcn.2010.29619
Schwingshackl L, Hoffmann G (2016) Does a Mediterranean-type diet reduce cancer risk? Curr Nutr Rep 5:9–17. doi:10.1007/s13668-015-0141-7141
Couto E, Boffetta P, Lagiou P, Ferrari P, Buckland G, Overvad K, Dahm CC, Tjonneland A, Olsen A, Clavel-Chapelon F, Boutron-Ruault MC, Cottet V, Trichopoulos D, Naska A, Benetou V, Kaaks R, Rohrmann S, Boeing H, von Ruesten A, Panico S, Pala V, Vineis P, Palli D, Tumino R, May A, Peeters PH, Bueno-de-Mesquita HB, Buchner FL, Lund E, Skeie G, Engeset D, Gonzalez CA, Navarro C, Rodriguez L, Sanchez MJ, Amiano P, Barricarte A, Hallmans G, Johansson I, Manjer J, Wirfart E, Allen NE, Crowe F, Khaw KT, Wareham N, Moskal A, Slimani N, Jenab M, Romaguera D, Mouw T, Norat T, Riboli E, Trichopoulou A (2011) Mediterranean dietary pattern and cancer risk in the EPIC cohort. Br J Cancer 104(9):1493–1499. doi:10.1038/bjc.2011.106
Pitsavos C, Panagiotakos DB, Tzima N, Chrysohoou C, Economou M, Zampelas A, Stefanadis C (2005) Adherence to the Mediterranean diet is associated with total antioxidant capacity in healthy adults: the ATTICA study. Am J Clin Nutr 82(3):694–699
Dilis V, Trichopoulou A (2010) Antioxidant intakes and food sources in Greek adults. J Nutr 140(7):1274–1279. doi:10.3945/jn.110.121848
Salas-Salvado J, Bullo M, Babio N, Martinez-Gonzalez MA, Ibarrola-Jurado N, Basora J, Estruch R, Covas MI, Corella D, Aros F, Ruiz-Gutierrez V, Ros E (2011) Reduction in the incidence of type 2 diabetes with the Mediterranean diet: results of the PREDIMED-Reus nutrition intervention randomized trial. Diabetes Care 34(1):14–19. doi:10.2337/dc10-1288
Penalvo JL, Oliva B, Sotos-Prieto M, Uzhova I, Moreno-Franco B, Leon-Latre M, Ordovas JM (2015) Greater adherence to a Mediterranean dietary pattern is associated with improved plasma lipid profile: the Aragon Health Workers Study cohort. Rev Esp Cardiol (Engl Ed) 68(4):290–297. doi:10.1016/j.rec.2014.09.019
Bland KCE (2009) The breast—comprehensive management of benign and malignant diseases, 4th edn. Saunders, Philadelphia
Kushi LH, Doyle C, McCullough M, Rock CL, Demark-Wahnefried W, Bandera EV, Gapstur S, Patel AV, Andrews K, Gansler T (2012) American Cancer Society Guidelines on nutrition and physical activity for cancer prevention: reducing the risk of cancer with healthy food choices and physical activity. CA Cancer J Clin 62(1):30–67. doi:10.3322/caac.20140
Harasym J, Oledzki R (2014) Effect of fruit and vegetable antioxidants on total antioxidant capacity of blood plasma. Nutrition 30(5):511–517. doi:10.1016/j.nut.2013.08.019
Flower G, Fritz H, Balneaves LG, Verma S, Skidmore B, Fernandes R, Kennedy D, Cooley K, Wong R, Sagar S, Fergusson D, Seely D (2014) Flax and breast cancer: a systematic review. Integr Cancer Ther 13(3):181–192. doi:10.1177/1534735413502076
Giovannucci E, Ascherio A, Rimm EB, Stampfer MJ, Colditz GA, Willett WC (1995) Intake of carotenoids and retinol in relation to risk of prostate cancer. J Natl Cancer Inst 87(23):1767–1776
Gallagher D, Heymsfield SB, Heo M, Jebb SA, Murgatroyd PR, Sakamoto Y (2000) Healthy percentage body fat ranges: an approach for developing guidelines based on body mass index. Am J Clin Nutr 72(3):694–701
NHLBI NHLI Target Levels for Weight Loss (2016) http://www.nhlbi.nih.gov/health-pro/guidelines/current/obesity-guidelines/e_textbook/txgd/4311.htm. Accessed 20 June 2017
Bach-Faig A, Berry EM, Lairon D, Reguant J, Trichopoulou A, Dernini S, Medina FX, Battino M, Belahsen R, Miranda G, Serra-Majem L (2011) Mediterranean diet pyramid today. Science and cultural updates. Public Health Nutr 14(12A):2274–2284. doi:10.1017/S1368980011002515
Mourouti N, Papavagelis C, Psaltopoulou T, Aravantinos G, Samantas E, Filopoulos E, Manousou A, Plytzanopoulou P, Vassilakou T, Malamos N, Panagiotakos DB (2013) Aims, design and methods of a case-control study for the assessment of the role of dietary habits, eating behaviors and environmental factors, on the development of breast cancer. Maturitas 74(1):31–36. doi:10.1016/j.maturitas.2012.10.004
Willett WC, Sacks F, Trichopoulou A, Drescher G, Ferro-Luzzi A, Helsing E, Trichopoulos D (1995) Mediterranean diet pyramid: a cultural model for healthy eating. Am J Clin Nutr 61(6 Suppl):1402S–1406S
Trichopoulou A, Georga K (2004) Composition tables of foods and Greek dishes, 3rd Edn. Parisianou Publications, Athens, GA
Trichopoulou A, Costacou T, Bamia C, Trichopoulos D (2003) Adherence to a Mediterranean diet and survival in a Greek population. N Engl J Med 348(26):2599–2608. doi:10.1056/NEJMoa025039348/26/2599
Papathanasiou G, Georgoudis G, Papandreou M, Spyropoulos P, Georgakopoulos D, Kalfakakou V, Evangelou A (2009) Reliability measures of the short International Physical Activity Questionnaire (IPAQ) in Greek young adults. Hellenic J Cardiol 50(4):283–294
Oken MM, Creech RH, Tormey DC, Horton J, Davis TE, McFadden ET, Carbone PP (1982) Toxicity and response criteria of the Eastern Cooperative Oncology Group. Am J Clin Oncol 5(6):649–655
Centers for Disease Control and prevention (CDC, 2015) About Adult BMI. https://www.cdc.gov/healthyweight/assessing/bmi/adult_bmi/index.html. Accessed 20 June 2017
Harris HR, Orsini N, Wolk A (2014) Vitamin C and survival among women with breast cancer: a meta-analysis. Eur J Cancer 50(7):1223–1231. doi:10.1016/j.ejca.2014.02.013
Potentas E, Witkowska AM, Zujko ME (2015) Mediterranean diet for breast cancer prevention and treatment in postmenopausal women. Prz Menopauzalny 14(4):247–253. doi:10.5114/pm.2015.5638126384
Wise J (2015) Reduced breast cancer risk seen with Mediterranean diet and added olive oil. BMJ 351:h4911
Villarini A, Pasanisi P, Traina A, Mano MP, Bonanni B, Panico S, Scipioni C, Galasso R, Paduos A, Simeoni M, Bellotti E, Barbero M, Macellari G, Venturelli E, Raimondi M, Bruno E, Gargano G, Fornaciari G, Morelli D, Seregni E, Krogh V, Berrino F (2012) Lifestyle and breast cancer recurrences: the DIANA-5 trial. Tumori 98(1):1–18. doi:10.1700/1053.11494
Demark-Wahnefried W, Platz EA, Ligibel JA, Blair CK, Courneya KS, Meyerhardt JA, Ganz PA, Rock CL, Schmitz KH, Wadden T, Philip EJ, Wolfe B, Gapstur SM, Ballard-Barbash R, McTiernan A, Minasian L, Nebeling L, Goodwin PJ (2012) The role of obesity in cancer survival and recurrence. Cancer Epidemiol Biomarkers Prev 21(8):1244–1259. doi:10.1158/1055-9965.EPI-12-0485
Druesne-Pecollo N, Touvier M, Barrandon E, Chan DS, Norat T, Zelek L, Hercberg S, Latino-Martel P (2012) Excess body weight and second primary cancer risk after breast cancer: a systematic review and meta-analysis of prospective studies. Breast Cancer Res Treat 135(3):647–654. doi:10.1007/s10549-012-2187-1
De Bruijn KM, Arends LR, Hansen BE, Leeflang S, Ruiter R, van Eijck CH (2013) Systematic review and meta-analysis of the association between diabetes mellitus and incidence and mortality in breast and colorectal cancer. Br J Surg 100(11):1421–1429. doi:10.1002/bjs.9229
Boyle P, Boniol M, Koechlin A, Robertson C, Valentini F, Coppens K, Fairley LL, Zheng T, Zhang Y, Pasterk M, Smans M, Curado MP, Mullie P, Gandini S, Bota M, Bolli GB, Rosenstock J, Autier P (2012) Diabetes and breast cancer risk: a meta-analysis. Br J Cancer 107(9):1608–1617. doi:10.1038/bjc.2012.414
Tabatabaei-Malazy O, Fakhrzadeh H, Sharifi F, Mirarefin M, Arzaghi SM, Badamchizadeh Z, Alizadeh Khoee M, Larijani B (2015) Effect of metabolic control on oxidative stress, subclinical atherosclerosis and peripheral artery disease in diabetic patients. J Diabetes Metab Disord 14:84. doi:10.1186/s40200-015-0215-5215
Acknowledgements
The authors would like to express their gratitude to all the volunteers who participated in the study. The authors would like also to express their very great appreciation to (1) Nikolaos Skourlis for his help in the Supplementary material and to (2) Anna Maria Maragaki for her help concerning data collection.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
M. Skouroliakou, D. Grosomanidis, P. Massara, C. Kostara, P. Papandreou, D. Ntountaniotis and G. Xepapadakis reported no conflict of interest related to the study.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Skouroliakou, M., Grosomanidis, D., Massara, P. et al. Serum antioxidant capacity, biochemical profile and body composition of breast cancer survivors in a randomized Mediterranean dietary intervention study. Eur J Nutr 57, 2133–2145 (2018). https://doi.org/10.1007/s00394-017-1489-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00394-017-1489-9
Keywords
- Breast cancer survivors
- Mediterranean diet
- Dietary antioxidants
- Body composition
- Biochemical profile