Abstract
Purpose
No conclusive information is available about the association between dietary total antioxidant capacity (DTAC) and risk of mortality. Current meta-analysis of prospective cohort studies was done to summarize available findings on the association between DTAC and risk of death from all-cause, cancer and cardiovascular diseases (CVDs).
Methods
Online databases were searched to detect relevant publications up to January 2018, using relevant keywords. To pool data, either fixed-effects or random-effects model was used. Furthermore, linear and non-linear dose–response analyses were also done.
Results
In total, five prospective studies were included in the current systematic review and meta-analysis. In a follow-up period of 4.3–16.5 years, there were 38,449 deaths from all-cause, 4470 from cancer and 2841 from CVDs among 226,297 individuals. A significant inverse association was found between DTAC and all-cause mortality (combined effect size: 0.62, 95% CI 0.60–0.64). Such finding was also seen for cancer (combined effect size: 0.81, 95% CI 0.75–0.88) and CVD (combined effect size: 0.71, 95% CI 0.63–0.82) mortality. Findings from linear dose–response meta-analysis revealed that a 5 mmol/day increment in DTAC based on ferric reducing antioxidant power (FRAP) and oxygen radical absorbance capacity (ORAC) was associated with 7% and 15% lower risk of all-cause mortality, respectively. Based on findings from non-linear dose–response meta-analysis, a significant reduction in risk of all-cause mortality was seen when increasing FRAP from 2 to 12 mmol/day (P-nonlinearity = 0.002) and ORAC from 5 to 11 mmol/day (P-nonlinearity < 0.001).
Conclusions
Adherence to diet with high total antioxidant capacity was associated with decreased risk of death from all-cause, cancer and CVDs.
Similar content being viewed by others
Abbreviations
- DTAC:
-
Dietary total antioxidant capacity
- FRAP:
-
Ferric reducing antioxidant power
- TRAP:
-
Total radical trapping antioxidant parameter
- TEAC:
-
Trolox equivalence antioxidant capacity
- ORAC:
-
Oxygen radical absorbance capacity
- OR:
-
Odds ratio
- RR:
-
Relative risk
- HR:
-
Hazard ratio
- FFQ:
-
Food frequency questionnaire
- CVD:
-
Cardiovascular disease
References
Reuter S, Gupta SC, Chaturvedi MM, Aggarwal BB (2010) Oxidative stress, inflammation, and cancer: how are they linked? Free Radic Biol Med 49:1603–1616. https://doi.org/10.1016/j.freeradbiomed.2010.09.006
Niemann B, Rohrbach S, Miller MR, Newby DE, Fuster V, Kovacic JC (2017) Oxidative stress and cardiovascular risk: obesity, diabetes, smoking, and pollution: part 3 of a 3-part series. J Am Coll Cardiol 70:230–251. https://doi.org/10.1016/j.jacc.2017.05.043
Robson R, Kundur AR, Singh I (2017) Oxidative stress biomarkers in type 2 diabetes mellitus for assessment of cardiovascular disease risk. Diabetes Metab Syndr. https://doi.org/10.1016/j.dsx.2017.12.029
Xie Z, Lin H, Fang R, Shen W, Li S, Chen B (2015) Effects of a fruit-vegetable dietary pattern on oxidative stress and genetic damage in coke oven workers: a cross-sectional study. Environ Health 14:40. https://doi.org/10.1186/s12940-015-0028-5
de la Iglesia R, Lopez-Legarrea P, Celada P, Sanchez-Muniz FJ, Martinez JA, Zulet MA (2013) Beneficial effects of the RESMENA dietary pattern on oxidative stress in patients suffering from metabolic syndrome with hyperglycemia are associated to dietary TAC and fruit consumption. Int J Mol Sci 14:6903–6919. https://doi.org/10.3390/ijms14046903
Kim K, Vance TM, Chen M-H, Chun OK (2017) Dietary total antioxidant capacity is inversely associated with all-cause and cardiovascular disease death of US adults. Eur J Nutr 57:2469–2476. https://doi.org/10.1007/s00394-017-1519-7
Bastide N, Dartois L, Dyevre V, Dossus L, Fagherazzi G, Serafini M et al (2017) Dietary antioxidant capacity and all-cause and cause-specific mortality in the E3N/EPIC cohort study. Eur J Nutr 56:1233–1243
Michaëlsson K, Wolk A, Melhus H, Byberg L (2017) Milk, fruit and vegetable, and total antioxidant intakes in relation to mortality rates: cohort studies in women and men. Am J Epidemiol 185:345–361
Henriquez-Sanchez P, Sánchez-Villegas A, Ruano-Rodríguez C, Gea A, Lamuela-Raventós RM, Estruch R et al (2016) Dietary total antioxidant capacity and mortality in the PREDIMED study. Eur J Nutr 55:227–236
Agudo A, Cabrera L, Amiano P, Ardanaz E, Barricarte A, Berenguer T et al (2007) Fruit and vegetable intakes, dietary antioxidant nutrients, and total mortality in Spanish adults: findings from the Spanish cohort of the European Prospective Investigation into Cancer and Nutrition (EPIC-Spain). Am J Clin Nutr 85:1634–1642
Peng C, Luo WP, Zhang CX (2017) Fruit and vegetable intake and breast cancer prognosis: a meta-analysis of prospective cohort studies. Br J Nutr 117:737–749. https://doi.org/10.1017/s0007114517000423
Wang X, Ouyang Y, Liu J, Zhu M, Zhao G, Bao W et al (2014) Fruit and vegetable consumption and mortality from all causes, cardiovascular disease, and cancer: systematic review and dose-response meta-analysis of prospective cohort studies. Bmj 349:g4490. https://doi.org/10.1136/bmj.g4490
Wang Q, Chen Y, Wang X, Gong G, Li G, Li C (2014) Consumption of fruit, but not vegetables, may reduce risk of gastric cancer: results from a meta-analysis of cohort studies. Eur J Cancer 50:1498–1509. https://doi.org/10.1016/j.ejca.2014.02.009
Tabernero M, Serrano J, Saura-Calixto F (2006) The antioxidant capacity of cocoa products: contribution to the Spanish diet. Int J Food Sci Technol 41:28–32
Pellegrini N, Serafini M, Colombi B, Del Rio D, Salvatore S, Bianchi M et al (2003) Total antioxidant capacity of plant foods, beverages and oils consumed in Italy assessed by three different in vitro assays. J Nutr 133:2812–2819
Dietrich M, Jacques P, Pencina M, Lanier K, Keyes M, Kaur G et al (2009) Vitamin E supplement use and the incidence of cardiovascular disease and all-cause mortality in the Framingham Heart Study: Does the underlying health status play a role? Atherosclerosis 205:549–553
Zhao LG, Shu XO, Li HL, Zhang W, Gao J, Sun JW et al (2017) Dietary antioxidant vitamins intake and mortality: A report from two cohort studies of Chinese adults in Shanghai. J Epidemiol 27:89–97. https://doi.org/10.1016/j.je.2016.10.002
Buijsse B, Feskens EJ, Kwape L, Kok FJ, Kromhout D (2008) Both alpha- and beta-carotene, but not tocopherols and vitamin C, are inversely related to 15-year cardiovascular mortality in Dutch elderly men. J Nutr 138:344–350
Pellegrini N, Vitaglione P, Granato D, Fogliano V (2018) Twenty-five years of total antioxidant capacity measurement of foods and biological fluids: merits and limitations. J Sci Food Agric. https://doi.org/10.1002/jsfa.9550
Fraga CG, Oteiza PI, Galleano M (2014) In vitro measurements and interpretation of total antioxidant capacity. Biochim Biophys Acta 1840:931–934. https://doi.org/10.1016/j.bbagen.2013.06.030
Pompella A, Sies H, Wacker R, Brouns F, Grune T, Biesalski HK et al (2014) The use of total antioxidant capacity as surrogate marker for food quality and its effect on health is to be discouraged. Nutrition 30:791–793. https://doi.org/10.1016/j.nut.2013.12.002
Manach C, Williamson G, Morand C, Scalbert A, Remesy C (2005) Bioavailability and bioefficacy of polyphenols in humans. I. Review of 97 bioavailability studies. Am J Clin Nutr 81:230s–242s. https://doi.org/10.1093/ajcn/81.1.230S
Basu A, Morris S, Nguyen A, Betts NM, Fu D, Lyons TJ (2016) Effects of dietary strawberry supplementation on antioxidant biomarkers in obese adults with above optimal serum lipids. J Nutr Metab 2016:3910630. https://doi.org/10.1155/2016/3910630.
Pinzani P, Petruzzi E, Magnolfi SU, Malentacchi F, De Siena G, Petruzzi I et al (2010) Red or white wine assumption and serum antioxidant capacity. Arch Gerontol Geriatr 51:e72–e74. https://doi.org/10.1016/j.archger.2009.12.007
Koutelidakis AE, Rallidis L, Koniari K, Panagiotakos D, Komaitis M, Zampelas A (2014) Anastasiou-Nana M, Kapsokefalou M. Effect of green tea on postprandial antioxidant capacity, serum lipids, C-reactive protein and glucose levels in patients with coronary artery disease. Eur J Nutr 53:479–486. https://doi.org/10.1007/s00394-013-0548-0
Lettieri-Barbato D, Villaño D, Beheydt B, Guadagni F, Trogh I, Serafini M (2012) Effect of ingestion of dark chocolates with similar lipid composition and different cocoa content on antioxidant and lipid status in healthy humans. Food Chem 132:1305–1310. https://doi.org/10.1016/j.foodchem.2011.11.109
Yang M, Chung SJ, Floegel A, Song WO, Koo SI, Chun OK (2013) Dietary antioxidant capacity is associated with improved serum antioxidant status and decreased serum C-reactive protein and plasma homocysteine concentrations. Eur J Nutr 52:1901–1911. https://doi.org/10.1007/s00394-012-0491-5
Wang Y, Yang M, Lee SG, Davis CG, Koo SI, Chun OK (2012) Dietary total antioxidant capacity is associated with diet and plasma antioxidant status in healthy young adults. J Acad Nutr Diet 112:1626–1635. https://doi.org/10.1016/j.jand.2012.06.007
Hermsdorff HH, Puchau B, Volp AC, Barbosa KB, Bressan J, Zulet M et al (2011) Dietary total antioxidant capacity is inversely related to central adiposity as well as to metabolic and oxidative stress markers in healthy young adults. Nutr Metab (Lond) 8:22. https://doi.org/10.1186/1743-7075-8-59
Zamora-Ros R, Serafini M, Estruch R, Lamuela-Raventós RM, Martínez-González MA, Salas-Salvadó J et al (2013) Mediterranean diet and non enzymatic antioxidant capacity in the PREDIMED study: evidence for a mechanism of antioxidant tuning. Nutr Metab Cardiovasc Dis 23:1167–1174. https://doi.org/10.1016/j.numecd.2012.12.008
Moher D, Liberati A, Tetzlaff J, Altman DG, Group P (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 6:e1000097
Lorente L, Martín MM, Pérez-Cejas A, Abreu-González P, Ramos L, Argueso M et al (2016) Association between total antioxidant capacity and mortality in ischemic stroke patients. Ann Intensive Care 6:39
Lorente L, Martín MM, Almeida T, Abreu-González P, Ramos L, Argueso M et al (2015) Total antioxidant capacity is associated with mortality of patients with severe traumatic brain injury. BMC Neurol 15:115
Sakhi AK, Russnes KM, Thoresen M, Bastani NE, Karlsen A, Smeland S et al (2009) Pre-radiotherapy plasma carotenoids and markers of oxidative stress are associated with survival in head and neck squamous cell carcinoma patients: a prospective study. BMC Cancer 9:458
Lorente L, Martín MM, Almeida T, Abreu-González P, Ferreres J, Solé-Violán J et al (2015) Association between serum total antioxidant capacity and mortality in severe septic patients. J Crit Care 30:217. e217–217. e212
Fletcher AE, Breeze E, Shetty PS (2003) Antioxidant vitamins and mortality in older persons: findings from the nutrition add-on study to the Medical Research Council Trial of Assessment and Management of Older People in the Community. Am J Clin Nutr 78:999–1010
Rautiainen S, Levitan EB, Orsini N, Åkesson A, Morgenstern R, Mittleman MA et al (2012) Total antioxidant capacity from diet and risk of myocardial infarction: a prospective cohort of women. Am J Med 125:974–980
Rautiainen S, Larsson S, Virtamo J, Wolk A (2012) Total antioxidant capacity of diet and risk of stroke: a population-based prospective cohort of women. Stroke 43:335–340. https://doi.org/10.1161/strokeaha.111.635557
Lucas AL, Bosetti C, Boffetta P, Negri E, Tavani A, Serafini M et al (2016) Dietary total antioxidant capacity and pancreatic cancer risk: an Italian case–control study. Br J Cancer 115:102–107. https://doi.org/10.1038/bjc.2016.114
Vance TM, Wang Y, Su LJ, Fontham ET, Steck SE, Arab L et al (2016) Dietary total antioxidant capacity is inversely associated with prostate cancer aggressiveness in a population-based study. Nutr Cancer 68:214–224. https://doi.org/10.1080/01635581.2016.1134596
Del Rio D, Agnoli C, Pellegrini N, Krogh V, Brighenti F, Mazzeo T et al (2011) Total antioxidant capacity of the diet is associated with lower risk of ischemic stroke in a large Italian cohort. J Nutr 141:118–123. https://doi.org/10.3945/jn.110.125120
Rautiainen S, Levitan EB, Mittleman MA, Wolk A (2013) Total antioxidant capacity of diet and risk of heart failure: a population-based prospective cohort of women. Am J Med 126:494–500
Wells G, Shea B, O’connell D, Peterson J, Welch V, Losos M et al (2015) The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. Ottawa Hospital Research Institute; 2011. oxford. asp
Green S, Higgins J (eds) (2008) The Cochrane handbook for systematic reviews of interventions. Wiley, Chichester
Greenland S, Longnecker MP (1992) Methods for trend estimation from summarized dose-response data, with applications to meta-analysis. Am J Epidemiol 135:1301–1309
Orsini N, Bellocco R, Greenland S (2006) Generalized least squares for trend estimation of summarized dose-response data. Stat J 6:40
Harre FE Jr, Lee KL, Pollock BG (1988) Regression models in clinical studies: determining relationships between predictors and response. JNCI 80:1198–1202
Jackson D, White IR, Thompson SG (2010) Extending DerSimonian and Laird’s methodology to perform multivariate random effects meta-analyses. Stat Med 29:1282–1297
Berlin JA, Longnecker MP, Greenland S (1993) Meta-analysis of epidemiologic dose-response data. Epidemiology 4:218–228
Wong MCS, Fung FDH, Leung C, Cheung WWL, Goggins WB, Ng CF (2018) The global epidemiology of bladder cancer: a joinpoint regression analysis of its incidence and mortality trends and projection. Sci Rep 8:1129. https://doi.org/10.1038/s41598-018-19199-z
Andersson C, Vasan RS (2017) Epidemiology of cardiovascular disease in young individuals. Nat Rev Cardiol. https://doi.org/10.1038/nrcardio.2017.154
Kwasny C, Manuwald U, Kugler J, Rothe U (2017) systematic review of the epidemiology and natural history of the metabolic vascular syndrome and its coincidence with type 2 diabetes mellitus and cardiovascular diseases in different European countries. Horm Metab Res. https://doi.org/10.1055/s-0043-122395
Uppal S, Al-Kindi SG, Oliveira GH (2018) Cardiovascular mortality among 76 864 survivors of childhood cancers in the United States: a report from the surveillance, epidemiology, and end-results program. J Cardiovasc Med (Hagerstown) 19:38–41. https://doi.org/10.2459/jcm.0000000000000585
Benisi-Kohansal S, Saneei P, Salehi-Marzijarani M, Larijani B, Esmaillzadeh A (2016) Whole-grain intake and mortality from all causes, cardiovascular disease, and cancer: a systematic review and dose-response meta-analysis of prospective cohort studies. Adv Nutr 7:1052–1065. https://doi.org/10.3945/an.115.011635
Wang JB, Fan JH, Dawsey SM, Sinha R, Freedman ND, Taylor PR et al (2016) Dietary components and risk of total, cancer and cardiovascular disease mortality in the Linxian Nutrition Intervention Trials cohort in China. Sci Rep 6:22619. https://doi.org/10.1038/srep22619
Pantavos A, Ruiter R, Feskens EF, de Keyser CE, Hofman A, Stricker BH et al (2015) Total dietary antioxidant capacity, individual antioxidant intake and breast cancer risk: the Rotterdam Study. Int J Cancer 136:2178–2186. https://doi.org/10.1002/ijc.29249
Serafini M, Jakszyn P, Lujan-Barroso L, Agudo A, Bas Bueno-de-Mesquita H, van Duijnhoven FJ et al (2012) Dietary total antioxidant capacity and gastric cancer risk in the European prospective investigation into cancer and nutrition study. Int J Cancer 131:E544–E554. https://doi.org/10.1002/ijc.27347
Schwingshackl L, Hoffmann G (2014) Adherence to Mediterranean diet and risk of cancer: a systematic review and meta-analysis of observational studies. Int J Cancer 135:1884–1897. https://doi.org/10.1002/ijc.28824
Perez-Jimenez J, Diaz-Rubio ME, Saura-Calixto F (2015) Contribution of macromolecular antioxidants to dietary antioxidant capacity: a study in the Spanish mediterranean diet. Plant Foods Hum Nutr 70:365–370. https://doi.org/10.1007/s11130-015-0513-6
Chang ET, Lee VS, Canchola AJ, Clarke CA, Purdie DM, Reynolds P et al (2007) Diet and risk of ovarian cancer in the California Teachers Study cohort. Am J Epidemiol 165:802–813. https://doi.org/10.1093/aje/kwk065
Vece MM, Agnoli C, Grioni S, Sieri S, Pala V, Pellegrini N et al (2015) Dietary total antioxidant capacity and colorectal cancer in the Italian EPIC cohort. PLoS One 10:e0142995. https://doi.org/10.1371/journal.pone.0142995
Kim K, Vance TM, Chun OK (2016) Greater total antioxidant capacity from diet and supplements is associated with a less atherogenic blood profile in US adults. Nutrients 8:15
Yang M, Chung S-J, Floegel A, Song WO, Koo SI, Chun OK (2013) Dietary antioxidant capacity is associated with improved serum antioxidant status and decreased serum C-reactive protein and plasma homocysteine concentrations. Eur J Nutr 52:1901–1911
Franklin SS, Wong ND (2013) Hypertension and cardiovascular disease: contributions of the Framingham Heart Study. Global heart 8:49–57
Vasan RS, Larson MG, Leip EP, Evans JC, O’Donnell CJ, Kannel WB et al (2001) Impact of high-normal blood pressure on the risk of cardiovascular disease. N Engl J Med 345:1291–1297
Devore EE, Feskens E, Ikram MA, den Heijer T, Vernooij M, van der Lijn F et al (2013) Total antioxidant capacity of the diet and major neurologic outcomes in older adults. Neurology 80:904–910. https://doi.org/10.1212/WNL.0b013e3182840c84
Stefanson AL, Bakovic M (2014) Dietary regulation of Keap1/Nrf2/ARE pathway: focus on plant-derived compounds and trace minerals. Nutrients 6:3777–3801. https://doi.org/10.3390/nu6093777
Kim Y, Je Y (2014) Dietary fiber intake and total mortality: a meta-analysis of prospective cohort studies. Am J Epidemiol 180:565–573. https://doi.org/10.1093/aje/kwu174
Acknowledgements
This study was supported jointly by Students’ Scientific Research Center, Tehran University of Medical Sciences, Tehran, Iran, and Torbat Heydariyeh University of Medical Sciences, Torbat Heydariyeh, Iran.
Author information
Authors and Affiliations
Contributions
MN, JAS, MP, SRK and MK contributed to conception, design, statistical analyses, data interpretation and manuscript drafting. OS and MP contributed to data analysis, data interpretation and manuscript drafting. All authors approved the final manuscript for submission.
Corresponding author
Ethics declarations
Conflict of interest
The author declares that there is no conflict of interest.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Parohan, M., Anjom-Shoae, J., Nasiri, M. et al. Dietary total antioxidant capacity and mortality from all causes, cardiovascular disease and cancer: a systematic review and dose–response meta-analysis of prospective cohort studies. Eur J Nutr 58, 2175–2189 (2019). https://doi.org/10.1007/s00394-019-01922-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00394-019-01922-9