Association of low plasma antioxidant levels with all-cause mortality and coronary events in healthy middle-aged men from France and Northern Ireland in the PRIME study

Springer Science and Business Media LLC - 2021
Gareth J. McKay1, Natalie Lyner1, Gerard J. Linden1, Frank Kee1, Marie Moitry2, Katia Biasch2, Philippe Amouyel3, Jean Dallongeville3, Vanina Bongard4, Jean Ferrières4, K. F. Gey5, Chris Patterson1, Jayne V. Woodside1
1Centre for Public Health, Royal Victoria Hospital, Queen’s University Belfast, Belfast, BT12 6BA, UK
2MONICA-Strasbourg, Strasbourg, France
3MONICA-Lille, Lille, France
4MONICA-Toulouse, Toulouse, France
5The MONICA Reference Centre for Vitamins, Department of Biochemistry and Molecular Biology, University of Bern, Bern, Switzerland

Tóm tắt

Abstract Background The main underlying risk factors associated with coronary heart disease (CHD) are modifiable and oxidative injury and systemic inflammatory damage represent key aetiological factors associated with the development and progression of CHD and premature mortality. Objective To examine associations of plasma antioxidant status with all-cause mortality and fatal or non-fatal cardiovascular events. Design The PRIME study prospectively evaluated 9709 men aged 50–59 years between 1991 and 1993 in Northern Ireland and France who were free of CHD at recruitment and followed annually for deaths and cardiovascular events for 10 years. Serum concentrations of vitamin C, retinol, two forms of vitamin E (α- and γ-tocopherol) and six carotenoids were quantified by high-performance liquid chromatography. Baseline conventional risk factors were considered, as well as socioeconomic differences and lifestyle behaviours including diet, smoking habit, physical activity, and alcohol consumption through Cox regression analyses. Results At 10 years, there were 538 deaths from any cause and 440 fatal or non-fatal cardiovascular events. After adjustment for country, age, systolic blood pressure, diabetes, body mass index, cholesterol, high density lipoprotein cholesterol, triglycerides, height, total physical activity, alcohol consumption and smoking habit, higher levels of all antioxidants were associated with significantly lower risk of all-cause mortality, with the exception of γ-tocopherol. Only retinol was significantly associated with decreased risk of cardiovascular events in a fully adjusted model. Conclusions Low antioxidant levels contribute to the gradient of all-cause mortality and cardiovascular incidence independent of lifestyle behaviours and traditional cardiovascular and socioeconomic risk factors.

Từ khóa


Tài liệu tham khảo

WHO. https://www.who.int/news-room/fact-sheets/detail/cardiovascular-diseases-(cvds). Accessed 1 July 2020

Libby P (2017) Interleukin-1 beta as a target for atherosclerosis therapy: biological basis of CANTOS and beyond. J Am Coll Cardiol 70:2278–2289

Libby P, Hansson GK (2018) Taming immune and inflammatory responses to treat atherosclerosis. J Am Coll Cardiol 71:173–176

Ceriello A, Motz E (2004) Is oxidative stress the pathogenic mechanism underlying insulin resistance, diabetes, and cardiovascular disease? The common soil hypothesis revisited. ArteriosclerThrombVasc Biol 24:816–823

Gey KF, Ducimetière P, Evans A, Amouyel P, Arveiler D, Ferrières J, Luc G, Kee F, Bingham A, Yarnell J, Cambien F (2010) Low plasma retinol predicts coronary events in healthy middle-aged men: the PRIME study. Atherosclerosis 208:270–274

Woodside JV, Yarnell JW, Patterson CC, Arveiler D, Amouyel P, Ferrières J, Kee F, Evans A, Bingham A, Ducimetière P (2012) Do lifestyle behaviours explain socioeconomic differences in all-cause mortality, and fatal and non-fatal cardiovascular events? Evidence from middle aged men in France and Northern Ireland in the PRIME Study. Prev Med 54:247–253

Aune D, Giovannucci E, Boffetta P, Fadnes LT, Keum N, Norat T, Greenwood DC, Riboli E, Vatten LJ, Tonstad S (2017) Fruit and vegetable intake and the risk of cardiovascular disease, total cancer and all-cause mortality—a systematic review and dose-response meta-analysis of prospective studies. Int J Epidemiol 46:1029–1056

Micha R, Peñalvo JL, Cudhea F, Imamura F, Rehm CD, Mozaffarian D (2017) Association between dietary factors and mortality from heart disease, stroke, and type 2 diabetes in the United States. JAMA 317:912–924

Picó C, Serra F, Rodríguez AM, Keijer J, Palou A (2019) Biomarkers of nutrition and health: new tools for new approaches. Nutrients 11:1092

Aune D, Keum N, Giovannucci E, Fadnes LT, Boffetta P, Greenwood DC, Tonstad S, Vatten LJ, Riboli E, Norat T (2018) Dietary intake and blood concentrations of antioxidants and the risk of cardiovascular disease, total cancer, and all-cause mortality: a systematic review and dose-response meta-analysis of prospective studies. Am J ClinNutr 108:1069–1091

Steinberg D, Parthasarathy S, Carew TE, Khoo JC, Witztum JL (1989) Beyond cholesterol. Modifications of low-density lipoprotein that increase its atherogenicity. N Engl J Med 320:915–924

Diaz MN, Frei B, Vita JA, Keaney JF Jr (1997) Antioxidants and atherosclerotic heart disease. N Engl J Med 337:408–416

Mattioli AV, Palmiero P, Manfrini O, Puddu PE, Nodari S, Dei Cas A, Mercuro G, Scrutinio D, Palermo P, Sciomer S, Di Francesco S, Novo G, Novo S, Pedretti RFE, Zito A, Parati G, Pedrinelli R, Farinetti A, Maiello M, Moscucci F, Tenaglia RL, Sucato V, Triggiani M, Cugusi L, Scicchitano P, Saba PS, Ciccone MM (2017) Mediterranean diet impact on cardiovascular diseases: a narrative review. J Cardiovasc Med (Hagerstown) 18:925–935

Huang J, Weinstein SJ, Yu K, Männistö S, Albanes D (2018) Serum beta carotene and overall and cause-specific mortality. Circ Res 123:1339–1349

Goyal A, Terry MB, Siegel AB (2013) Serum antioxidant nutrients, vitamin A, and mortality in US Adults. Cancer EpidemiolBiomarkPrev 22:2202–2211

Hercberg S, Galan P, Preziosi P, Bertrais S, Mennen L, Malvy D, Roussel AM, Favier A, Briançon S (2004) TheSU.VI.MAX Study: a randomized, placebo-controlled trial of the health effects of antioxidant vitamins and minerals. Arch Intern Med 164:2335–2342

Blot WJ, Li JY, Taylor PR, Guo W, Dawsey S, Wang GQ, Yang CS, Zheng SF, Gail M, Li GY, Yu Y, Liu BQ, Tangrea J, Sun YH, Liu F, Fraumeni JF, Zhang YH, Li B (1993) Nutrition intervention trials in Linxian, China: supplementation with specific vitamin/mineral combinations, cancer incidence, and disease-specific mortality in the general population. J Natl Cancer Inst 85:1483–1492

Tunstall-Pedoe H, Kuulasmaa K, Mahonen M, Tolonen H, Ruokokoski E, Amouyel P (1999) Contribution of trends in survival and coronary-event rates to changes in coronary heart disease mortality: 10-year results from 37 WHO MONICA project populations. Monitoring trends and determinants in cardiovascular disease. Lancet 353:1547–1557

Yarnell JW (1998) The PRIME study: classical risk factors do not explain the several fold differences in risk of coronary heart disease between France and Northern Ireland. Prospective epidemiological study of myocardial infarction. QJM 91:667–676

Yarnell J, Yu S, McCrum E, Arveiler D, Hass B, Dallongeville J, Montaye M, Amouyel P, Ferrières J, Ruidavets JB, Evans A, Bingham A, Ducimetière P, PRIME study group (2005) Education, socioeconomic and lifestyle factors, and risk of coronary heart disease: the PRIME study. Int J Epidemiol 34:268–275

Yarnell JW, Patterson CC, Arveiler D, Amouyel P, Ferrières J, Woodside JV, Haas B, Montaye M, Ruidavets JB, Kee F, Evans A, Bingham A, Ducimetière P (2012) Contribution of lifetime smoking habit in France and Northern Ireland to country and socioeconomic differentials in mortality and cardiovascular incidence: the PRIME study. J Epidemiol Community Health 66:599–604

Wagner A, Simon C, Evans A, Ducimetière P, Bongard V, Montaye M, Arveiler D, PRIME Study Group (2003) Physical activity patterns in 50–59 year men in France and Northern Ireland. Associations with socio-economic status and health behaviour. Eur J Epidemiol 18:321–329

Ruidavets JB, Ducimetière P, Evans A, Montaye M, Haas B, Bingham A, Yarnell J, Amouyel P, Arveiler D, Kee F, Bongard V, Ferrières J (2010) Patterns of alcohol consumption and ischaemic heart disease in culturally divergent countries: the prospective epidemiological study of myocardial infarction (PRIME). BMJ 341:c6077

Dauchet L, Ferrières J, Arveiler D, Yarnell JW, Gey F, Ducimetière P, Ruidavets JB, Haas B, Evans A, Bingham A, Amouyel P, Dallongeville J (2004) Frequency of fruit and vegetable consumption and coronary heart disease in France and Northern Ireland: the PRIME study. Br J Nutr 92:963–972

Ducimetière P, Ruidavets JB, Montaye M, Haas B, Yarnell J, PRIME Study Group (2001) Five-year incidence of angina pectoris and other forms of coronary heart disease in healthy men aged 50–59 in France and Northern Ireland: the prospective epidemiological study of myocardial infarction (PRIME) study. Int J Epidemiol 30:1057–1062

Hess D, Keller HE, Oberlin B, Bonfanti R, Schuep W (1991) Simultaneous determination of retinol, tocopherols, carotenes and lycopene in plasma by means of high-performance liquid chromatography on reversed phase. Int J Vitam Nutr Res 61:232–238

Vuilleumier JP, Keck E (1989) Fluorimetric assay of vitamin C in biological materials using a centrifugal analyser with fluorescence attachment. J Micronutr Anal 5:25–35

Gey KF, Brubacher GB, Stähelin HB (1987) Plasma levels of antioxidant vitamins in relation to ischemic heart disease and cancer. Am J ClinNutr 45:1368–1377

Gey KF, Moser UK, Jordan P, Stähelin HB, Eichholzer M, Lüdin E (1993) Increased risk of cardiovascular disease at suboptimal plasma concentrations of essential antioxidants: an epidemiological update with special attention to carotene and vitamin C. Am J ClinNutr 57(5 Suppl):787S-797S

Mayland CR, Bennett MI, Allan K (2005) Vitamin C deficiency in cancer patients. Palliat Med 19:17–20

Hickenbottom SJ, Follett JR, Lin Y, Dueker SR, Burri BJ, Neidlinger TR, Clifford AJ (2002) Variability in conversion of beta-carotene to vitamin A in men as measured by using a double-tracer study design. Am J ClinNutr 75:900–907

Chai W, Maskarinec G, Franke AA, Monroe KR, Park SY, Kolonel LN, Wilkens LR, Le Marchand L, Cooney RV (2020) Association of serum γ-tocopherol levels with mortality: the multiethnic cohort study. Eur J ClinNutr 74:87–96

Parohan M, Anjom-Shoae J, Nasiri M, Khodadost M, Khatibi SR, Sadeghi O (2019) 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

Bastide N, Dartois L, Dyevre V, Dossus L, Fagherazzi G, Serafini M, Boutron-Ruault MC (2017) Dietary antioxidant capacity and all-cause and cause-specific mortality in the E3N/EPIC cohort study. Eur J Nutr 56:1233–1243

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

Wang X, Ouyang Y, Liu J, Zhu M, Zhao G, Bao W, Hu FB (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

Browne D, Williams MA, Maxwell AP, McGuinness B, Passmore P, Silvestri G, Woodside JV, McKay GJ (2019) Serum xanthophyll carotenoids are associated with estimated glomerular filtration rate in an aged cohort. Sci Rep 9:17068

Thies F, Mills LM, Moir S, Masson LF (2017) Cardiovascular benefits of lycopene: fantasy or reality? ProcNutrSoc 76:122–129

Jialal I, Norkus EP, Cristol L, Grundy SM (1991) Beta-Carotene inhibits the oxidative modification of low-density lipoprotein. Biochim Biophys Acta 1086:134–138

Alpha-Tocopherol, Beta Carotene Cancer Prevention Study Group (1994) The effect of vitamin E and beta carotene on the incidence of lung cancer and other cancers in male smokers. N Engl J Med 330:1029–1035

Browne D, McGuinness B, Woodside JV, McKay GJ (2019) Vitamin E and Alzheimer’s Disease: what do we know so far? ClinInterv Aging 14:1303–1317

Bates CJ, Hamer M, Mishra GD (2011) Redox-modulatory vitamins and minerals that prospectively predict mortality in older British people: the National Diet and Nutrition Survey of people aged 65 years and over. Br J Nutr 105:123–132 ((Erratum in: Br J Nutr 2013;110:1548))

Martín-Calvo N, Martínez-González MÁ (2017) Vitamin C intake is inversely associated with cardiovascular mortality in a Cohort of Spanish Graduates: the SUN Project. Nutrients 9:E954

Grosso G, Bei R, Mistretta A, Marventano S, Calabrese G, Masuelli L, Giganti MG, Modesti A, Galvano F, Gazzolo D (2013) Effects of vitamin C on health: a review of evidence. Front Biosci (Landmark Ed) 18:1017–1029

Toniolo P, Van Kappel AL, Akhmedkhanov A, Ferrari P, Kato I, Shore RE, Riboli E (2001) Serum carotenoids and breast cancer. Am J Epidemiol 153:1142–1147

Mullan K, Cardwell CR, McGuinness B, Woodside JV, McKay GJ (2018) Plasma antioxidant status in patients with Alzheimer’s Disease and cognitively intact elderly: a meta-analysis of case-control studies. J Alzheimers Dis 62:305–317

Mullan K, Williams MA, Cardwell CR, McGuinness B, Passmore P, Silvestri G, Woodside JV, McKay GJ (2017) Serum concentrations of vitamin E and carotenoids are altered in Alzheimer’s disease: a case control study. Alzheimers Dement 3:432–439

Jenab M, Slimani N, Bictash M, Ferrari P, Bingham SA (2009) Biomarkers in nutritional epidemiology: applications, needs and new horizons. Hum Genet 125:507–525

Zheng JS, Sharp SJ, Imamura F, Chowdhury R, Gundersen TE, Steur M, Sluijs I, van der Schouw YT, Agudo A, Aune D, Barricarte A, Boeing H, Chirlaque MD, Dorronsoro M, Freisling H, El-Fatouhi D, Franks PW, Fagherazzi G, Grioni S, Gunter MJ, Kyrø C, Katzke V, Kühn T, Khaw KT, Laouali N, Masala G, Nilsson PM, Overvad K, Panico S, Papier K, Quirós JR, Rolandsson O, Redondo-Sánchez D, Ricceri F, Schulze MB, Spijkerman AMW, Tjønneland A, Tong TYN, Tumino R, Weiderpass E, Danesh J, Butterworth AS, Riboli E, Forouhi NG, Wareham NJ (2020) Association of plasma biomarkers of fruit and vegetable intake with incident type 2 diabetes: EPIC-InterAct case-cohort study in eight European countries. BMJ 370:m219

Thông tin
Thông tin xuất bản

Springer Science and Business Media LLC

Thông tin tác giả